CHAPTER SIX
Eco-Evolutionary Dynamics
of Agricultural Networks:
Implications for Sustainable
Management
Nicolas Loeuille ,†,1, Sébastien Barot{, Ewen Georgelin ,†,
Grigorios Kylafis ,†, Claire Lavigne}
*Laboratoire EcoEvo, UMR 7625, UPMC, Paris, France
†
Laboratoire Ecologie des Populations et des Communautés, USC INRA 2031, Paris, France
{
Laboratoire BIOEMCO, UMR 7618, IRD, Paris, France
}
Laboratoire Plantes et Systèmes de culture Horticoles, UR1115, INRA, Avignon Cedex, France
1
Corresponding author: e-mail address: [email protected]
Contents
1. Introduction
2. Within Field, Applying Evolutionary Perspectives to the Selection of Agricultural
Species
2.1 General effects of domestication and selection
2.2 Beyond the one trait approach: Accounting for trade-offs
2.3 Adapting to local practices and conditions: The importance of diversity
2.4 Beyond individuals: The influence of selection processes on the community
and ecosystem context
3. Disturbances Due to Agriculture: Implications for Eco-Evolutionary Dynamics
Within Surrounding Ecosystems
3.1 Nutrient enrichment and its ecological and evolutionary consequences in
agricultural landscapes
3.2 Chemical warfare in agricultural landscapes: The ecological and evolutionary
consequences of pesticide use
3.3 Effects of altering species composition and relative abundance of species in
agricultural landscapes
4. Accounting for Spatial Heterogeneities: Dispersal, Fragmentation, and Evolution
in Agricultural Landscapes
4.1 Characteristics of agricultural landscapes, past, present and future
4.2 Consequences of agricultural landscape structure in terms of gene flow
4.3 Consequences of spatial modifications from a demographic point of view
4.4 Consequences of spatial structure for pairwise co-evolution
4.5 Beyond pairwise interactions: Consequences of eco-evolutionary dynamics
for community structure and composition
4.6 Land sparing versus land sharing, from an evolutionary point of view
Advances in Ecological Research, Volume 49
ISSN 0065-2504
http://dx.doi.org/10.1016/B978-0-12-420002-9.00006-8
#
2013 Elsevier Ltd
All rights reserved.
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5. Perspectives and Challenges
Acknowledgements
Appendix A. Evolution of the investment into nutrient uptake, effects on emergent
functioning
Appendix B. Mixing group selection and individual selection in co-evolutionary
models
Appendix C. Effects of enrichment on the control of biomass within a tri-trophic food
chain when the herbivore evolves
Appendix D. Eco-evolutionary dynamics in a plant–herbivore–predator confronted to
insecticides
Appendix E. Evolution of specialization rate of the pest and its ecological
consequences
Glossary
References
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Abstract
Community and ecosystem ecology are paying increasing attention to evolutionary
dynamics, offering a means of attaining a more comprehensive understanding of ecological networks and more efficient and sustainable agroecosystems. Here, we review
how such approaches can be applied, and we provide theoretical models to illustrate
how eco-evolutionary dynamics can profoundly change our understanding of
agricultural issues. We show that community evolution models can be used in several
contexts: (1) to improve the selection of agricultural organisms within the context of
their ecological networks; (2) to predict and manage the consequences of agricultural
disturbances on the ecology and evolution of ecological networks; and (3) to design
agricultural landscapes that benefit from network eco-evolutionary dynamics, but without negative impacts. Manipulation of landscape structure simultaneously affects both
community ecological dynamics (e.g., by modifying dispersal and its demographic
effects) and co-evolution (e.g., by changing gene flows). Finally, we suggest that future
theoretical developments in this field should consider appropriate co-evolutionary
models and ecosystem services.
1. INTRODUCTION
Models and experiments in ecology have increasingly incorporated
evolutionary dynamics in the context of community structure and ecosystem functioning (Agrawal et al., 2012; Brännström et al., 2012; Loeuille
and Loreau, 2009). Such models have been coined ‘community evolution
models’ (Brännström et al., 2012; Loeuille and Loreau, 2009). They link
evolutionary processes driven by individual fitness to emergent properties
of ecological networks, linking small-scale processes to large-scale patterns.
Eco-Evolutionary Dynamics in Agroecosystems
341
Evolutionary dynamics affect important structural attributes of ecological
communities, such as connectance or the number of trophic levels of a food
web, via the evolution of body size (Loeuille and Loreau, 2005) or adaptive
foraging (Beckerman et al., 2006). Similarly, the structure of mutualistic networks (e.g., plant–pollinator or plant–seed disperser) largely depends on the
co-evolution of partner species (Bascompte et al., 2006; Nuismer et al.,
2012). Evolution also modifies ecosystem functioning, in ways that are particularly relevant to agricultural systems: biomass, productivity, nutrient
cycling or ecosystem sustainability are all potentially affected. It can also produce counter-intuitive effects (Abrams and Matsuda, 2005) and the interplay
of ecological and evolutionary dynamics (hereafter, eco-evolutionary dynamics) changes the distribution of nutrients within ecosystems (Boudsocq et al.,
2011), the way nutrients are recycled (De Mazancourt et al., 2001; Loeuille
et al., 2002) and their spatial distribution (Loeuille and Leibold, 2008a). Evolution also constrains the resilience of ecological assemblages (Kondoh, 2003;
Loeuille, 2010a, b), thereby affecting the sustainability of the system.
Agricultural development is based on a selective process (Gepts, 2004), so
it is particularly important to incorporate rigorous evolutionary thinking
into it. Human populations have long chosen species and favoured traits that
increase the productivity of cultivated organisms or make their cultivation
easier. Because selective processes are at the heart of agricultural developments, it should be possible to implement current progresses linking trait
evolution with emergent properties of ecosystems, to improve selection
and the management of agricultural landscapes.
An immediate difficulty, however, results from differences in the ways
selective processes are considered in ecological versus agricultural contexts.
Because evolutionary concepts are often phrased differently in ecology and
agriculture, precise definitions of key concepts are necessary (see Glossary).
Selection in agriculture is driven by the choice, conscious or otherwise, of
cultivated species and of their characteristics (Meyer et al., 2012). Such a
choice is often based on total biomass or yield (Perales et al., 2004;
Vigouroux et al., 2011) and the process de facto relies on a group selection
criterion (Denison et al., 2003, but see Duputié et al., 2009). In contrast,
evolutionary ecology usually considers phenotypic changes based on individual or gene fitness (Dieckmann and Law, 1996; Fisher, 1930;
Hamilton, 1964). Thus, fitness in community evolution models can be complex, due to the need to account for multispecies assemblages and interaction
networks (Ito and Ikegami, 2006; Loeuille and Loreau, 2005), as well as various disturbance scenarios (Loeuille and Loreau, 2004; Norberg et al., 2012).
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Here, we will discuss what agriculture can learn from these community
evolution models, as well as associated experimental and empirical works in
evolutionary ecology. Particularly, are there lessons to be learned to reconcile economic goals (e.g., an appropriate level of food production) with the
desire to conserve ecological networks? A few reviews have already shown
how evolutionary arguments can be applied to agricultural systems
(Denison, 2012; Denison et al., 2003; Thrall et al., 2011), by providing case
studies and examples of the many ways in which we can use evolutionary
ecology to design a better agriculture. Here, although some arguments will
be based on single-species evolution studies, we will focus on tackling the
links between evolutionary and community contexts, drawing extensively
on community evolution models and ecological theories.
We divide our central theme into two parts. (i) we ask how do community evolution models help us to guide the choice of cultivated species, traits
or genes for a sustainable agriculture? This requires the assessment of how
these choices affect the co-evolution of species within associated ecological
networks and their consequences in terms of yield and sustainability. (ii) we
ask, can we use community evolution models to predict the consequences of
disturbances due to agriculture on surrounding ecosystems? Such disturbances include fertilization, pesticide use, changes in species community
composition and landscape modifications. Empirical observations suggest
that each of these disturbances has far reaching implications for the ecology
and evolution of the natural communities that abut agricultural systems
(Klein et al., 2007; Tscharntke et al., 2005). We also ask whether current
ecological and evolutionary theory can provide guidelines to limit the consequences of these disturbances and preserve ecological networks.
It is necessary to point out that agricultural systems vary considerably in
how they create heterogeneities and disturbances (Malézieux, 2011; Massol
and Petit, 2013, Chapter 5 of this volume). From a low-intensity gatherer
mode of farming to intensive industrialized agriculture, a continuum exists
along which disturbances increase. Malézieux (2011) distinguishes ‘traditional agriculture’ from ‘intensive agriculture’ and warns that much of the
surface currently occupied by agriculture is not, despite common misconceptions, intensively managed. He also proposes to manage agriculture
through ‘ecological intensification’, relying on services provided by ecological networks (Doré et al., 2011; Malézieux, 2011). Here, we will try to state
for each example whether it is applicable to intensive or traditional agriculture, within agricultural fields or in surrounding ecosystems.
Justifications for questions (i) and (ii) can take several forms. One
important motivation is the conservation of species diversity. Agricultural
Eco-Evolutionary Dynamics in Agroecosystems
343
development has triggered marked declines in species diversity (Robinson
and Sutherland, 2002), although some species, such as those associated
with downland, heathlands and other semi-natural or farmed landscapes,
have benefited (Eriksson, 2012). The maintenance of (at least some)
diversity is important, not only for the intrinsic value of species, but also
because it generally enhances ecosystem functioning (Loreau et al., 2001),
and another important justification emerges from this point. When ecosystems within the field and in the surrounding landscape are functioning
effectively, human populations receive important economical benefits,
commonly called ‘ecosystem services’ (Costanza et al., 1997; Raffaelli
and White, 2013; Bohan et al., 2013, Chapter 1 of this volume). Several of these ecosystem services directly benefit agriculture, such as pollination (Klein et al., 2007; Tscharntke et al., 2005), biological control of
pests by pathogens and predators (Crowder et al., 2010; Macfadyen et al.,
2011; Thrall et al., 2011) and the efficient recycling of nutrient and maintenance of soil fertility (Young and Crawford, 2004). Community assembly and co-evolution have built the ecological networks that provide
these services, so community evolution models should be able to explain
the impact of agriculture on them.
We organize the text in three different parts, focusing on evolutionary
ecology within fields, around them, and then across the whole agricultural landscape. In the first part, within agricultural fields, we ask how
evolutionary ecology in general and community evolution models in particular can guide the choice of cultivated species and of their traits, to
account simultaneously for agricultural yield and ecological sustainability.
In the second part, concerning adjacent ecosystems, we propose that
community evolution models can be used to discuss the consequences
of agricultural disturbances on the ecology and evolution of natural networks. The third part, integrating agricultural fields and their adjacent
ecosystems, investigates how spatial evolutionary models may guide the
landscape management of agricultural systems. In each part, we build
the arguments by increasing levels of organizational complexity, moving
from a species perspective (often the cultivated species), to pairwise interactions, then to community structure and finally to ecosystem functioning. A table summarizing main arguments and key references introduces
each part. At several junctures, we illustrate our statements by developing
new models tightly focused on a key question. The main result of each
model is then presented in a box, while detailed hypotheses and analyses
are provided in appendices. In the fourth and final part, we finish by indicating possible future developments.
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2. WITHIN FIELD, APPLYING EVOLUTIONARY
PERSPECTIVES TO THE SELECTION OF AGRICULTURAL
SPECIES
2.1. General effects of domestication and selection
Domestication is the outcome of artificial selection that leads to increased
adaptation of plants and animals to cultivation by humans (Gepts, 2004).
The most detailed studies concern crop domestication (Gepts, 2004;
Harlan et al., 1973) and we will focus on this literature here as a complete
review is beyond the scope of the present chapter. Instead, we will focus on
the main phenotypic traits that have been selected via domestication then
show that most selected strategies would perform poorly in natural selection
settings. Inevitably, such a selection procedure requires extensive use of continued inputs to maintain the cultivated species and traits, posing a sustainability problem.
About 2500 plant species have been domesticated (Meyer et al., 2012) in
an ongoing process that is rooted in the transition from hunter-gatherers to
settled agriculture during the Neolithic. The first steps of domestication
were probably unconscious: wild plants were simply translocated across
newly man-made environments, which altered selective pressures. However, further selection of varieties has probably been conscious for a very
long time. Artificial selection inspired much of Darwin’s theory of evolution
by natural selection (Darwin, 1859) and he later dedicated a whole book to
this subject (Darwin, 1868) after being struck by the strength and pace of
artificial selection and the obvious link it makes between present selective
pressures and subsequent evolution.
Many different traits are often selected in several domestication events,
defining a domestication syndrome (Gepts, 2004; Harlan, 1992; Meyer
et al., 2012; Purugganan and Fuller, 2009). In cereals, two types of traits
are essential: an ability to germinate deep in the soil in open, disturbed habitats
(e.g., large seeds, loss of dormancy) and traits that facilitate harvesting (e.g.,
non-shattering seeds, maturation synchrony, reduced branching, and resistance to tilling). Domestication also involved the loss of secondary metabolites, allowing seeds or fruits to taste better or to be more easily digested
(Meyer et al., 2012). Changes in the reproductive strategy are frequently
encountered, from outcrossing to selfing or from sexual to vegetative reproduction. Such changes made further selection easier, as they increase reproductive isolation and facilitate the rapid fixation of selected traits.
345
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Take home messages and key references for section 2
Agriculture and crop
Ecology and evolutionary
ecology
Section breeding
References
Meyer et al.,
2012
Purugganan
and Fuller,
2009
Section Domestication and crop
2.1
breeding is a diversified
evolutionary process
impacting many plant
traits, favouring
easy cultivation and higher
yields
Domestication and artificial
selection have selected traits
that could not evolve
through natural selection,
due to differences in
selective regimes
Section Crop breeding often
involves group selection
2.2
based on collective
properties of crops such as
yield. Such a selection has
favoured fast-growing crops,
incurring costs in terms of
competitive abilities
Existing allocation trade-offs Denison
between growth rates and et al., 2003
many different traits (e.g.,
competitive ability,
defences) constrain the
evolution of these traits
Section Crop breeding has resulted
2.3
in some homogenization of
crop plants associated with
the development of
agricultural practices
allowing homogeneous
environmental conditions
through high inputs. An
unsettled controversy exists
regarding the degree of
desired local adaptation of
crops to different
agricultural practices.
Modern crop breeding
has led to a drastic reduction
in within field genetic
diversity
Natural selection selects
diversified strategies as soon
as environment is not totally
homogeneous.
Ecology increasingly views
genetic diversity as an
important factor for
ecosystem functioning
Thrall and
Burdon,
2003
Murphy
et al., 2007
Van Bueren
et al., 2008
Crutsinger
et al., 2006
Section Results from community
2.4
evolution models suggest
that crop breeding could be
constrained by trade-offs
between yield and
sustainability
Allocation and ecological
trade-off are likely to result
in trade-offs at the
community or ecosystem
scale, including
between different
ecosystem services
Fussman
et al., 2007
Strauss et al.,
2002
Box 6.1
Box 6.2
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The selective process changes widely among agricultural systems: in traditional cropping systems, farmers manage local landraces based on networks
of seed exchanges (Pautasso et al., 2013), whereas since the end of the nineteenth century, selection has been increasingly undertaken by specialized
farmers, public organisms and private companies. This specialization of roles
has allowed the development of sophisticated methods using the latest developments of biological sciences: genetics, molecular markers and biotechnologies, and the development of a global multinational agroindustry (Dennis
et al., 2008; Pennisi, 2008). Such modern changes in selection methods are
intertwined with the development of modern agriculture based on mechanization, and the use of fertilizers and pesticides.
Crop breeding has targeted varieties with higher yields and three major
staple crops—wheat, rice, and corn—provide about 45% of human-ingested
calories worldwide. The grain yield of these cereals doubled during the
twentieth century, modern crop breeding methods playing a key role in this
increase (Richards, 2000). A trait related to yield, the harvest index (ratio of
the grain biomass to the whole aerial biomass), has also doubled, reaching
values as high as 0.5 in most cereals (Hay, 1995; Richards, 2000). Increases
in the harvest index have been obtained by selecting increased allocation to
reproductive parts and decreased allocation to leaves and stems. The development of dwarfed varieties during the Green Revolution has led to shorter
and stiffer stems that are less sensitive to falling over, or lodging (caused by
bending or breakage of the stem or root problems), even at high fertilization
rates. Prior to the 1970s, these trends were mostly driven by ‘defect elimination’ and ‘selection for yield’ (Donald, 1968). The first corresponds to
removing major flaws, such as weak straws for cereals or fragile skins for
tomatoes. The second is based on the need to increase production, regardless
of the plant traits involved (Donald, 1968).
Harvest indices have seemingly plateaud (Hay, 1995), and crop breeding
now targets traits that appear most promising to increase yield: resistance to
pests and pathogens and to unfavourable conditions (Witcombe et al., 2008),
such as drought (Pennisi, 2008) or saline soils (Richards, 1992). This is crucial for exploiting new, less favourable, land and to cope with global changes
(e.g., climate change, soil degradation). Other selected traits focus on the
efficient acquisition and recycling of resources. Such research aimed at optimizing root systems (De Dorlodot et al., 2007) and at increasing their capacity to take up phosphorus (Gahoonia and Nielsen, 2004). Artificial selection
of nutrient use also goes beyond individual plant traits to consider the complex relationships with soil microbial communities. Nutrient management is
Eco-Evolutionary Dynamics in Agroecosystems
347
a key point for future agricultural sustainability because: (1) mineral fertilizers are not produced sustainably (phosphorus is dug in mines, nitrogen
is industrially fixed using fossil fuels as an energy source); (2) fertilizers leak
from agroecosystems, altering functioning and contributing to greenhouse
gas emissions (e.g., N2O) (Vitousek et al., 1997).
Artificial selection could also aim to increase photosynthetic rates (Long
et al., 2006; Richards, 2000), but when expressed per unit land area these
have mostly increased through inputs (irrigation, inorganic fertilizer).
Whether higher photosynthetic rates through crop breeding are possible
is still hotly debated (Denison et al., 2003), and it would require manipulation of many genes simultaneously, while most modern crop breeding usually targets just a few genes.
Domestication and artificial selection alter the composition of communities at all spatial scales: out of 2500 domesticated species, 20 major crops
cover about 12% of the land surface (Leff, 2004), while the worldwide number of seed plant species is estimated at about 260,000. About 22% of continental surfaces are used as pastures and rangelands planted to some extent
with domesticated grasses (Glémin and Bataillon, 2009). In addition to
reducing species diversity, modern agriculture and crop breeding have
developed a restricted number of pure or hybrid lines so that genetic diversity is drastically reduced, both locally and globally (Haudry et al., 2007).
Reduced genetic diversity can happen early in the domestication due to bottlenecks, with early farmers using a limited number of plant individuals as
progenitors (Reif et al., 2005). A second step in the genetic erosion occurred
when pure or hybrid lines were preferred to local landraces. Genetic diversity in bread wheat cultivated in a region of France, for instance, has halved
since 1878 (Bonneuil et al., 2012). On the contrary, farmers in traditional
systems often increase genetic diversity through the creation of local landraces adapted to different local uses, tastes, agricultural practices, and environments (Elias et al., 2001; Pautasso et al., 2013).
Can evolutionary ecology shed new light on the whole process of
domestication and crop breeding and can it improve crop breeding and
the sustainability of agriculture? Evolutionary arguments are not always present in the recent crop breeding literature (but see Harlan et al., 1973). For
example, whole review papers on crop breeding do not use the term ‘evolution’ in its Darwinian sense (Good et al., 2004; Zhang, 2007). Only some
relatively recent initiatives have appealed to more evolutionary-oriented
thinking in agriculture and crop breeding (Denison, 2012; Denison et al.,
2003; Gepts, 2004; Thrall et al., 2011).
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Nicolas Loeuille et al.
Artificial selection has led to species and varieties that depend on humans
to reproduce, as they have lost the suitable reproduction and dispersal strategies, and to grow, with the need for nutrient addition and physical protection.
It tends to produce organisms whose traits would usually be disfavoured by
natural selection. The loss of traits allowing independent reproduction is only
possible because artificial selection is based on group level criteria, such as yield
(Denison et al., 2003). Such traits incur low individual fitness and would be
expected to disappear through natural selection. For instance, non-shattering
stems would be disfavoured in nature, because seed would not fall to the ground, but are systematically selected in harvesting systems where humans want
to collect the seed before the seed is lost (Harlan et al., 1973). In some cases,
improving crop varieties has reversed the effects of past natural selection.
Thinking of natural selection therefore allows an a priori assessment of future
crop breeding avenues: Denison et al. (2003) hypothesize that natural selection is likely to have already optimized the major physiological pathways of
plants (e.g., photosynthesis), so significant further improvement through crop
breeding is unlikely.
Because the units of selection are different in artificial and natural selection, most evolutionary models developed in plant ecology have no straightforward links with crop breeding. Some theoretical models study the
evolution of traits relevant to crops, including growth rate, nutrient uptake
efficiency (Boudsocq et al., 2011), defences against herbivores (Loeuille and
Leibold, 2008a), seed size (Geritz et al., 1999), plant height (Falster and
Westoby, 2003), and shoot–root ratio (Vincent and Vincent, 1996). However, many crop traits are entirely anthropocentric and essentially irrelevant
in natural systems, such as those linked to the taste of the food or allowing an
easier harvest (e.g., non-shattering grains).
2.2. Beyond the one trait approach: Accounting for trade-offs
While we have listed above a list of traits targeted by artificial selection, they
should not be considered in isolation. Trade-offs may cause negative correlations between two or more traits, so that considering just one does not give
an adequate description of selection dynamics. This concept is at the very
heart of most evolutionary models and the influence of trade-offs has been
systematically investigated in this context (De Mazancourt and Dieckmann,
2004; Loeuille and Loreau, 2004). Trade-offs also exist between traits relevant to artificial selection and their analysis is critical in terms of agricultural
Eco-Evolutionary Dynamics in Agroecosystems
349
management, although they are often overlooked in such a context
(Denison, 2012; but see Thrall, 2013).
Trade-offs can emerge due to allocation constraints of resources, time, or
space. For instance, resources allocated to growth cannot be used for reproduction or to produce defensive compounds against herbivores or pathogens
(Herms and Mattson, 1992). In the same vein, opening stomata allows photosynthesis but increases losses of water by evapotranspiration. We list below
the trade-offs that are commonly considered in evolutionary ecology and
that are relevant to agroecosystems.
In ecology, selection for yield could be related to the r–K theory (Pianka,
1970), which can emerge from existing trade-offs between individual traits
(Rueffler et al., 2006a) High yield, fast growth rates (r strategies) are thus
traded-off against traits that improve competitive ability (K strategies), such
as large size, long generation time, so that crop breeding is likely to produce
poor competitors (Denison et al., 2003; Donald, 1968; Weiner, 2004). Crop
individuals have higher yield because they spare the resource otherwise
required to interfere efficiently with other individuals. If only conspecifics
are present, having poor-competitor r strategists in turn decreases competition,
and yield is further increased (Donald, 1968). It also requires a release from competition with wild plants. This type of selection is therefore dependent on tillage
and herbicides. The loss of competitiveness favours short stems (dwarfed varieties), upright and erect leaves and lower individual leaf surface area, whereas
natural selection usually selects against these traits.
Recognition of the growth/competition trade-off raises the question of
the optimal strategy for achieving more sustainable agriculture. In a succession context, fast-growing r strategies are progressively replaced by K strategies. In agriculture, artificial selection maintains r strategies in the field.
From an evolutionary and ecosystem ecology point of view, this maintenance at early stages of succession cannot be a sustainable strategy for two
reasons. First, this situation is far from equilibrium, so that the system is susceptible to abrupt changes, low resilience and invasions (Odum, 1953). Second, this maintenance of r strategies requires large inputs. Lower-yielding
phenotypes would allow lower rates of fertilization, as suggested by a theoretical model (Zhang et al., 1999) and experiments (Gersani et al.,
2001). They could also tolerate cultivation on marginal soils or under
stressed conditions.
Growth rate is also often negatively correlated with defences against herbivores or pathogens, as resources allocated to growth cannot be used for
both purposes (Herms and Mattson, 1992). Also, the allocation of mineral
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Nicolas Loeuille et al.
nutrient to roots or leaves should attract pathogens and herbivores (Mattson,
1980; White, 2005). Most often, in nature, intermediate strategies along the
growth/defence trade-off are selected (De Mazancourt et al., 2001; Loeuille
and Leibold, 2008a; Loeuille and Loreau, 2004; Loeuille et al., 2002). Crops
selected on yields in the absence of pests are again at one extreme of the continuum. They clearly depend on inputs (pesticides, fungicides) to compensate, again raising sustainability issues.
Trade-offs also limit the improvements that are possible through crop
breeding, suggesting great difficulties in enhancing photosynthetic rate
(Denison et al., 2003). Without accounting for trade-offs, some scientists
have proposed the breeding of a Green Super Rice (Zhang, 2007), with
increased: (1) resistance to herbivores, (2) resistance to drought, (3) nutrient
use efficiency, (4) grain quality, and (5) yield. Most of these traits are likely to
be linked via antagonistic constraints, for instance due to resource allocation.
As a more general illustration of the lack of consideration given to these constraints, we have searched ISI Web of Science using the terms ‘crop breeding’ and ‘trade-off’ (in keywords, title, and abstract) and only found
27 articles. Ideally, for any selection procedure, existing trade-offs among
targeted traits should be assessed before deciding which combination is more
desirable, and indeed feasible, using a hierarchical set of criteria (yield, crop
quality, sustainability of the production, etc., e.g., Quilot-Turion
et al., 2012).
In extreme cases, targeting one trait can lead to the loss of others (Ellers et al.,
2012; Ostrowski et al., 2007), and reduced genetic diversity in crop plants can
increase the likelihood of such losses. Examples of traits that are threatened by
modern crop breeding include: (1) the ability to interact with mycorrhizae
(Zhu et al., 2001), (2) symbiotic nitrogen fixation (Kiers et al., 2007), (3) inhibition of nitrification (Subbarao et al., 2006), and (4) the ability to benefit from
earthworm activities (Noguera et al., 2011). These four examples suggest that
trade-off choices have consequences for interspecific interactions, and, by
extension, ecological networks. Artificial selection of higher growth rates
may therefore have a general effect of decreasing benefits from interactionrelated traits. In natural ecosystems, plants rely heavily on such traits, which
evolved in complex four-dimensional settings involving soil organic matter
and interactions with micro- and macro-organisms (Puga-Freitas et al.,
2012; Shahzad et al., 2012). Selection of such traits can play a critical role for
a more sustainable management of agriculture, as once interaction traits are present, ecological processes can partly replace artificial inputs, via ecological intensification (Doré et al., 2011; Malézieux, 2011).
Eco-Evolutionary Dynamics in Agroecosystems
351
Many trade-offs have already been documented in crop plants:
between seed size and seed number (Sadras, 2007), between nutrient
use efficiency and nutrient stress tolerance (Maia et al., 2011), between
water and phosphorus acquisition (Ho et al., 2005) or between performance at low and high salinity levels (Richards, 1992). The growth/
defence trade-off seems to be widespread in wild plants (Lind et al.,
2013) and has been investigated in a number of crop plants (e.g., tomato:
Le Bot et al., 2009; sunflower: Mayrose et al., 2011), although no general
overview exists for the latter. There is an emerging consensus, however,
that fertilization affects herbivores (Butler et al., 2012) and pathogens
(Huber and Watson, 1974), as well as plant growth, in agricultural systems. This trade-off is thus critical as it may provide an important key
to conceive alternatives to pesticide use.
The potential trade-off between nutrient uptake, at high and low concentrations of fertilizer, is controversial both for wild plants and for crops
(Craine, 2009), and results to date have produced little or no supporting evidence (Hasegawa, 2003; Reich et al., 2003), suggesting that the same crop
varieties may be cultivated regardless of the fertilization practice.
This assessment of costs, and of trade-offs in general, is central to evolutionary ecology and for agronomy. In ecology, the results of community evolution models depend mostly on the shape of trade-offs, but such information
is often unavailable (De Mazancourt and Dieckmann, 2004; Loeuille and
Loreau, 2004). Artificial selection in agriculture could provide very important
data to address this gap, creating a synergy between the two disciplines.
2.3. Adapting to local practices and conditions: The
importance of diversity
Diverse conditions, in space or time, typically favour a diversification of
strategies through natural selection (Thrall and Burdon, 2003; Thompson,
1999), unless strong homogenizing are operating via high gene flow impeding local specialization (Harrison and Hastings, 1996; Day, 2001; Loeuille
and Leibold, 2008b; Urban et al., 2008), or if generalists are equally fit as
specialists, regardless of environmental conditions. This last condition
implicitly assumes an absence of trade-off. These conditions are very stringent, so that diversification due to environmental variation is expected to
happen in most natural conditions.
This contrasts markedly with the situation in intensive agricultural systems, with a few species and a low genetic diversity. From an evolutionary
point of view, this homogenization of cultivated plants can be interpreted as
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Nicolas Loeuille et al.
either we have indeed managed to select highly generalist no-cost varieties,
or the heterogeneity of conditions in which crops grow is insufficient to support many specialized varieties. The second explanation seems a better fit to
our understanding of agricultural systems, for several reasons. First, a temporal correlation exists between diversity decline of cultivated plants and
homogenization of their growing conditions, which is obtained by tillage,
herbicides and pesticides that remove biotic interactions, while irrigation
and mineral fertilization smooth out variations in resource conditions.
A more sustainable agriculture would require management that changes
modern agricultural practices and crop breeding approaches simultaneously
(Tilman, 1999), but because both belong to the same technological regime,
this creates inertia that impedes the development of alternative strategies
(Vanloqueren and Baret, 2009).
A direct corollary is that more sustainable crop varieties should fit better
to their local environment and practices. Interactions between genotypes
and environmental conditions determine crop performance (Van Bueren
et al., 2008), and differences among varieties have been found for systems
where there is variation in intercropping practices (O’leary and Smith,
1999), mineral fertilization (Atlin and Frey, 1990; but see Hasegawa,
2003), or soil salinity (Kelman and Qualset, 1991). Yields of 35 genotypes
of soft white winter wheat were compared between organic and conventional practices, and a significant interaction between the genotype and
cropping system was evident in four out of five locations (Murphy et al.,
2007). This suggests that varieties to be used in organic farming should be
selected for under the conditions of organic farming (Przystalski et al.,
2008), whereas at present it currently largely relies on ‘conventional’ varieties. Breeding particular varieties for this type of agriculture could increase
yields and improve organic agriculture sustainability (Wolfe et al., 2008).
Since a better adaptation to local environments and practices should enhance
sustainability and yields, such a strategy should inevitably be favoured,
although the costs entailed by such local adaptation also need to be
accounted for, such as those related to economies of scale, labour, agronomic
management, and crop handling.
The loss of genetic diversity of cultivated organisms is detrimental to agriculture sustainability because it limits the scope of potential future evolution
(Dieckmann and Law, 1996; Lande, 1979). This, in addition to the fact that
farmers in intensive systems no longer produce their own seeds,
will compromise future local adaptation in crops. In traditional cropping systems, farmers adjust the landraces to suit their own farm. It may be argued that
Eco-Evolutionary Dynamics in Agroecosystems
353
modern tools of artificial selection (e.g., genetic engineering) can offset the
lack of on-farm local evolution, but local adaptation involves many, often
unknown, niche dimensions, and understanding its significance requires a predictive framework we still lack. In traditional agriculture, on the other hand,
on-farm selection and seed exchange networks allow the necessary evolution
of crops in the face of global change (Bellon et al., 2011) and the evolution of
resistance to pathogens (Paillard et al., 2000).
Mechanisms identified from ecological biodiversity-ecosystem functioning studies also suggest how diversity loss can be detrimental to agricultural
sustainability. In natural ecosystems, higher plant species diversity produces
higher biomass, primary production, as well as more resilient systems
(Loreau et al., 2001). Different species react to environmental variations,
often in uncorrelated ways, which decreases the overall variance of the community (Yachi and Loreau, 1999). This ‘portfolio’ mechanism, postulated
for species diversity, also applies to genetic diversity (Vellend and Geber,
2005). Genetic diversity within species also influences ecosystem functioning (Crutsinger et al., 2006; Kotowska et al., 2010), and in agroecosystems,
for instance, a mixture of genotypes with different resistance levels may
impede a pathogen outburst by reducing the overall risk of contamination
(Zhu et al., 2000; Bohan et al., 2013, Chapter 1 of this volume).
2.4. Beyond individuals: The influence of selection processes
on the community and ecosystem context
Choices of domesticated species and artificial selection of their traits will
ultimately affect the overall structure of ecological networks. Indeed, the
selection imposed on cultivated organisms, often the dominant species
of their ecosystem, affects interspecific interaction in multiple ways. We
previously described trade-offs based on allocation costs, but while these
are undoubtedly important drivers of the evolution of some traits
(Herms and Mattson, 1992), the evolution of other traits incurs a different
type of cost. They may be constrained by the balance of various ecological
interactions (thereafter, ecological costs), rather than by energy allocation
within individuals.
Strauss et al. (2002) propose that anti-herbivore defences can have different allocation and/or ecological costs. Importantly, ecological costs
directly link trait selection to community aspects. For instance, MüllerSchärer et al. (2004) suggest that although some phenolic compounds are
effective against generalist herbivores, they may attract specialists. In principle, a plant species can then be invasive simply because their specialists are
354
Nicolas Loeuille et al.
absent, reducing the costs of these defences to zero. Evolution of defences
that incur ecological costs affect herbivore insect communities in complex
ways (Courtois, 2010), and they can also affect higher trophic levels or
mutualistic species. In tobacco plants, nicotine compounds, usually considered to be primarily selected as herbivore defences (Krieger et al., 1971), are
negatively linked to the pollinator reliance of the plant (Adler et al., 2012).
Defences also affect nectar quality, so that herbivore repulsion is traded-off
against pollinator attraction (Adler and Bronstein, 2004). Some volatile
compounds serve as a defence but they can also act as cues for herbivore
behaviours, leading to attraction to damaged plants for example, and signals
to insects at higher trophic levels and pollinators (Poelman et al., 2008; Van
Zandt and Agrawal, 2004; Xiao et al., 2012). Artificial selection can directly
modify defensive traits (Carrière et al., 2010) and domestication often
involves modification of palatability or digestibility of the cultivated organism (Meyer et al., 2012). This has indirectly selected against secondary metabolic compounds that are used for defence. How a modification of these
defences affects the surrounding ecological network will, in turn, depend
on the ecological costs associated with these traits.
The importance of ecological trade-offs goes beyond insect communities, as other taxa and soil maintenance and recycling processes are also
involved. Tannin production, again a classical defensive compound, slows
down litter recycling by affecting the soil microbial loop (Grime et al.,
1996; Whitham et al., 2003). Community evolution models also suggest that
defences affect recycling processes via the herbivore loop (De Mazancourt
et al., 2001). Defences could decrease root association with mycorrhizae,
impairing the plant’s ability to take up mineral nutrients (de Roman
et al., 2011). Plant defensive traits may therefore be linked to the long-term
maintenance and recycling efficiency of soils, a feature that underpins the
sustainability of agricultural yields (Malézieux, 2011). More recently, an
experimental study has even shown that defences may be traded-off against
competitive ability (Agrawal et al., 2012), thereby coupling two traditionally
separate issues in agriculture: competition from weeds and control of pests.
Community evolution models illustrate ways in which evolution under
ecological costs can affect network properties. For instance, Loeuille and
Leibold (2008a) introduced a model in which two defensive strategies are
incorporated, one incurring an allocation cost and the other having an ecological cost. Because of ecological costs, under high nutrient conditions,
evolution of defences within the food web decreases species diversity and
the network also becomes more compartmentalized, with well-separated
Eco-Evolutionary Dynamics in Agroecosystems
355
food chains. Evolution constrained by ecological costs is also usually less positive for community resilience than when it is constrained by allocation costs
(Loeuille, 2010a). While such models suggest that ecological costs can have
considerable implications for community structure and stability, empirical
data to determine their consequences in an agricultural context are scarce.
Recent observations on rice, however, indicate that such implications can
be far-reaching (Xiao et al., 2012), as artificial selection of anti-herbivore
defensive strategies may indeed modify the structure and interactions of
the complete insect community, including parasitoids and predators. The
direct implementation of defensive traits in the absence of an assessment
of ecological costs for the maintenance of associated ecological networks
should therefore be treated with caution.
Evolution also affects ecosystem functioning and services (Fussman et al.,
2007), and, as an example, selection for the high yield and fast-growing strategies favoured in agriculture can lead to a ‘tragedy of the commons’, in
which evolution of acquisition of shared resources leads to the overexploitation and eventual extinction of these resources (Hardin, 1968) with
negative consequences for the sustainability of the system.
Emergent properties of the system such as biomass or mineral nutrient
availability are affected by the evolution of such traits in complex ways
(Boudsocq et al., 2011; Loeuille et al., 2002). For example, in the model
by Boudsocq et al. (2011) (see also Box 6.1), plant evolution of nutrient
uptake may lead to three contrasting evolutionary outcomes depending
on costs: (1) an evolutionary equilibrium is reached, (2) evolution negatively
affects the population viability, and (3) accumulation of mineral nutrient,
eventually followed by a switch to another limiting nutrient or factor. From
an agricultural perspective, only option (1) is sustainable. Outcome (2)
shows how evolution of plant strategy can affect biodiversity maintenance,
while outcome (3) highlight how it can have important consequences for
ecosystem functioning (here, changes in the limiting nutrient).
Let us focus on the first case, evolutionary equilibrium, whereby natural
selection leads to intermediate rates of nutrient uptake at which the availability of mineral nutrient is minimal and the selected strategy does not maximize primary productivity or plant biomass. Modifying the model by
Boudsocq et al. (2011) to account more closely for artificial selection
(Box 6.1) and using primary productivity (yield, a common target for crop
breeding) as a criterion for selection then leads to higher mineral nutrient
availability accompanied by a faster rate of loss from the system, which creates a sustainability cost.
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BOX 6.1 Natural selection, artificial selection, and the
functioning of ecosystems
The model (Boudsocq et al., 2011) is based on a simple representation of nutrient
cycling between three compartments (primary producers, dead organic matter,
and limiting mineral nutrient) in an open ecosystem (see the detail of model in
Appendix A). Nutrient availability is strictly determined by the quantity of mineral
nutrient. Nutrient losses occur from the mineral nutrient pool, due to diffusion. To
predict the evolution of investment into nutrient uptake, we use the adaptive dynamics framework (Dieckmann and Law, 1996; Geritz et al., 1999). We consider a trade-off
between nutrient uptake and plant nutrient turnover due to root and leaf mortality.
The existence of this trade-off is supported by many mechanisms and observations.
For example, a higher investment into the root system to increase nutrient uptake
may (1) decrease the allocation of resources to defences against herbivores
(Herms and Mattson, 1992), (2) increase the mineral nutrient concentration in the
plant biomass which stimulates litter decomposition (Endara and Coley, 2011), (3)
require the production of many thin roots with a high turnover (Eissenstat et al., 2000).
Three types of evolutionary dynamics are possible depending on the tradeoff shape: (1) evolution of plant traits lead to an accumulation of nutrient so that
another nutrient type eventually becomes limiting, (2) evolution leads to a runaway towards higher uptake of nutrient, which asymptotically leads to plant
extinction, (3) an evolutionary equilibrium is reached with an intermediate investment in nutrient uptake. Analytical computations show that the availability of
mineral nutrient always decreases along evolutionary dynamics. Neither the biomass of primary producers nor primary productivity are maximized at the evolutionary equilibrium (Boudsocq et al., 2011).
Focusing on cases that lead to an evolutionary equilibrium, we illustrate these
results in Fig. 6.1, that shows how two compartments (mineral nutrient pool, plant biomass) and primary productivity change depending on the value of the evolving trait s,
the investment into nutrient uptake. Natural selection yields an s value (s , vertical solid
line) that minimizes mineral nutrient availability (N , horizontal solid line), thus minimizing mineral nutrient losses happening through diffusion out of the system.
Can this model help predicting the result of the artificial selection in crop
plants? A possible scenario is that crop breeding is managed to maximize primary
productivity (f0) and thus drives crop plants towards the s0 value (doted vertical
lines). Compared with the previous ‘natural selection’ scenario, such a selection
increases mineral nutrient availability (N0 , horizontal dotted line) and associated
nutrient losses (Fig. 6.1A). Therefore, our results suggest that artificial selection
per se, even in the absence of fertilization, may modify nutrient diffusion in ways
that are negative for agricultural sustainability.
The three other panels (B, C, D) of Fig. 6.1 display the same type of results after
an increase in fertilization (panel B), an increase in plant biomass export to mimic
harvesting (C), or an increase in both (D). These changes increase the effect of
artificial selection, further enhancing nutrient losses. This result is not trivial.
357
Eco-Evolutionary Dynamics in Agroecosystems
BOX 6.1 Natural selection, artificial selection, and the
functioning of ecosystems—cont'd
A
B
¢
0
¢
0
F
0
0
0
F0
¢
C
¢
D
0
0
¢
¢
F
¢
0
F
¢
0
Figure 6.1 Each panel describes variations in the nutrient stock of primary producer (V 0), the stock of mineral nutrient (N0) and primary productivity (F0) at their
ecological equilibriums as a function of the investment into nutrient uptake (s). In
the displayed cases an evolutionary equilibrium is reached (vertical solid line, s )
and natural selection has been show to minimize N (solid horizontal cases, N ).
Crop breeding can be supposed to maximize primary productivity (vertical dotted
line (s0 )). This value of the investment into nutrient uptake leads to an availability of
mineral nutrient N0 (doted horizontal line). In all cases crop breeding leads to a
higher availability of mineral nutrient (N0 > N ). Panel A is based on the same
parameters as in the original article (fertilization, 6 kg nutrient ha1 year1; biomass exportation, 0.1 year1)(see original Fig. 6.2 in Boudsocq et al., 2011). Panel
B uses a higher fertilization rate (30 kg nutrient ha1 year1). Panel C uses a higher
exportation rate of plant biomass (0.5 year1). Panel D uses both a higher fertilization and a higher exportation rate.
Fertilization and crop harvesting can intuitively be thought as factors increasing
nutrient losses at the ecological scale, but crop breeding could have mitigated
such effects. We find the contrary: crop breeding further increases nutrient losses.
Our results illustrate that the intensification of agriculture (increase in harvest
index and mineral fertilization) interacts with crop breeding to determine the
sustainability of agriculture (here characterized by nutrient losses). This result
is useful since the mitigation of nutrient losses is generally viewed independently
either from the point of view of agricultural practices (e.g., Gardner and
Drinkwater, 2009) or of crop breeding (e.g., Good et al., 2004).
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Nicolas Loeuille et al.
Such results raise an intriguing possibility: evolutionary dynamics can
lead to negative relationships between ecosystem services (here primary production versus nutrient conservation). While such negative relationships
have already been noted (Bennet et al., 2009), their fundamental causes as
well as their consequences for ecosystem management, ecological engineering and agriculture are mostly unknown. We suggest that they may naturally
emerge from artificial selection.
In agricultural networks, species co-evolve with the cultivated plant. We
now consider a system in which cultivated species would be selected
through artificial selection and a wild herbivore species would follow natural
selection based on individual fitness (Box 6.2). The initial community
BOX 6.2 Mixing group and individual selection to study the
co-evolution of agroecosystem networks
Most often, community evolution models that tackle co-evolution use individual fitness to determine evolutionary dynamics. In the case of agriculture, to study the
co-evolution of a cultivated plant species and of the species from its surrounding
network, one may want to base the evolutionary dynamics of the plant species
on an artificial group selection criterion, and the evolutionary dynamics of other species based on individual fitness. We know of only one mixed model of this kind
(Fletcher and Doebeli, 2013). We illustrate some possible implications of this idea
using the model described fully in Loeuille et al. (2002), which studies the
co-evolution between defence investment by the plant, and herbivore attack rate.
The plant–herbivore interaction is modelled using a Lotka–Volterra function, whose
rate depends on the two traits. Plant defences incur a cost in terms of growth while
herbivore investment in consumption incurs a mortality cost. In its initial version,
based on natural selection, the plant–herbivore co-evolution model leads to a set
of strategies (plant defences, herbivore attack rate) that allow the coexistence of
plants and herbivores, although some oscillations may exist around the equilibrium
state (Fig. 6.2A). If plant selection now depends on total biomass, for instance
because the farmer selects phenotypes producing higher yields, higher defences
are always favoured, and co-evolutionary dynamics are profoundly affected. Eventually, such a co-evolution causes the extinction of the herbivore (evolutionary murder, Fig. 6.2B, see also Appendix B). This incurs an economic benefit if the herbivore is
a crop pest. On the other hand, the argument is fairly general, so that the
co-evolutionary dynamics associated with artificial selection can also produce
unwanted extinctions. Of course, this model is largely simplified compared to
real agricultural systems, in which herbivores have not disappeared (though
they are usually less abundant). In any case, it illustrates a mechanism through
which co-evolution community structure may be profoundly affected by artificial
selection.
Eco-Evolutionary Dynamics in Agroecosystems
359
BOX 6.2 Mixing group and individual selection to study the
co-evolution of agroecosystem networks—cont'd
Figure 6.2 Plant herbivore co-evolution depending on the selection regime. In
panel A, plant defences co-evolve with herbivore attack rate depending on individual fitness. The evolutionary outcome (black filled circle) is at the intersection of the
herbivore isocline (light grey) and of the plant isocline (black). Herbivore evolutionary dynamics always converge towards the isocline (plain line). For the plant isocline,
evolutionary dynamics can be convergent (plain line) or divergent (dotted line).
When the isoclines intersect in the plain part, evolutionary dynamics will lead to
the evolutionary singularity. In the dotted part, dynamics may cycle around
the singularity. In all instances, the full system plant–herbivore survives (i.e.,
co-evolution stays within existence boundaries, dashed curve). For more details
see Loeuille et al. (2002). Panel B: Same model, but plant selection is based on
biomass production instead of individual fitness. Under such conditions, more defended morphs are always favoured (Appendix B). This creates an ever increasing
trait value for the plant that leads to the extinction of the herbivore (dashed curve),
that is, an evolutionary murder (Dercole et al., 2006).
co-evolution model, where both species evolved out of natural selection,
predicts the maintenance of the complete community. Such maintenance
is unlikely when plants are subjected to group selection, where higher
defences are favoured, because they allow a higher plant biomass by reducing
herbivory. Eventually, such high defences cause the extinction of the herbivore. Therefore, artificial selection regime can have important implications not only for evolutionary dynamics, but also for side-effects on the
community structure and conservation issues of non-targeted species.
Such results of mixing artificial and natural selection pose interesting new
questions. As evolution affects the system’s functioning, a possible target for
crop breeding would be not only the plant species or traits, but also some
part of its connected ecological network. A clear example is the experiment
described in Swenson et al. (2000), who grew Arabidopsis in pots whose soil
was chosen from an ecosystem selection perspective. At each generation,
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Nicolas Loeuille et al.
pots were inoculated with soil samples selected from the biomass of an Arabidopsis individual of the previous generation. Group selection then involved
all organisms present in the inoculate soil based on plant yield. Individual
plant biomass increased rapidly through this selection process. From a theoretical point of view, such outcomes raise intriguing questions, such as
what sets of species of the network should we incorporate in this ecosystem
selection processes? How many species or functional groups should be
involved? What constrains the efficiency of the selection process? All of these
aspects remain largely unknown.
3. DISTURBANCES DUE TO AGRICULTURE:
IMPLICATIONS FOR ECO-EVOLUTIONARY DYNAMICS
WITHIN SURROUNDING ECOSYSTEMS
Lessons from eco-evolutionary models can applied when considering
the effects of agricultural disturbances (Gould, 1991; Thrall et al., 2011;
Verbruggen and Kiers, 2010), which typically correspond to strong selective
pressures on wild organisms, so fast evolution should be expected when suitable variability exists for associated heritable traits. It is critical to account for
these eco-evolutionary dynamics, as they affect the ultimate survival of these
organisms in the landscape (Ferrière et al., 2004; Loeuille and Leibold,
2008b) and produce indirect effects that propagate through ecological networks. Alternatively, adaptation can also take place via plasticity. Phenotypic
plasticity may limit the evolution of genetic responses to disturbances, by
modulating individual fitness (Ghalambor et al., 2007; Hendry et al.,
2011). Also, the degree of plasticity is itself under selection and ultimately
depends on the disturbance regime (frequency, amplitude and predictability). We first list a few of the disturbances associated with agriculture. This
is not meant to be an exhaustive or exclusive list. Rather, we focus on disturbances whose implications may be assessed using community evolution
models.
As modern approaches of crop selection often rely on minimizing environmental variation through a wide use of nutrient additions and a strong
control of enemies, these efforts to simplify the system correspond to strong
selective pressures on the ecological networks in which the cultivated
organism is embedded. There are three main disturbances, which we
will now focus on in turn: nutrient addition, pesticide use, and habitat
alteration.
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Eco-Evolutionary Dynamics in Agroecosystems
Take home messages and key references for section 3
Agriculture and crop
Ecology and evolutionary
ecology
Section breeding
References
Section Agriculture exerts strong
3.1
selective pressures on wild
animals and plants through
direct inputs and habitat
modification
Fast evolution is expected
for variable traits, given the
strong disturbances
Co-evolution creates
indirect effects that
propagate throughout the
network
Thrall et al.,
2011
Loeuille and
Leibold, 2008a
Section Fertilization creates global
3.2
nutrient enrichment
Evolutionary impacts of
enrichment on
communities modify
important ecosystem
services
Nutrient enrichment
modifies top-down
controls within food chains
by altering the selection
regime of defences
Oksanen et al.,
1981
Herms and
Mattson, 1992
Loeuille and
Loreau, 2004
Box 6.3
Section Pesticides exert strong
selective pressures that
3.3
trigger the evolution of
resistances. This incurs
large economic costs
Side-effects exist on nontargeted species
Extra-mortality
evolutionary models can be
used to discuss such
disturbances
Evolution of resistance
depends on the community
context
Mallet, 1989
Abrams and
Matsuda, 2005
Box 6.4
Section The homogenization of
3.4
biotic and abiotic
conditions by agriculture
should mostly select for
specialized interactions
Evolution of specialization
affects pest management
and ecosystem services
Evolution of specialization
depends on species
abundance distributions in
communities
Evolution of specialization
affects the propagation of
disturbances in the system
Poisot et al.,
2011
Doré et al.,
2011
Symondson
et al., 2002
Box 6.5
3.1. Nutrient enrichment and its ecological and evolutionary
consequences in agricultural landscapes
Most natural ecosystems being limited by either N, P or K (Boudsocq et al.,
2012; Vitousek and Howarth, 1991), and agroecosystems are no exception.
Fertilization mainly consists of these nutrients. They are transported in surrounding ecosystems through abiotic factors (diffusion, transport by water)
or through biotic factors (e.g., metaecosystem effects: Loreau et al., 2003).
Nutrient additions profoundly change the diversity and composition of
362
Nicolas Loeuille et al.
natural communities, in terrestrial and aquatic systems (Tilman, 1999; Xia and
Wan, 2008) and are one of the major players in current global changes
(Langley and Megonigal, 2010; Reich, 2009).
From an evolutionary point of view, nutrient additions have direct selective effects, by alleviating costs of life history or physiological traits that are
energetically expensive. They also generate indirect selective effects on traits
related to interspecific interactions, as they modify the composition and
structure of ecological networks. We will analyse first the direct effect (allocation costs), and then turn our attention to assessing indirect effects (community composition and diffuse co-evolution).
To illustrate how the evolution of traits with allocation costs alters the
dynamics of communities, the best starting point is to study the qualitative
effects it has on food chains. Comparing the impact of nutrient enrichment
on food chain dynamics without and with evolution will enable us to assess
its role in community structure and composition.
If a food chain is supplied with increased resources, two possibilities exist.
If biomass at each trophic level is bottom-up controlled—meaning that
competition for resources is the major driver of ecological dynamics—then
biomasses at all trophic levels will increase, because enrichment relaxes competition constraints. This type of pattern holds well in some ecosystems
(Chase, 2003; White, 2005). In other instances, when the biomass at a given
level is determined by predation exerted on it (top-down control), the biomass at the top level of the food chain will increase during enrichment, as
well as all odd levels from the top-down, while the biomasses at other trophic levels remain constant or decrease (Hairston et al., 1960; Oksanen et al.,
1981). Again, empirical patterns can be found to support such top-down
control predictions (Persson et al., 1992; Ripple and Betscha, 2012).
Figure 6.3 in Box 6.3 illustrates such an ecological impact of nutrient
enrichment. Of course, the picture is inevitably more complicated when
omnivory and generalist feeding, which are common features of most ecological networks, blur trophic levels into continua, but the same general
principles apply.
Biological control of crop pests by natural enemies is one of the many
ecosystem services on which the development of a sustainable agriculture
relies (Costanza et al., 1997; Crowder et al., 2010; Doré et al., 2011;
Malézieux, 2011). Top-down control models therefore provide conditions
under which biological controls should operate. For instance, considering
herbivore as pests, nutrient enrichment would increase pest biomass when
the food chain has two levels (plant–herbivore) or an even number of levels
Biomass
BOX 6.3 Herbivore pest evolution under nutrient enrichment:
Implications for biological control
(e.g.,
predator)
(Fig.
6.3). Otherwise,
Theplant–herbivore–predator–super
dynamics of food chains are fairly well
understood.
Particularly,
when top-we
expect
control tonutrient
act, andenrichment
herbivoresincreases
to be maintained
at of
constant
downbiological
controls dominate,
the biomass
the
levels
their enemies
enrichment
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top by
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and during
of everythe
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The biomass of other
levels
remains unchanged
or decreases
(Hairston
et al.,the
1960;conditions
Oksanen et under
al.,
Unfortunately,
evolutionary
dynamics
erode
1981,
see
also
Fig.
6.3,
top).
The
strength
of
top-down
controls
strictly
determine
which this top-down control is expected to happen. Many phenotypic traits
constraining top-down controls have allocation costs, so that their selection
regime may change when energetic constraints are relaxed. Allocation costs
are for instance well described for some plant defences (Herms and Mattson,
1992; Strauss et al., 2002). If nutrient enrichment selects for more defended
plants, energy is less easily transmitted up the food chain, so that top-down
controls are decreased (Loeuille and Loreau, 2004). This is also true for other
traits, such as vigilance, where a possible cost is the foregone time and energy
from activities not related to resource acquisition (Illius and Fitzgibbon,
1994). Again, if nutrient enrichment makes the resource more abundant
or more nutritious, higher vigilance can be favoured (Armstrong, 1979;
Leibold, 1996), which decreases energy transmission through the food
chain. Similar arguments could be made for the evolution of time partitioning between productive and unproductive habitat (Schmitz et al.,
2004; Grabowski and Kimbro, 2005) or for the evolution of body size, a trait
120 some degree of predator avoidance (Emmerson and
whose increase allows
P
100 incurring metabolic costs (Kleiber, 1961).
Raffaelli, 2004), while
80
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H
Loreau (2004) show60how the evolution of plants, evol
the evolution of herbivores, or the co-evolution
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40
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20
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0
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150
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300
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totaland
number
species of
the community
(Chase
Leibold,
starting
from
an
initial
nutrient
input
level
of
100,
the
net
effect
of
the
evolution
2002; Kassen et al., 2000) as well as the number of trophic levels
of herbivores on the weakening of the biological control can be fully perceived
(Oksanen
et al., 1981) so that interactions are globally changed within the
as the distance between the two grey lines. For the analytical demonstration and
parameter setting of Fig. 6.3, see Appendix C.
Continued
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Nicolas Loeuille et al.
BOX 6.3 Herbivore pest evolution under nutrient enrichment:
Implications for biological control—cont'd
the possibility of biological controls, an important ecosystem service (Costanza et al.,
1997). A crucial question is whether evolutionary dynamics strengthen or
undermine top-down controls when nutrient enrichment takes place. Using an
adaptive dynamics approach applied to a Lotka–Volterra food chain model,
Loeuille and Loreau (2004) studied how the biomass variation pattern described
above changed, depending on different plant–herbivore co-evolution scenarios.
One of their conclusions was that plant evolution significantly weakens the
top-down control, because nutrient enrichment selects for higher defence levels
that decrease herbivore impacts. This result is not especially relevant within the agricultural context where plant trait is often more constrained by human action than by
direct selection from herbivores, but a more interesting question arises about how
top-down control is changed considering the evolution of herbivore pests facing
their natural predators. The action of such predators, that is, the biological control,
may change due to herbivore evolution, as modified by nutrient additions. We study
this issue by extending the model of Loeuille and Loreau (2004), adding a predator
level and studying the evolution of herbivore defences. In Appendix C, we show that
the weakening of top-down controls observed in the original model also applies in
such longer food chains. That is, herbivores evolve higher anti-predator defences
during the enrichment, which decreases the biological control (see Fig. 6.3). The
result is fairly general. It does not depend on the trade-off functions that are used,
just requires that the defensive trait of the herbivore has an allocation cost. Identity of
the defensive trait can be of many types, from chemical anti-predator defences
(development of toxicity) to changes in behaviour (increased vigilance, use of
refugia, etc.). As in Loeuille and Loreau (2004), co-evolution scenarios—whether they
are plant–herbivore, herbivore–predator co-evolution, or co-evolution of the three
species—are likely to yield much more complicated results. Note however that
studying herbivore evolution is a logical first step given the agricultural context. Herbivore pests are often insects or small invertebrates, whose evolution has been
shown to be very rapid in response to agricultural change (Gould, 1991; Carrière
et al., 2010): evolution of species at other levels of the food chain may very well
be slower.
network. Because of such changes, the diffuse co-evolution of the entire
ecological network is likely to be affected. It is, of course, more difficult
to predict how such changes in the network will impact evolutionary
dynamics, but some recent models have linked diffuse co-evolutionary
dynamics to community structure or ecosystem functioning. Loeuille and
Loreau (2005) explain that, in a food web based on predator–prey body size
co-evolution that considers interference competition, nutrient enrichment
Eco-Evolutionary Dynamics in Agroecosystems
365
yields more trophic levels and diversity. Brännström et al. (2012), in a related
model, show that it also affects the strength of disruptive selection on body
size in ecological networks, thereby favouring ecological speciation. Results
of increased diversity, numbers of trophic levels and of changes in connectance are also found in a co-evolutionary model that relies on many phenotypic traits evolving independently (Drossel et al., 2001). Note that the
optimistic message that may be inferred from these studies—that nutrient
enrichment increases community diversity—should be taken with caution,
because species niches in these models rely on a single energy axis, so that
enrichment simply inflates the available niche space for diversification. In
nature, at high nutrient loads, negative side-effects such as toxicity or anoxia
ultimately come into play to halt such increases in diversity (Harnik et al.,
2012; Justic et al., 1995).
3.2. Chemical warfare in agricultural landscapes:
The ecological and evolutionary consequences of
pesticide use
A second disturbance that creates important selective pressures is the use of
insecticides, herbicides, or other chemical pesticides. While usually targeted
at specific pests, pesticide toxicities are usually tested on just a few other species and they may have side-effects on a far larger number across different
trophic levels (Crowder et al., 2010; McMahon et al., 2012; Robinson
and Sutherland, 2002), some of which, such as pollinators, may provide
important ecosystem services (Klein et al., 2007). Direct effects can be
observed when sensitivity to the pesticide evolves due to selective pressures
exerted by chemicals. Alternatively, because this disturbance propagates
through the ecological network and affects its structure and diversity, it
modifies the selective pressures indirectly throughout the community, altering the course of diffuse co-evolution.
The use of pesticides is an important disturbance associated with agriculture on local to global scales (Matson, 1997) and by generating extra mortality
on wild organisms, pesticides have detrimental consequences for ecological
dynamics and overall ecosystem functioning (Matson, 1997). Impacts have
been noted on many groups such as birds (Carson, 1962), pollinators (Potts
et al., 2010,) and natural enemies of pests (Bianchi et al., 2006; Geiger
et al., 2010). Decreases in such groups erode their associated ecosystem services (Bianchi et al., 2006; Potts et al., 2010), yet few studies have considered
how associated evolutionary dynamics affect ecological networks.
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Nicolas Loeuille et al.
The potential for an evolutionary response to pesticides varies among wild
organisms associated with agricultural landscapes. Examples of rapid evolutionary responses abound in the agricultural literature (Palumbi, 2001;
Thrall et al., 2011), where resistance to pesticides is a classical textbook example of how continuous selection pressures on a trait with generally simple
genetic determinism results in rapid allele change. The international survey
of resistance in weeds (http://www.weedscience.com) listed 217 species
(129 dicots and 88 monocots) that had evolved resistance to 21 of the
25 known herbicide sites of action and to 148 different herbicides.
A similar pattern is observed in insect pests, with an extremely rapid increase
in the number of species showing resistance to at least one insecticide since the
1950s (Mallet, 1989). Approximately 8000 cases of resistance to 300 insecticide compounds are now reported in more than 500 insect species (Arthropod
Pesticide Resistance Database; http://www.pesticideresistance.com; Whalon
et al., 2008). Similarly, 300 cases of field resistance to 30 fungicides have been
reported in 250 species of phytopathogenic fungi (Fungicide Resistance Action
Committee database; http://www.frac.info; Bourguet et al., 2013). That evolutionary responses are less well-known in non-pest organisms could simply
reflect the fact that they are largely ignored in such instances (Pelosi et al.,
2013), because of the lesser economic concern they represent.
It is, however, not expected that all species will evolve in response to
pesticides: even when a variable and heritable response trait exists, some processes can limit its effective evolution. Plastic responses can play a role in the
emergence of resistance to pesticides, by alleviating fitness costs (Hendry
et al., 2011). For organisms with a plastic behaviour that can simply avoid
crops with insecticides selective pressures for increased resistance will be
weak. Such exploitation of alternative habitats can, however, incur indirect
costs, for instance when such habitats have fewer resources. When plasticity
actually impedes the evolution of pesticide resistance, it still raises important
evolutionary questions: namely, when do we expect the evolution of such
plasticity and what are the associated costs? A general idea is that plasticity is
favoured when selective constraints are variable in space and time (Agrawal,
2001; Lind and Johansson, 2007). Because pesticide use may be highly variable in time, being most prevalent during infestation periods, and because
semi-natural habitats are not directly treated, creating a spatial heterogeneity,
plastic responses should commonly evolve. This view is supported by the
existence of many plastic behaviours allowing some resistance to pesticides (Gould, 1991). Changes in the oviposition and host fidelity behaviour
of corn rootworm, for instance, allowed it to counter crop rotations
(Gray et al., 2009).
Eco-Evolutionary Dynamics in Agroecosystems
367
Demographic constraints, such as population density or generation time,
also affect the evolutionary response to pesticides. This idea can be illustrated
using evolutionary rescue models (Bell and Gonzalez, 2011; Gomulkiewicz
and Holt, 1995). A population facing a disturbance can go extinct when the
extra mortality decreases its per capita growth rate sufficiently. On the other
hand, selection of less vulnerable phenotypes will occur, increasing average
fitness. Evolutionary rescue is determined by the race between these two
processes (Gomulkiewicz and Holt, 1995): extinction or rescue depends
on the initial density of the population and on the generation time of the
species. Small populations or long-lived organisms, having small variability
in the response trait, are most at risk. Their densities following pesticide use
may fall under a critical value, where demographic stochasticity increases the
risk of extinction (Gomulkiewicz and Holt, 1995). However, species whose
effective population size is large (therefore possibly harbouring high genetic
variability), or generation times are short (so that new mutations can appear
more readily), may escape extinction when adaptation happens fast enough
to increase average fitness values before the population viability threshold is
reached. Most pests probably fall in this category, as they have short generation times and high population densities. Pollinator populations, on the
other hand, have lower densities and longer life cycles. Evolutionary rescue
therefore provides a potential explanation for the often-observed selection
of resistance to insecticides in pests (Bourguet et al., 2013; Mallet, 1989),
while many pollinator populations collapse (Beismeijer et al. 2006). Another
example is the evolution of pesticide resistance in fungi, which is determined
by the pathogen’s evolutionary potential, as set by its life cycle and reproduction system (Barrett et al., 2008; McDonald and Linde, 2002).
Most existing works related to pesticides tackle the conditions for the
evolution of higher resistance in pest species (Bourguet et al., 2013;
Gould, 1991; Mallet, 1989; Thrall et al., 2011), reflecting the huge economic costs incurred (Palumbi, 2001). Evolutionary models can then suggest managements that delay the emergence of these resistances, such as
high-dose/refuge or pyramid strategies that use the ensemble activity of
multiple compounds (Bourguet et al., 2013). A complete review of this
aspect is beyond the scope of the present chapter and has been covered elsewhere (Bourguet et al., 2013; Carrière et al., 2010). These approaches, however, mostly focus on one species, the targeted pest, ignoring the broader
ecological network (Tabashnik et al., 2004; Vacher et al., 2003).
Many observations suggest that the community context does affect the evolution of resistance. For example, resistance to insecticides in mosquitoes negatively affects the resistance to parasites, so that evolutionary dynamics ultimately
368
Nicolas Loeuille et al.
depends on the overall parasite load within the population (Agnew et al., 2004).
Resistance in the peach-potato aphid increases its sensitivity to predators due to a
decreased response to alarm pheromones (Foster et al., 2003). Through such
ecological costs, the predation context affects evolution of resistance. Evolution
of resistances also affects pest densities, allowing them to attain large numbers,
and these effects can propagate through ecological networks, creating top-down
or bottom-up effects. Because pests interact both directly and indirectly with
many other species, density-dependent effects will eventually impinge on the
eco-evolutionary dynamics of other wild species of the community.
We have little information on such eco-evolutionary dynamics within the
pesticide context, but another corpus of models, developed in fisheries science, have studied the evolutionary dynamics of communities in which a subset of species faces extra mortality, via harvesting. Even though these models
are not explicitly designed for agricultural systems, they are often stated in general equation systems that can be applied outside the fisheries context,
although such an analysis is still restricted to the mortality effects of pesticides.
Other sub-lethal effects (e.g., modification of fecundity or of consumption
rates) require more explicit and detailed models.
Abrams and Matsuda (2005) studied a two-species model that we have
translated to a herbivore pest and its host plant, where the former suffers
extra mortality (e.g., due to pesticides) and plant nutrient uptake rate evolves. Nutrient uptake rate is supposedly positively correlated with plant
vulnerability, because of an allocation trade-off between defences and
growth. The model shows that herbivore density can increase when its
own mortality increases. This counter-intuitive result occurs because herbivore density initially decreases, causing selection of higher vulnerabilities of
the plant. Because the plant is more vulnerable, the density of herbivore subsequently increases. This latter positive evolutionary effect eventually exceeds the direct negative effects of extra mortality (Fig. 2 in Abrams
and Matsuda, 2005). This result has interesting agricultural implications
because it suggests an evolutionary mechanism through which pesticides
eventually increase pest abundances. Abrams and Matsuda suggest that
plastic responses could produce similar qualitative trends. The model would
also be suitable to describe the evolution of wild plants consumed by
the pest. When increasing pesticide application, pest density increases until
a threshold is reached, but beyond this value the pest abruptly goes extinct.
In a four-compartment model that can be translated as two plants sharing a
limiting nutrient and a pest herbivore, Abrams (2009) again studied how the
response of the pest to extra mortality is affected by adaptation in the plant. Plant
Eco-Evolutionary Dynamics in Agroecosystems
369
evolution can again create an increase in pest density when pesticide is used.
Compared with the simple food chain model of Abrams and Matsuda
(2005), the evolution of the second plant species extends the range of pesticide
use the pest can suffer before going extinct. A possible agricultural implication is
that evolution of a lesser vulnerability in wild plants can improve the existence
conditions of a pest confronted with pesticides. While an exact test of such patterns has not been done, existing data comparing the evolution of weeds within
fields and out of fields can provide an interesting point of comparison (Ellstrand
et al., 2010). Evolutionary effects of extra mortality can also affect the stability of
natural communities, which may increase or decrease, depending on how pesticide impacts relate to population densities (Witting, 2002).
Another important result of fisheries research is that increased mortality can
select for earlier maturation and smaller body size at maturation (Allendorf et al.,
2008; Barot et al., 2004; Enberg et al., 2009; Law, 2000). Because of high mortality, those who mature faster are more likely to reproduce and are therefore
favoured. Similarly, because the pesticide use exerts extra mortality, the same
selective mechanism may apply, with fast-reproducing strategies being
favoured, although we could not find any experiment or observation that
has tested this idea. An obvious difficulty lies in the fact that confounding factors
exist: having a fast life cycle in the first place makes it more likely for a species to
be a pest, and it may also facilitate the evolution of resistance.
This prediction of selection for earlier reproduction may be dependent on
the community context. Gårdmark et al. (2003) used a model in which a prey
population consisting of three-age classes suffers extra mortality from harvesting
and is consumed by a predator species. They studied the evolution of the age at
reproduction (age 2 or 3; age 1 being juveniles), depending on the stage being
predated. Substituting the prey species with a pest species and harvesting with
pesticide extra mortality, in the absence of predation evolution of early maturation is favoured. However, reproduction is delayed to age 3 when extra mortality acts on age 1 and predation on age 2. Thus, the two mortality-related
selective pressures can interact antagonistically (Gårdmark et al., 2003).
Importantly, it is unlikely that only pests are affected by pesticide use, and
impacts on other members of the network are likely to modify associated
ecosystem services as a result. To illustrate this, we modelled a plant–
herbivore pest–predator food chain where both the pest and the predator
are vulnerable to pesticides. For the sake of simplicity, we considered that
only the herbivore evolves in response to pesticides and that evolution of
resistance incurs a cost in growth rate (allocation cost). The model and principal results are detailed in Box 6.4.
BOX 6.4 Evolution of resistance to insecticides in a tri-trophic
food chain
We model a three-species community consisting of a plant attacked by a herbivore pest, consumed by a predator and in which insecticide use affects both the
herbivore and the predator. Detailed equations and analysis of the model are
given in Appendix D. We assume that the herbivore evolves in response to insecticide use. Its susceptibility incurs an allocation cost: when susceptibility
decreases, herbivore reproduction decreases (Carrière et al., 1994). A possible
mechanism is that conversion efficiency is reduced, due to an allocation in detoxification metabolism (Després et al., 2007). We study three different community
scenarios: the predator is absent from the community, the predator has a low susceptibility to insecticides, and the predator has a high susceptibility to insecticides. We use the adaptive dynamics framework to study the impact of
herbivore evolution on the three-species food chain (see Appendix D).
Figure 6.4 shows how evolved resistance changes when pesticide use
(parameter l) increases. Figure 6.5 displays the variations in densities for the three
community scenarios and depending on whether herbivore evolution happens
or not. As intuitively expected, resistance is selected for at higher inputs
of insecticides (Fig. 6.4). Herbivore adaptation delays the extinction of both
Figure 6.4 Influence of insecticide intensity on the value of herbivore susceptibility trait at the evolutionary equilibrium, for the three different community scenarios: ‘No predator’, ‘Low susceptibility of predator’ and ‘High susceptibility of
predator’. Parameters values: r ¼ 2; I ¼ 0.2; w ¼ 0.2; a ¼ 0.5; dh ¼ 0.5; g ¼ 0.5;
dp ¼ 0.1; c(s) ¼ exp(0.1 s); j(s) ¼ exp(0.3 s); Low h ¼ 0.1; High h ¼ 1. For parameter
definitions and details of the equations, see Appendix D.
BOX 6.4 Evolution of resistance to insecticides in a tri-trophic
food chain—cont'd
Figure 6.5 Densities of the three species at the ecological equilibrium (left) or ecoevolutionary equilibrium (right) for different intensities of insecticide application
and for three community scenarios. Continuous lines show plant density V 0,
long-dashed lines herbivore density H0 and dotted lines predator density P0. In these
graphs, all species coexist in areas labelled ‘1’, ‘2’ indicates plant–herbivore coexistence and ‘3’ parameter sets for which only the plant exists. Parameters values are
the same as in Fig. 6.4. When there is no evolution the susceptibility trait for the
herbivore is fixed at 0 (alternative values do not alter the qualitative results).
the herbivore and the predator with increasing load of insecticides (Fig. 6.5).
However, when the predator is not strongly affected by pesticides,less
evolved resistance appears in the herbivore. This last result can be explained
by density-dependent mechanisms: when the predator has a low susceptibility, the plant is at a higher density because of the predator exerts top-down
control on the herbivore. It is then beneficial for the herbivore to be more
susceptible (but with a high conversion efficiency) as the efficient consumption of abundant plants offsets mortality costs. When the predator is highly
susceptible to pesticide, its density is decreased or it goes extinct, so that the
density-dependent advantage disappears. Community context and evolutionary dynamics thereby interact to determine evolution of pests subjected to
increased mortality.
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Nicolas Loeuille et al.
Overall, resistance levels increased with insecticide use, but predator
presence decreased the evolved level of resistance and pest density. Therefore, conservation of predators not only maintains an important ecosystem
service through biological controls, but it may also limit the evolution of
resistance in the pest. Note, however, that this double service is lost when
the predator is highly sensitive to pesticides. Such effects are produced by the
interaction between density-dependent ecological processes (here, predation) and trait dynamics due to species evolution. They affect both the magnitude of species responses and the qualitative direction of such responses, as
reflected in densities and trait values.
In more complex networks, evolutionary effects of pesticide can propagate through many trait-dependent and density-dependent pathways
(Wootton, 1994; Yodzis, 2000). Predicting the associated diffuse evolution
is difficult, especially because most models are based on trophic interactions,
while pesticide use may also affect non-trophic compartments (e.g., pollinators). The interplay between different interaction types is a growing research
area in ecology and evolution (Altermatt and Pearse, 2011; Fontaine et al.,
2011). Antagonistic and mutualistic interactions influence each other,
both through ecological, density-dependent effects and through selective
pressures (Adler et al., 2012; Herrera et al., 2002). This is particularly relevant for agricultural landscapes, whose sustainability relies on ecosystem
services that come from different interaction types. Biological control is
linked to trophic interactions acting on pests, while pollination services rely
on mutualistic interactions. Pesticides may affect all different interaction
types, coupling the different ecosystems services through eco-evolutionary
dynamics.
3.3. Effects of altering species composition and relative
abundance of species in agricultural landscapes
A third disturbance corresponds to changes in habitat, species abundance,
distribution, and composition due to agricultural activities, which can have
multiple effects. By developing open landscapes at the expense of natural
habitats, agriculture modifies landscape composition; at more local scales,
community diversity and composition are also affected. Agricultural communities usually contain just a few dominant species (the cultivated ones),
represented by a few artificially maintained genotypes (Purugganan and
Fuller, 2009), so the base of the food web changes differs markedly from
the natural state that typically contains many plant species.
Eco-Evolutionary Dynamics in Agroecosystems
373
The impact of crop management practices on communities is wellknown: for instance, changes in the relative abundance of crop and weed
plants can generate bottom-up effects changing arthropod community
structure (Lenardis et al., 2011). On the other hand, insects can directly
reduce weed biomass in favour of the crop biomass, and vice versa
(Maron and Crone, 2006; Norris and Kogan, 2005). Such changes in species
biomass at the different trophic levels alter selective pressures, which, in turn,
affect the degree of specialization in species interactions.
The topic of specialization has recently attracted considerable attention
from community and ecosystem ecologists (Forister et al., 2012; Poisot
et al., 2011) and at least three factors influence the relative fitness of generalists and specialists have been identified. First, evolution of specialization
depends on trade-off shapes, with weaker trade-offs, that is, low cost of
switching from one interaction to another, favouring generalists (Levins,
1962; Rueffler et al., 2006b; 2007). Second, specialization can arise from
ecological opportunities created in complex networks (Forister et al.,
2012), such as plant-mediated enemy-free space in tri-trophic systems
favouring specialization in herbivore insects (Singer and Stireman, 2005).
Third, temporal variation in fluctuating and highly disturbed environments
favours generalists while environmental constancy favours specialists
(Levins, 1968, Futuyma and Moreno, 1988). Existing models predict specialization under high resource predictability (little or no seasonality),
abundance and diversity (Roughgarden, 1972; Van Valen, 1965). Behavioural selectivity and plasticity, however, modulate the effects of spatial and
temporal heterogeneity and can promote the evolution of specialization
(Poisot et al., 2011). In a mathematical model, Ravigne et al. (2009)
suggested that the joint evolution of local adaptation and habitat choice
leads to specialization regardless of the shape of trade-offs, provided that
the cost of habitat selection is not too high.
The general trend of agricultural intensification has been simplification
in terms of reduced diversity of species (few crop species, mostly one crop
plant per field), genes (few varieties, genetic homogeneity within each cultivar and mostly one cultivar by field), and management practices (few active
ingredients or tillage systems). Consequently, the transition from traditional
to intensive agriculture should favour specialized interactions, although this
may be partially mitigated by crop rotation. While these ideas require experimental investigation, two lines of observational evidence provide empirical
support. At the species level, outbreaks of pests feeding on the dominant
crop happen more readily in these landscapes. The apparently strong
374
Nicolas Loeuille et al.
modularity (i.e., weakly interlinked subsets of species, strongly connected
internally) observed in species networks within agricultural systems suggests
a high degree of specialization (Macfadyen et al., 2011). Traditionally, modular structure has been thought a stabilizing factor, slowing down the spread
of disturbance between modules (May, 1972; Krause et al., 2003, but see
Allesina and Tang, 2012), but this has been challenged recently, as it appears
that although modularity can enhance stability in trophic networks whereas,
a highly connected and nested architecture, resulted from generalized interactions, can promote community stability in mutualistic networks
(Bascompte et al., 2006, Thébault and Fontaine, 2010).
Specialization has important implications for biological control in agricultural systems. Traditionally, it has been assumed (Howarth, 1991) that an
effective biological control should be highly host-specific, based on the
resource concentration hypothesis that consumers are more likely to prefer
the most abundant resource (Root, 1973). Experimental and theoretical evidence, however, suggests that in the case of pest predators, generalists can
generate better pest control services (Flaherty, 1969), especially in pest-rich
communities where generalist predators maintain low prey populations via
resource partitioning (Symondson et al., 2002).
Less effort has been devoted to the study of biological weed control in crop
fields. On the one hand, the introduction of insects has been proposed as a
mechanism of weed control (McEvoy 2002), but it has also been hypothesized
that the top-down effects of a generalist insect on a crop can be diluted via the
presence of weed species (Root, 1973). Therefore, a generalist insect–weed–
crop system may be easy to manipulate to favour a crop or other beneficial
plant species. What remains unclear, however, is how eco-evolutionary
dynamics can affect specialization of the herbivore and hence, biological weed
control. A simple model of the interaction between a herbivore pest and two
plant species, one crop and one weed, competing for a common resource
(Box 6.5) can be proposed here, in line with the diamond shape commonly
applied in general ecological scenarios (Armstrong, 1979; Leibold, 1996). This
structure is also ideal for studying the interaction between weeds and insect
pests. Indeed, experimental observations suggest that insect pest outbreaks
may be negatively affected by the presence of weeds, because they may host
predators or parasitoids (Altieri, 1981). All else being equal, results of the diamond model suggest that a crop species, despite being a poor resource competitor, can coexist with a competitive weed, due to its herbivore-resistance
mechanism favoured by breeding efforts. Biological weed control in such a
system can be readily achieved via fertilization (see Box 6.5). The generated
BOX 6.5 Degree of specialization of pests and its eco-evolutionary
effects: Implications for weed and pest management
A major challenge in ecology is to understand how species can coexist despite being
limited by the same biotic or abiotic factors (Hutchinson, 1961; Tilman, 1982; Chase
and Leibold, 2003). In theory, species coexistence requires that the abundance of
each species is limited by a different (biotic or abiotic) factor. A generalist herbivore
may represent this additional limiting factor and insure the coexistence of two plant
species competing for a common limiting resource (e.g., a mineral nutrient). This
interaction configuration matches fairly well the case of a generalist insect feeding
on two plant species, a crop and a weed sharing a common limiting resource. Damage to the crop (weed) leads to decreased use of resources by the crop (weed).
Resources not used by the crop (weed) theoretically become available to weeds
(the crop), resulting in increased weed (crop) growth (Norris and Kogan, 2005).
The question is how the eco-evolutionary dynamics of such a system can help to
design effective weed and pest management.
At low resource inputs (small I) the model predicts that competitively superior
weeds dominate because densities of herbivore would be insufficient to reverse their
competitive advantage. At high resource input (high I), however, the crop dominates
because it can support a high herbivore density that in its turn suppresses weed to low
biomass. In other words, the pest functions as an agent of biological control on the
weed at high fertilization levels. Therefore, an agronomist can readily assure a high crop
yield by merely increasing nutrient input and/or by inflicting a high mortality rate on
the weed (e.g., through herbicide use). The efficiency of this biological control mechanism, however, can be compromised by the evolution of herbivore specialization.
A strong selective pressure exists for a relative increase in herbivore’s specialization rate
on the more abundant/profitable crop species (see Appendix E). A consequence of this
evolution of specialization on the abundant crop is that the pest-insect no longer exerts
biological control at high fertilization (Fig. 6.6B and C). Moreover, the evolution of specialization enhances the top-down control on crop plants, which results in the positive
response of the pest herbivore biomass to fertilization (Fig. 6.6A).
Pest biomass
A
0.0
0.2
0.4
0.8
1.0
C
Crop biomass
Weed biomass
B
0.6
0.0
0.2
0.4
0.6
0.8
Nutrient input (I )
1.0
0.0
0.2
0.4
0.6
0.8
1.0
Nutrient input (I)
Figure 6.6 Illustration of changes in the biomasses of the pest, crop and weed species along a gradient of nutrient with (continuous lines) and without evolution (dotted lines). For the analytical demonstration and parameter setting, see Appendix E.
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Nicolas Loeuille et al.
increase in crop biomass, however, will likely affect the degree of specialization of the herbivore. The herbivore species responds adaptively to the relative
decrease of the weed population by increasing its specialization rate on the
most abundant crop population. Thus, the evolution of specialization, via
density-dependent mechanisms or plasticity, may ultimately compromise
the efficiency of biological control practices.
4. ACCOUNTING FOR SPATIAL HETEROGENEITIES:
DISPERSAL, FRAGMENTATION, AND EVOLUTION
IN AGRICULTURAL LANDSCAPES
4.1. Characteristics of agricultural landscapes, past,
present and future
Large changes in agricultural landscapes have happened in the last 60 years:
on a global scale, cultivated areas (1.5 109 ha in 2003) increased by 13%
between 1961 and 2003 and irrigated land has doubled (Paillard et al.,
2010). In some regions of Asia and South-America, the ‘Green Revolution’ favoured the transition from subsistence agriculture to industrial agriculture, and similar changes took place in North America and parts of
Europe. Through increased inputs and breeding of modern varieties, the
productivity of the major crops improved, reducing malnutrition in some
Take home messages and key references for section 4
Agriculture and crop
Ecology and evolutionary
ecology
Section breeding
References
Section Ecological intensification of
4.1
agriculture would lead to
more fragmented and
diverse agricultural areas.
Impact on fragmentation of
natural areas depends on the
land-sparing/land-sharing
choice
Habitat heterogeneity and Tscharntke
steepness of environmental et al., 2005
gradients affect ecoevolutionary dynamics
Section The spatial distribution of
4.2
fields affects gene flows from
cultivated species to wild
populations and among wild
populations. This
subsequently affects pest and
wild species evolution
The spatial organization of
the patches of a
metacommunity influences
gene flows and the
subsequent evolutionary
dynamics
Haygood
et al., 2003
Plantegenest
et al., 2007
377
Eco-Evolutionary Dynamics in Agroecosystems
Take home messages and key references for section 4—cont'd
Agriculture and crop
Ecology and evolutionary
Section breeding
ecology
References
Section Conservation biological
4.3
control of pests aims at
promoting movement of
individuals from seminatural areas to fields.
Spillover of individuals from
crops to natural habitats also
happens. This impacts the
ability of species to adapt to
crop/natural habitats
Dispersal between patches
impacts community
composition and related
eco-evolutionary dynamics.
Amount of spillover and
habitat characteristics also
affect evolution of dispersal
and species adaptation to
new habitat
Rand et al.,
2006
Blitzer et al.,
2012
Section Agriculture would benefit
4.4
from co-evolution scenarios
that would foster the
evolution of mutualistic
interactions between crops
and other organisms
Landscapes lead to a mosaic
of coldspots and hotspots of
co-evolution, linked by the
dispersal of either one or the
two species
Thompson,
1999
Hochberg
et al., 2000
Section Agricultural activities create Eco-evolutionary dynamics
gradients of productivity
lead to higher diversity and
4.5
more complex networks
due to fertilization
when gradients of
productivity are smooth and
in intermediate productivity
locations
Section Land sharing is likely to be
the safest option for
4.6
agriculture in terms of ecoevolutionary dynamics
Loeuille and
Leibold,
2008a
Doebeli and
Dieckmann,
2003
Based on metapopulation/
metacommunity models,
land sharing may better limit
the evolution of pest
resistance, maintain
mutualistic interactions,
maintain diversity
regions and allowing other regions to reach food self-sufficiency (Evenson
and Gollin, 2003), albeit sometimes at the cost of increased social inequality
(Jarosz, 2012).
The industrialization of agriculture has had large impacts on the structure
(composition and spatial configuration, Turner, 1989) of the landscape, whose
composition (i.e., the nature of land covers/uses) has become less diverse as local
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crops or landraces have been replaced by a few highly productive cereals (wheat,
corn, and rice that now represent 40% of cultivated lands; Tilman, 1999). The
local intensification of agriculture and increased inputs also reduced plant diversity in cultivated areas through improved weed control and reduced necessity
for set-aside fallows. The proportion of natural or semi-natural areas in landscapes were reduced and these areas became more fragmented, partly because
of an increase in cultivated area, but also because of land reallocation procedures
to increase field sizes and facilitate mechanization. This has destroyed the edge
habitats that surrounded small fields and acted as corridors between different
parts of the natural habitat (Davies and Pullin, 2007), which, combined with
intensive agricultural practices in cultivated fields, sharpened the boundaries
between different habitat types.
The industrialization of agriculture has also altered the temporal dynamics of land use, replacing stable perennial cultivated areas, such as orchards or
pastures, with arable land (Malézieux, 2011; Tscharntke et al., 2005) and a
fast habitat turnover through crop rotations. Asynchrony of sowing and harvest dates among crops further creates a ‘hidden heterogeneity’ of the crop
mosaic, such that a given landscape exhibits very different structures both
within and across years (Vasseur et al., 2013), including more frequent
periods with no vegetation cover (Malézieux, 2011).
The low sustainability of intensive agricultural development has been
widely documented, in particular based on its negative environmental impacts
(Flohre et al., 2011; Geiger et al., 2010). New paradigms have been proposed,
such as ‘sustainable agricultural intensification’ (Lee et al., 2006) or ‘ecological
intensification’ (Doré et al., 2011; Griffon, 2010; Malézieux, 2011). Based on
some principles of agroecology (Altieri, 1989, 1999), these approaches propose
that part of a response to global food security challenges, in the context of
increasing population size and climatic variability, relies on an increase of biodiversity at the agricultural landscape scale and within fields, and they should
also increase the provision of additional ecosystem services, beyond that of food
production (Macfadyen et al., 2012; Smith et al., 2012). In contrast to the limited range of management techniques used in intensive systems, at the landscape
level, this ecological intensification requires more diverse cropping systems (De
Schutter, 2010; Paillard et al., 2010). Within fields, higher levels of aboveground diversity could be provided, either by growing spatial associations
of species, possibly in an agroforestry framework (Ratnadass et al., 2012;
Smith et al., 2012), or by increasing the diversity of crops over time by diversifying rotations and/or including intercrops (Altieri, 1999). Increasing crop
intra-specific genetic diversity, by increasing the numbers of genotypes per species grown either within or across fields, is another suggested solution
Eco-Evolutionary Dynamics in Agroecosystems
379
(Goldringer et al., 2006; Tooker and Frank, 2012). Because the development of
ecological intensification involves large changes in agricultural management,
the associated (initial) economic costs must be considered. Recent studies suggest that current trends in yield may not be sufficient to meet future demands
(Ray et al., 2013), so ideally ecological intensification should not decrease yields
relative to the present situation (Tilman et al., 2011). To achieve this will
require considerable development in scientific knowledge, training of farmers
and more sophisticated landscape planning (Doré et al., 2011, Médiène et al.
2011). The predicted changes in agricultural systems are likely to increase
the diversity and the fragmentation of agricultural habitats, but whether the
converse will be true for natural and semi-natural habitats will depend on
the options taken during landscape planning.
Future agricultural management is often seen as a choice between land
sparing versus land sharing. With an increasing population to feed, the
land-sparing solution proposes to increase the local productivity of fields
by any means necessary, including high inputs, so that remaining ecosystems
can be preserved. Following this approach, the result would be very intensive,
nature unfriendly, agricultural fields on one side, and spared patches of wildlife
on the other side, the two being as clearly separated as possible (Fig. 6.7, left).
In the land-sharing solution, the management of agricultural ecosystems aims
at being wildlife friendly (less intensive production, less inputs, etc.), with the
land being ‘shared’ by human and nature. Meeting increased food demands
then needs larger agricultural surfaces. If the land-sparing solution is chosen
(Fig. 6.7, left), the amplitude of environmental gradient increases, as all
Figure 6.7 Impact of land-sparing and land-sharing management options on the spatial
gradient of environmental conditions. On each panel, exploited areas are in dark, natural systems in light. In the case of land sparing, the difference between the two habitats
is large and they are well separated in space. In the land-sharing scenario, agricultural
exploitation is made closer to natural conditions and agricultural fields are embedded in
a matrix of natural habitats.
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patches, both natural and agricultural, are either extremely suitable or
extremely unsuitable for any species and the environment becomes more spatially aggregated. In the land-sharing situation (Fig. 6.7, right) these scenarios
are reversed. Agricultural fields are managed as lightly as possible so that variations between the field and the surrounding ecosystems are minimized: the
ecotone is less extreme. Also, semi-natural habitat is kept within agricultural
landscapes, so that the environment is less spatially aggregated.
4.2. Consequences of agricultural landscape structure
in terms of gene flow
By fuelling local genetic variability or, conversely, by introducing locally
maladapted genes, gene flows are major constraints on eco-evolutionary
dynamics. They interact with local selection processes to determine the
amount of evolutionary change. Also, they depend on the level of spatial
heterogeneity and species dispersal abilities. Here, we will give a brief review
of the ways the spatial organization can constrain gene flows, by considering
how gene flows have affected the domestication and artificial selection process, how genes flow from cultivated species to surrounding ecosystems, and
how agricultural fragmentation affects gene flows among natural
populations. Finally, we will highlight the implications of gene flows for
the eco-evolutionary dynamics of agricultural pests.
Gene flows in cultivated–wild/weed complexes have long been recognized as an important process for crop domestication and as a source of crop
improvement in traditional agriculture (de Wet and Harlan, 1975; Elias
et al., 2001). Most crops indeed have wild relatives with which they can
hybridize readily. Ellstrand (2003) lists 49 cultivated plant species for which
there is genetic evidence of spontaneous hybridization with wild relatives
among which wheat, corn and rice and 12 of the 13 most important crops
in the world hybridize with their wild relatives (Ellstrand et al., 1999).
Increases in cultivated areas and anthropogenic modifications of wild species
habitats have promoted the likelihood of new contact zones between crops
and related species (Crispo et al., 2011). When the crop and its relatives
co-occur, the structure of the agricultural landscape determines the amount
of crop-to-wild gene flow by affecting their relative spatial distributions. It is
only recently, however, with the use of GM crops, that the impact of the
spatial distribution of crops and their relatives on such gene flow has been
thoroughly investigated and that attempts have been made to quantify it.
Quantification has proved difficult because landscape-scale experiments
are logistically challenging and gene flow events are rare. Historical gene
flow estimates based on population genetic structure cannot be used
Eco-Evolutionary Dynamics in Agroecosystems
381
effectively because of the dynamical spatial distribution of crops over the
landscape (Holderegger et al., 2010; Sork et al., 1999). Most effort has thus
been devoted to measures of contemporaneous gene flow, as measured, for
example, in Brassica napus (Hall et al., 2000), Brassica rapa (Warwick et al.,
2003; Schafer et al., 2011), Beta vulgaris (Arnaud et al., 2010), and Agrostis
stolonifera (Snow, 2012). Experiments have also been conducted to estimate
the rate of crop-to-wild gene flow (e.g., for oilseed rape Jorgensen et al.,
2009), some of which have addressed the spatial distribution of plants
(Klinger et al., 1992; Massinga et al., 2003). Quantitatively, results depend
on the parental species and genotypes, especially their selfing rate, as well as
on the experimental design (e.g., plant densities and management) (e.g.,
Jorgensen et al., 2009). The amount of gene flow also depends on the relative abundance of the crop versus its wild relative (e.g., Giddings, 2000,
Lavigne et al., 2002). For species that are pollinated by wind or both insects
and wind, more insight concerning the impact of landscape structure may
come from models describing gene flows between fields planted with the
same crop (review in Beckie and Hall, 2008; Kuparinen, 2006). Qualitatively, most studies typically report leptokurtic gene flow curves, with most
cross-pollination events occurring over short distances and few events at
large distances. Modelling approaches indicate that gene flow will be maximized in landscapes where the wild relative populations are small and
nearby (Klein et al., 2006a,b). They also indicate that, in species with sufficient long distance pollen dispersal (i.e., fat-tailed dispersal kernels, Kot
et al., 1996), gene flow with distant wild relative populations will largely
depend on the overall abundance of the crop over the landscape (Lavigne
et al., 2008), while for short distance dispersing species, it will mainly depend
on the proximity of the nearest field (Klein et al., 2006a,b). Larger relative
wild populations will also be less impacted because of the protection effect of
their local pollen cloud, that is, it is easier to find mates of the same species
(Lavigne et al., 2008; Rhymer and Simberloff, 1996).
Other landscape characteristics, such as its physical heterogeneity (barren
land, high hedgerows), may either promote or limit gene flow from crops
(Dupont et al., 2006; Manasse, 1992; Morris et al., 1994; Reboud, 2003).
Predicting in detail how the structure of the agricultural landscapes affects
crop-to-wild gene flow in insect-pollinated species is particularly challenging because pollinator movements may depend on the specific spatial distribution of habitats (Hadley and Betts, 2012).
The fate of introgressed genes will depend on a balance between frequency of gene introgression and selection for the ‘cultivated’ gene in the
hybrids and their progeny in the wild population (e.g., Nagylaki, 1975).
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If the introgressed gene is selected for, it can result in genetic assimilation and
possible losses of diversity in wild populations. Assimilation is also expected
for detrimental genes when migration rates are high (e.g., Felsenstein, 1976;
Haygood et al., 2003; Huxel, 1999; Nagylaki, 1975; Slatkin, 1985).
Introgressed genes can negatively affect the fitness of the hybrids or subsequent generations, placing wild populations at risk of extinction via demographic swamping (Haygood et al., 2003; Kwit et al., 2011; Levin et al.,
1996). Finally, if hybrids or their progeny exhibit higher fitness than their
parents, they may become weedy or invasive. Given the huge, and increasing, areas that have been planted with cultivated crops and, given their ability to hybridize with wild relatives, invasions in natural areas are surprisingly
infrequently reported. Situations where hybridization led to invasive or
weedy species becoming agricultural pests are far more frequently reported,
possibly because more easily observed and of larger economic interest. These
include, for instance, Johnson grass, weedy rice and weedy beet (Ellstrand
et al., 2010).
Genetic assimilation is less easily observed because introgressed genes may
have little or no impact on the wild species phenotype (Rhymer and
Simberloff, 1996), yet reports of introgression of cultivated genes in the wild
species (or subspecies) are numerous (e.g., Arias and Rieseberg, 1994; de la
Cruz et al., 2005; Linder et al., 1998; Rieseberg et al., 1999; Warwick
et al., 2003; Whitton et al., 1997). The relatively infrequent reports of genetic
assimilation in wild relatives of crops or in invasive species that descend from
crops may be caused by the generally poor adaptation of crops outside fields
(de Wet and Harlan, 1975) and the low fitness of hybrids with cultivated traits.
Indeed, low hybrid fitness, rather than promoting genetic assimilation of wild
populations, increases the risk of local extinction because of increased demographic stochasticity and maladaptation (Ellstrand, 1992; Simberloff, 1988).
The exact cause of extinction may then be difficult to determine a posteriori.
The modified spatial structure of the agricultural landscape also affects
existing gene flows between semi-natural habitats embedded within it, as
they are prone to shrinkage and fragmentation. In theory, this should isolate
wild populations from each other, increase their risk of extinction by a
simultaneous increase of demographic stochasticity and of genetic drift limiting their evolutionary potential and favouring inbreeding depression (e.g.,
Simberloff, 1988; Stockwell et al., 2003; Young et al., 1996). These processes are, in particular, expected in species that are specialists of semi-natural
environments, and which have low reproductive rates and limited dispersal
abilities (Ryall and Fahrig, 2006). For these species, habitat fragmentation
Eco-Evolutionary Dynamics in Agroecosystems
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results in a loss of connectivity among populations (Kindlmann and Burel,
2008). The overall trend for reduced diversity in populations from fragmented landscapes has been confirmed using a meta-analysis, which further
highlighted that the level of diversity also decreased with age since fragmentation (Aguilar et al., 2008). However, habitat fragmentation does not always
lead to genetic isolation of populations, and landscape genetics has helped to
clarify this issue (Manel et al., 2003). In some landscapes, semi-natural elements, such as hedges, can connect remnant forest patches, although the
effectiveness of such corridors largely depends on the species considered
(Davies and Pullin, 2007), and some species are also capable of movement
across the open habitats of agricultural landscapes (Kanuch et al., 2012).
In certain cases, gene flows by pollen may even be enhanced in fragmented
landscapes, as is often the case for trees (Bacles and Jump, 2011), and in some
species with long distance dispersal, isolated individuals may receive more
diverse pollen than those growing in large groups (Ismail et al., 2012; Klein
et al., 2006a,b). A different pattern emerges for insect-pollinated species
(Hadley and Betts, 2012), for which the combined effects of habitat loss
and fragmentation tend to have negative impacts, probably because of pollen
limitation. The most susceptible species are self-incompatible species that need
outcrossing from genetically distinct individuals (Aguilar et al., 2006).
Finally, some generalist species can live in both the semi-natural areas of
agroecosystems and in the fields, provided that pesticide intensity is not too
high (Rand et al., 2006; Samu and Szinetar, 2002) and for them habitat
opening through agricultural conversion is not necessarily negative and
may even make for more connected landscapes (e.g., Eriksson, 2012;
Nève et al., 2008).
While gene flows among natural populations affect their densities, and in
some cases threaten their conservation, gene flows are also modified for pest
species, with possibly large economic implications. Landscape structure
influences not only the dynamics of pests but also their evolutionary dynamics (Burdon and Thrall, 2008; Plantegenest et al., 2007). Evolutionary consequences of the spatial distribution of crops over the landscape have been
largely investigated in the case of the evolution of pest resistance to pesticides
(insecticides, fungicides, herbicides) and of variety resistances by pathogens.
The rapid increase of resistance in general is due to the widespread use of
pesticides that globally increases the selection pressure for resistance and
to the mode of action of compounds that focus on specific targets. Similarly,
varietal resistances by pathogens have broken down, due to the deployment
over large areas of a same monogenic resistance to a pathogen resulting in a
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rapid increase in virulence alleles: currently estimated at 4–6 years on average
in western countries (McDonald and Linde, 2002).
The spatial context also provides solutions for the management of the
evolution of resistance. Deployment strategies of plants or pesticides have
been developed to cope with the rarefaction of new pesticide molecules
and the high cost for producing varieties resistant to pathogens or, more
recently, insecticidal GM crops. When the pesticide resistance (or virulence
gene) is already present in the population, or when it appears quickly, as is
the case for many pesticides, spatial strategies aim to reduce the overall selection pressure and slow the progression of the resistance (respectively, virulence) alleles or, even, to stabilize their frequency at a low level where
resistance (respectively, virulence) has an associated fitness cost (Bourguet
et al., 2013; Vacher et al., 2003). These strategies are based on establishing
mosaics (also named mixtures) of resistance genes/pesticide treatments over
the landscape at different spatial scales (within or between fields), so that pest
populations experience heterogeneous selection pressures. The optimal spatial scale of patches within the mosaic depends on the dispersal ability of the
pest/pathogen (Bourguet et al., 2013). When the resistance is not already
present in the populations, as in GM crops, high-dose refuge strategies have
been proposed and tested (Bourguet et al., 2013; Gould, 1991; Lu et al.,
2012). High doses are meant to severely reduce pest densities to slow the
emergence of resistance, be it monogenic or polygenic, and to make resistance functionally recessive. Refuges are most commonly areas that are not
treated with pesticides, not planted with GM crops, or not planted with varieties resistant to a particular pathogen. They favour sensitive (respectively
avirulent) individuals of the pest species when there is a fitness cost to resistance (respectively, virulence) (Bourguet et al., 2013; Carrière et al., 2010).
Dispersal of individuals between refugia and non-refugia zones is essential
(Carrière et al., 2010; Gould, 1998), so that their use actually alters gene
flows within the landscape.
Pests may also have hosts in natural populations, and wild or weedy
plant species that act as a ‘reservoir’ of inocula when the crop plant is absent
in the landscape are important for pathogen dynamics and evolution
(Burdon and Thrall, 2008). In fact, the optimal strategy to promote the
durability of varieties depends on the importance of reservoirs as sources
of inocula relative to field-to-field dispersal. When reservoirs are important
pest sources, high cropping ratios of resistant varieties should be promoted
because the pathogen population may be maintained at a low level (Fabre
et al., 2012). Wild or weedy plants may also include the host where pest
Eco-Evolutionary Dynamics in Agroecosystems
385
sexual reproduction occurs, which can accelerate pest evolution rates
(Plantegenest et al., 2007).
In practice, controlling the spatial structure of varieties or treatments over
landscapes can be difficult when different farmers own discrete parcels of land.
The scale of ecological processes then differs from the scale of management
(scale mismatch hypothesis, Pelosi et al., 2010). Some large-scale management
programmes have nevertheless been implemented in co-ordinated refuge
strategies for GM crops (Carrière et al., 2012) or in landscape designs aimed
at enabling efficient pest control (Bianchi et al., 2006).
4.3. Consequences of spatial modifications from a
demographic point of view
Consequences of individual movements across agricultural landscapes go
beyond gene flows, and ‘spillover’ also modifies densities and species
interactions in both the cultivated and wild habitats. Most studies have
focused on movements from the wild to the cultivated habitats, with the
aim to protect the ‘integrity’ of crops (Rand et al., 2006): field edges, for
example, were long considered as a reservoir of weeds or diseases by
farmers (Norris and Kogan, 2000). Semi-natural habitats are also seen
as a source of pest enemies that can act as biological control agents.
The promotion of predator and parasitoid spillovers from semi-natural
areas into the crops is one aim of conservation biological control
programmes (Landis et al., 2000). Landscape management options
designed to promote biological control are based on increasing the proximity of cultivated to semi-natural areas, so that pest enemies active in
fields may find additional food resources, refugia, or overwintering sites
in adjacent semi-natural areas (Bianchi et al., 2010; Brosi et al., 2008).
This increase of contact zones may, however, have evolutionary consequences for populations inhabiting semi-natural areas, by changing their
interactions within their species assemblage (Knight et al., 2005).
A recent review also highlighted the frequency of the opposite direction
of spillover, from crops to semi-natural areas for a wide range of functional groups (Blitzer et al., 2012), which will depend on species traits,
such as dispersal ability and attack rate on the pest prey (Chalak et al.,
2010), and on similarity between cultivated and semi-natural areas
(Opatovsky et al., 2010; Prevedello and Vieira, 2010). It may have dramatic consequences for ecological networks when crops are the dominant land cover and when they harbour larger populations of organisms
than semi-natural habitats. Consequences are direct when herbivore
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spillover reduces the size of semi-natural plant populations (Louda et al.,
2003; McKone et al., 2001) or when generalist predators or parasitoids
considered beneficial in the fields attack non-pest herbivores (Gladbach
et al., 2011; Rand and Louda, 2006). Pathogens that build up large
populations in fields may also affect wild related species, and wild plants
may be affected by pollinator spillover from the crops. Indeed, cultivated
areas may provide rich resources for pollinators, as in the case of mass
flowering crops, such as bean or oilseed rape, and large pollinator
populations may build up (Hanley et al., 2011; Westphal et al.,
2003), which could benefit wild plant populations. However, such
changes of the pollinator community may also disfavour certain competing wild pollinator species and their associated plants in semi-natural
habitats next to crops (Diekötter et al., 2010). The interplay of such
changes in the composition of ecological communities and of gene flows
crucially affects the eco-evolutionary dynamics within agricultural landscapes, and is likely to affect species coexistence (Urban et al., 2008) and
the overall structure of interaction webs (Loeuille and Leibold, 2008a;
Rossberg et al., 2008).
Eco-evolutionary dynamics are also affected by changes in fragmentation due to agricultural activities. A directly impacted trait is dispersal: several models show that the spatial heterogeneity of environmental
conditions (Mathias et al., 2001; Parvinen, 2002) or the fragmentation
of the landscape in patches of asymmetric size (Hanski and Mononen,
2011, Massol et al., 2011) favour the evolution of high variability in
intra-specific dispersal strategies. These theoretical results are consistent
with observations in natural populations (Hanski et al., 2004). Agricultural
activities, by modifying the level of fragmentation, change the selective
pressures that maintain such variation. Beyond a certain level of fragmentation, positive evolutionary effects are likely to be compensated by
increased local extinctions, so fragmentation effects are likely to be negative overall. A recent model simulating the impact of climate change shows
that evolution of dispersal in a very fragmented landscape did not allow the
species to escape extinction (Kubisch et al., 2013), while it did at intermediate fragmentation levels. These examples suggest that fragmentation caused by agricultural activities not only has evolutionary—and sometimes
positive—implications for dispersal, but also should be seen in the light
of other disturbances.
The spatial heterogeneity created by agricultural activities raises the
question of the conditions under which a species that inhabits the natural
Eco-Evolutionary Dynamics in Agroecosystems
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habitat will adapt to the agricultural field and be maintained there. Clearly,
this is of critical importance for developing sustainable agriculture and
accounting for species conservation. A suitable modelling framework for
addressing this question is the one developed for source–sink landscapes
(Pulliam, 1988), in which some areas can maintain populations even in
the absence of dispersal (sources), while others do not (sinks). The blackhole sink model by Holt et al. (2003) is particularly relevant here: it shows,
in a fixed landscape, that if a population has a source (e.g., the natural habitat)
and a sink (e.g., surrounding agricultural fields), then, in the absence of habitat selection, the population eventually adapts to survive in the sink. The
worse the conditions are in the sink, the longer it takes for adaptation to
occur, although higher dispersal from the source accelerates this rate, so
adaptation can be quite abrupt and rapid.
These results are particularly relevant for considering the erosion of
diversity in agricultural landscapes (Robinson and Sutherland, 2002).
From the black-hole sink model, one would expect that species from surrounding habitats will eventually adapt to agricultural locations and that
diversity would be restored in the long run. Indeed, adaptations to new
agricultural landscapes have been observed in many species (Eriksson,
2012), such as those adapted to open habitats maintained by agricultural
activities. However, in high input, intensive agricultural fields, it is likely
that adaptation to the black-hole sink is delayed by the extreme conditions
in the sinks (i.e., the fields) so that diversity recovery is slower and may be
outpaced by extinctions (Gomulkiewicz and Holt, 1995). In the light of
the black-hole sink model, restoring diversity is much more feasible in traditional agriculture, where the conditions within fields and in surrounding
landscapes are not so different, so that adaptation to agricultural conditions
can happen faster. Restoration of diversity is important not only for the
conservation of species, as diverse networks of species interactions most
often have a better functioning and stability (Loreau et al., 2001) and
may in turn provide more efficient and stable ecosystem services to agricultural fields (Crowder et al., 2010).
The black-hole sink model can also help to explain why cultivated species so rarely invade natural ecosystems. Through artificial selection, cultivated species have often evolved a suite of traits that make them non-viable
in natural conditions (Meyer et al., 2012; Purugganan and Fuller, 2009), so
the surrounding ecosystems are strong black-hole sinks for them. Adaptation
and invasion of these habitats would therefore be very slow and, since the
evolution of these cultivated species is often constrained by human
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populations in ways that are unrelated to the sink conditions, there is no reason to expect that the within-sink adaptation will ever take place.
4.4. Consequences of spatial structure for pairwise
co-evolution
Metapopulation models such as the black-hole sink model consider the evolution of a single species in space, and by ignoring species interactions they
focus on spatial heterogeneities and fragmentation. However, most ecosystem
services on which agriculture relies, such as pollination or biological control,
depend on species interactions, so we need to know how the spatial effects of
agricultural activities affect pairwise co-evolution within communities.
A suitable framework for addressing this is the ‘geographic mosaic of
co-evolution’ (Thompson, 1999, 2005), which is based on the idea that
the conditions of co-evolution between two species are highly variable in
space. In some places, called ‘hotspots’, the two species interact strongly
and their evolution is mostly explained by their pairwise interaction. In
other places (‘coldspots’), the co-evolution is less tight due to local conditions. The landscape consists of a mosaic of coldspots and hotspots, linked
by the dispersal of either one or the two species (Gomulkiewicz et al.,
2000). Several interaction types have been modelled in this framework, such
as host–parasite interactions (Nuismer and Kirkpatrick, 2003; Nuismer et al.,
2000), predator–prey interactions (Hochberg and van Baalen, 1998), or
mutualistic interactions (Gomulkiewicz et al., 2003).
A key strength of the geographic mosaic of co-evolution is that it goes
beyond this simple classification of interaction types, so mutualistic and antagonistic interactions need not be treated separately, and can be considered as
part of a continuum. The empirical situation that motivated the geographic
mosaic of co-evolution explains how this new approach arose (Thompson,
1999): in the interaction between a moth (Greya politella) and a plant of the
genius Lithophragma, the female moth transports pollen from flower to flower
when they oviposit within the corolla, thereby providing a basis for a mutualistic interaction. The larvae subsequently eat a few flowers, decreasing plant
fitness. Therefore, the balance of the interaction, positive or negative, varies
depending on other local conditions. If many other pollinators are available,
the interaction may be seen as negative. If pollinators are rare, the interaction
can be seen as mutualistic, as the moth then provides a much-required service.
The nature, strength and degree of reciprocity of the pairwise co-evolution
will change accordingly, making the landscape a geographic mosaic of
co-evolution (Thompson, 1999). Theoretical works on the mosaic of
co-evolution have investigated this continuum of antagonistic and mutualistic
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interactions, as well as their dynamics in space and time (Gomulkiewicz et al.,
2000, 2003; Nuismer et al., 1999, 2000, 2003).
This evolution along a continuum between antagonistic and mutualistic
interactions has potentially huge implications for agriculture. Sustainable agriculture would, ideally, rely on ecosystem services produced by mutualistic
interactions, so any co-evolution scenario that turns mutualistic interactions
into antagonistic ones would be detrimental. Considering this, the geographic
mosaic of co-evolution gives two important insights regarding the long-term
management of interactions. First, the long-term maintenance of mutualism
depends on local energetic constraints. Hochberg et al. (2000) investigated
how co-evolution makes the nature of a symbiosis change along gradients
of productivity. They showed that mutualistic interactions are expected in
poor environments, while richer places should harbour strong parasitism. If
one considers the interaction between plants and mycorrhizae or between
plants and soil microbes in general, the association should evolve to be mutualistic in poor environments, but antagonistic when too much nutrient would
be added, due to evolution or adaptation of either plants or mycorrhizae. In a
geographic mosaic of co-evolution, nutrient addition could therefore indirectly disrupt an important ecosystem service. Because the model by
Hochberg et al. (2000) is fairly general, the warning may seem speculative.
However, two models more tightly focused on this particular issue (De
Mazancourt and Schwartz, 2010; Thrall et al., 2007) and reviews of empirical
data (Verbruggen and Kiers, 2010) support this general idea.
The second important insight is that just a few strongly selecting hotspots
can drive co-evolution at the landscape scale (Gomulkiewicz et al., 2000),
and there is ample evidence of strong selection in agricultural systems
(Gould, 1991). If an agricultural field is a hotspot for the co-evolution of
an interaction, then co-evolution happening there would have important
ramifications for co-evolution within surrounding ecosystems. Returning
to the example of the maintenance of plant–microbe mutualism, this raises
a puzzling question: if fertilization within fields were to turn some mutualistic interactions into negative ones, might it also disrupt interactions in surrounding ecosystems? An interesting example in which evolution under
agricultural practices may lead to large changes in wild populations concerns
pollination. In intensive landscapes, fragmentation of wild habitats and use of
insecticides have altered pollinator diversity and densities, disrupting the
ecological link between pollinators and wild plants. Under such conditions,
evolutionary models predict the selection of more self-fertilization in wild
plants (Massol and Cheptou, 2011), with large implications for the genetic
structure, further evolution and ecological dynamics of plant species.
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4.5. Beyond pairwise interactions: Consequences of
eco-evolutionary dynamics for community structure
and composition
Agricultural development creates strong spatial heterogeneities in habitats
and species pools: semi-natural areas coexist with agricultural fields and
community structure changes markedly over space. Total diversity, the
number of trophic levels, and the overall productivity or biomass of the
community are all structural and functional aspects that vary between
the field, its margins, and the surrounding habitats.
Models accounting for spatial heterogeneities and variations in community structure can help us understand their implications for the evolutionary
and ecological dynamics of species assemblages (e.g., community evolution
models along gradients of productivity may explain how spatial heterogeneities in nutrient enrichment affect community stability and complexity).
One relevant result of such models is that the emerging diversity eventually
maintained throughout the landscape depends on the amplitude of the gradient of
productivity. In a sympatric speciation model, Doebeli and Dieckmann (2003)
showed that maximum diversity is obtained at intermediate gradient amplitude.
If the initial gradient is shallow, increasing its steepness creates niche opportunities
that are positive for the emergence of diversity. Increasing the steepness of the
gradient further leads to adjacent locations having increasingly contrasted settings.
Any dispersal then produces maladaptation, and such negative gene flows eventually impede the diversification process and select for generalists. This illustrates
that the management of productivity gradients, a central challenge in contemporary agriculture, is likely to affect the maintenance of species diversity at landscape
scales, as well as the scope for future speciation.
Such results do not seem to necessarily depend on the precise settings of a particular model (seee.g.,Day,2001;Kawata,2002;Massol,2012): in avery different
model based on predator–prey co-evolution, Hochberg and van Baalen (1998)
also showed how the productivity gradient affects the maintenance of phenotypic
diversity.Thetotaltraitdiversitymaintaineddependedontheslopeoftheproductivity gradient and peaked in areas of intermediate productivity. In an unrelated
model, Loeuille and Leibold (2008a) studied the evolution of plant defences in
response to specialist and generalist herbivores, along a gradient of productivity.
As with the other models, regional diversity was higher when the steepness of
the productivity gradient was intermediate. Local diversity was again highest
and trophic structure most complex in areas of intermediate productivity. In
Box 6.6, we discuss more thoroughly how this model can be used to explore
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BOX 6.6 How enrichment and fragmentation interact, illustration
using a plant defence-based evolutionary model
Contemporary ecosystems are often exposed to multiple stressors, but how these
interact is usually difficult to assess. In the case of nutrient enrichment and fragmentation, an important point is that local selective pressures are modified, but
dispersal is also altered. Dispersal and local selective pressures interact in complex ways (Urban et al., 2008). Part of this interaction stems from gene flows that
constrain the genetic variation on which natural selection can apply. Other mechanisms are also involved, such as the modification of community structure due to
the incoming dispersal of new species or when dispersal creates densitydependent effects.
A key condition to tackle this interaction is to consider simultaneously community structure, evolution and space. One example model that fits these
requirements is the one by Loeuille and Leibold (2008a), which studies the evolution of two types of plant defences. One defence is efficient against all herbivores, but has an allocation cost that decreases plant growth rate. The second
defence type is efficient against generalist herbivores, but may attract specialist
herbivores, therefore having an ecological cost. Space is divided in 12 patches
along a gradient of productivity, connected by passive dispersal of herbivores
and plants. Evolutionary dynamics can yield diversification of the defensive strategies, but such a diversification critically depends on the level of dispersal. If dispersal is very high, the plant population has only highly defended morphs (no
diversification), else three functional groups coexist within the metacommunity
(low defences, intermediate defences, high defences). In the latter case, highly
defended morphs are in richer patches, lowly defended morphs in poor patches
and intermediate defences are observed mainly in intermediate patches. The
degree of spatial overlap of these three functional groups depends again on
the level of dispersal in the metacommunity. As shown in Fig. 6.8, these evolutionary dynamics constrain the architecture of the local food webs.
Using these results (Fig. 6.8), it is possible to illustrate how fragmentation—
implemented as a decrease of dispersal—and nutrient enrichment interact to
affect the local structure of food webs. Arrow 1 shows that the effects of fragmentation can be impressive while you stand in a location of poor productivity. At
first, fragmentation has a positive effect on diversity, because it increases spatial
structure along the productivity gradient. Subsequently, diversity is lost as only
locally adapted morphs are maintained in the patch. Arrows 1 and 2 show how
this effect of fragmentation depends on the productivity of the patch: in a rich
patch (arrow 2), fragmentation does not affect the local food web at all as such
patches are dominated by highly defended morphs regardless of the dispersal
level.
Continued
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Nicolas Loeuille et al.
BOX 6.6 How enrichment and fragmentation interact, illustration
using a plant defence-based evolutionary model—cont'd
Figure 6.8 Food web architecture as constrained by the evolution of plant defences in
a metacommunity. Each web is supported by a limiting inorganic nutrient (triangle) on
which plants (circles) feed, supporting herbivores (squares). The white circle is a plant
species whose evolution is not considered. For the other (evolving) plant, the shade of
grey gives the quantity of defence the plant has at evolutionary equilibrium, from lowly
defended (pale grey) to highly defended (black). At the start of the simulations, the
white herbivore is a generalist feeding on both plants while the black herbivore specializes on the evolving plant species. The initial food web architecture therefore resembles the middle web of the left column. Arrows (1) and (2) show two contrasted
fragmentation scenarios, arrows (3) and (4) show two enrichment scenarios, as detailed
in the text. Adapted from Loeuille and Leibold (2008a).
Similarly, effects of enrichment will depend on the level of fragmentation in
the system. If the dispersal is very small (arrow 3), increasing the richness of the
patch first increases diversity, but then decreases the complexity of the food web.
Note that such a bell shape relationship between complexity and productivity is
commonly observed in ecology, in models as in experiments or empirical works
(Kassen et al., 2000; Mittelbach et al., 2001; Chase and Leibold, 2002). However, it
is not observed when enrichment happens in a very well-connected metacommunity (arrow 4). Then, neither local diversity nor local trophic structure
is modified by nutrient enrichment.
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the management of existing interactions between nutrient enrichment and fragmentation, two common side-effects of agricultural activities.
4.6. Land sparing versus land sharing, from an evolutionary
point of view
The pros and cons of land sparing versus land sharing have been discussed
in detail from many different viewpoints: economic, ecological, agricultural,
political, etc. (Fischer et al., 2011; Green et al., 2005; Hodgson et al., 2010;
Tscharntke et al., 2005). Here, we ask whether one of these two solutions is
overall likely to perform better than the other, considering eco-evolutionary
dynamics. This is particularly important because these management strategies involve large-scale modifications of landscapes over several decades, a
timescale over which evolution needs to be considered, given the strength
of selection agriculture imposes on natural systems. Before we explore the
benefits and costs of the two options, let us reconsider the spatial consequences of the two choices, which differ in the amplitude of the environmental gradient (large for the sparing strategy, lower for the sharing strategy),
and the level of spatial aggregation (high for sparing, lower for sharing)
(Fig. 6.7). Considering these characteristics, land sharing appears to be a
more sensible option in the light of eco-evolutionary models, for three main
reasons.
The first concerns the management of pest evolution. In the land-sparing
solution (Fig. 6.7, left panel), high pesticide inputs equate to high selective
pressures on the enemies of the cultivated species, so they are likely to evolve
resistance in just a few generations (Carrière et al., 2010; Gassmann et al.,
2009; Gould, 1991). The use of no-pesticide refuges is already widely
applied to fight the spread of resistance (Carrière et al., 2010), based on many
evolutionary models (Bourguet et al., 2013; Tyutyunov et al., 2008; Vacher
et al., 2003). Under land-sharing management, patches of natural habitats
readily provide many refugia in which resistance will be counter-selected.
In the land-sparing choice, agricultural fields are aggregated, so high selective pressures and limited availability of and connectivity with refugia make
the appearance and maintenance of resistance much more likely.
The lessons of evolutionary models for the maintenance of diversity and
the complexity of communities also suggest that land sharing is a safer
choice. As evolution along a gradient of productivity of intermediate
steepness is more favourable to the emergence and maintenance of species
diversity (Doebeli and Dieckmann, 2003), locations of intermediate productivities should contain maximum phenotypic diversity (Hochberg and van
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Baalen, 1998) and the most complex food webs (Loeuille and Leibold,
2008a, Box 6.6). The gradient associated with land sparing is likely to be
too extreme to maintain diversity, and intermediate locations are absent
(Fig. 6.7). Land sharing, on the other hand, provides a shallower gradient
with many locations of intermediate productivity, creating a spatial structure
that may harbour high diversity.
A third reason why land sharing may be a better solution is linked to the
results of the geographic mosaic of co-evolution. Due to gene flows, hotspots can drive the co-evolution at larger scales, even when rare, if selection
is sufficiently strong (Gomulkiewicz et al., 2000). Under land-sparing management, it is likely that this condition is met because very intensive agriculture concentrates on part of the landscape, so selective pressures there will be
high for any species present. Hence, if these exploited locations are hotspots
for some species co-evolution—not an unlikely scenario because few species
will coexist in such high-input, fragmented landscapes, so their reciprocal
interactions will be relatively more important—these will influence
co-evolutionary dynamics throughout the landscape. Essentially, this means
that what is considered ‘land sparing’ may not really be sparing species
co-evolution in space.
We must point out, however, that the black-hole sink model (Holt et al.,
2003) gives a more nuanced answer concerning the relative benefits of land
sharing and land sparing. For instance, with the spatial heterogeneities
depicted on Fig. 6.7 for a species that is best suited to the natural area in
the land-sparing situation, the cultivated area is likely to be very unsuitable,
creating a very strong black-hole sink. Adaptation to the sink will be very
slow to arise, a drawback from a conservation point of view (although from
a land-sparing perspective, these areas were not designed to support biodiversity in the first place). In land-sharing scenarios, cultivated areas are more
wildlife-friendly and closer to natural conditions, so they may still be sinks,
but less strong. Adaptation should therefore be faster, allowing some species
to persist in the exploited areas. Now consider a cultivated species, for which
the reverse reasoning can be made. In land-sparing scenarios, this species will
never adapt to the natural environment, because it will be a very black-hole
sink, and because the species evolves through artificial selection. But in the
land-sharing scenarios, evolution of the cultivated species will have to
account for conditions closer to the ones existing in semi-natural areas.
Environmental conditions vary less spatially, so some of the cultivated species may adapt to the natural locations or gene introgression may become
more frequent. Therefore, from an evolutionary point of view, it is quite
Eco-Evolutionary Dynamics in Agroecosystems
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possible that land sharing eventually produces new ‘invasive species’ (or at
least large introgressions) in the embedded semi-natural areas.
5. PERSPECTIVES AND CHALLENGES
In this chapter, we have taken recent insights gained from general ecoevolutionary models and applied them to agricultural perspectives. On the
one hand, attempting such an exercise represents a stretch because community evolution models are general, while agricultural questions are precise
and embedded in real field situations. However, as exemplified by the
land-sharing versus land-sparing debate, there is a need for agriculture to
set a general strategy for sustainability to complement smaller-scale political
decisions. General questions and debates do also exist regarding agriculture
sustainability, how it is constrained, and community evolution models can
be useful when these general questions arise. It is therefore desirable to try to
adapt certain features of these mechanistic models to the agricultural context,
to obtain more appropriate answers to these questions.
The spatial heterogeneity of environmental conditions in agricultural
landscapes is often quite different from that assumed in community evolution models. Some locations are agricultural fields and some others are natural habitats and transitions between the two are quite abrupt. Variations in
location type and environmental characteristics should be modelled accordingly, rather than on a continuous environmental gradient, a choice that is
often favoured in community evolution models (Dieckmann and Doebeli,
1999; Doebeli and Dieckmann, 2003; Norberg et al., 2012). Also, simply
varying environmental conditions may not be sufficient. In agricultural
fields, the cultivated species often account for most of the local biomass,
so to model efficiently such situations, it is important to have the dominant
species and species composition varying—again abruptly—across the landscape. The metacommunity framework is a suitable starting point for developing such evolutionary approaches (Urban et al., 2008), but adapting it
fully to suit agricultural settings more effectively will involve some further
efforts (Massol and Petit, 2013, Chapter 5 of this volume).
Another possible issue concerns the modelling of evolutionary dynamics.
Individual-based selection drives evolution in wild species, while cultivated
species are most often selected based on yield, a group property. In Box 6.2,
we study co-evolution, combining individual selection for the wild species
and group selection for the cultivated species in a simple two-species model.
The results differed greatly from the initial individual selection model, and
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the robustness of the simple two-species community decreased markedly.
To understand the co-evolution between cultivated species, based on
human choice, and wild species, these differences in selection regimes need
to be built into appropriate models in the future. If we can simultaneously
adapt landscape structure and selection regime to agricultural constraints, the
geographic mosaic of co-evolution could provide important new perspectives on pest management (Bousset and Chèvre, 2013).
Another necessary improvement is to gain better assessments of evolutionary speed driven by artificial selection for cultivated species relative to
other species in the landscape. Superficially, it would seem that artificial
selection, with breeding programmes and genetic tools, would produce
faster evolution for cultivated species, with the evolutionary dynamics of
wild species lagging behind, but this is not necessarily true. In fact, the
development of new traits, new seeds or new species for agriculture is faced
with many constraints, ranging from the research time needed to develop
these, to the health regulations to sell them. Once on the market, it is in
the interest of companies that sell them to maintain them for a sufficient
amount of time and in a sufficiently large number of places, so that the initial
investment is compensated. Clearly, such marketing constraints favour the
replacement of many genotypes by just a few recently engineered (Bonneuil
et al., 2012). This decrease in genetic diversity in turns diminishes the potential for fast evolution in the future. Sociological issues may also be involved:
the reluctance of some populations regarding some engineering tools (e.g.,
GMO) has clearly slowed down their use in some parts of the world.
Similarly, legislation (e.g., on the exchange of seeds) also constrains the
speed of evolution for cultivated species. For all these reasons, evolutionary
speed may not be so fast as is commonly perceived for most cultivated
species. It is, however, abrupt, as it may introduce new genes or traits on
very large scales in very short times when new varieties are chosen. That
intensive agriculture still uses so much input emphasizes that artificial
selection has failed to provide cultivated species adapted to local conditions
and their variations. Evolution of wild species on the other hand is very variable in speed and depends on the genetic variability, population size, mating
system and generation time of the organism involved (Frankham, 1996;
Leimu et al., 2006; Loeuille, 2010b; Soulé, 1976). It is important to
bear in mind here that agricultural pests, whether they are soil
pathogens (Burdon and Thrall, 2009), insect herbivores (Carrière et al.,
2010) or weeds (Gould, 1991), all have large population sizes and short
generation time, allowing them to adapt rapidly to changes imposed by
Eco-Evolutionary Dynamics in Agroecosystems
397
agriculture. Many other species (pollinators, predators, etc.) do not have
such traits and therefore cannot evolve at a similar pace, which might help
to partially explain their declines in agricultural landscapes. The assessment
of evolutionary speed is clearly critical for the associated modelling and if
species are expected to evolve on similar time scales, a co-evolutionary
model is most appropriate. On the contrary, if a subset of species evolves
sufficiently slowly, it is possible to ignore their evolution for short or intermediate term questions, decreasing the complexity of the model and increasing its robustness.
The development of adequate models can help to address important challenges. One of them is the consideration of agricultural change in the context
of other global scale disturbances. A large literature exists on the effects of climate change, and the understanding of multispecies system responses to global
change has been the subject of considerable research (Hagen et al., 2012;
Ledger et al., 2013; O’Gorman et al., 2012; Raffaelli and White, 2013).
Understanding of the evolutionary aspects and dispersal constraints,
of climate change, are also just starting to emerge (Le Galliard et al., 2012;
Norberg et al., 2012; Kubisch et al., 2013; Moya-Laraño et al., 2012). Because
agriculture drives changes in habitats, in species composition and in fragmentation, it interacts strongly with climate change disturbances and joint studies
of these two aspects are clearly urgently needed. This interaction between
agricultural modifications and CO2-related disturbances also involves fertilization management, and several experiments have shown how CO2 and
nutrient loads interact to create unexpected responses in wild communities
(Langley and Megonigal, 2010; Reich, 2009).
Finally, a lot of work remains to be done to understand how ecoevolutionary dynamics affect our perception of ecosystem services. As
shown in Boxes 6.3 and 6.5, it is quite possible that the selective pressures
we exert on a community (e.g., nutrient enrichment or weed removal) affect
an a priori unrelated ecosystem service (biological control). Ecosystem services constrain the future sustainability of agriculture, but also the extent
to which we can rely on ecological intensification (Doré et al., 2011;
Malézieux, 2011) or the benefits we would gain from land sharing.
Trade-offs existing between different phenotypic traits may naturally couple
different ecosystem services together: for instance, plant chemistry simultaneously affects the repulsion of some herbivores, the attraction of others
(Müller-Schärer et al., 2004; Van Zandt and Agrawal, 2004), the attraction
of enemies (Poelman et al., 2008), and of pollinators (Adler et al. 2006; Adler
et al., 2012). These chemical traits clearly couple pest management with
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pollination and biological control ecosystem services, and some defences,
such as tannins, simultaneously decrease plant growth rate and change the
litter degradability (Grime et al., 1996; Whitham et al., 2003). Evolution
then affects two ecosystem services: food provision, and long-term maintenance of soil organic matter. In the light of evolutionary trade-offs, it is
important to develop models that investigate this coupling of various ecosystem services. Adequate community evolution models could be a great
step forward, and agricultural issues could therefore provide important inspiration for the development of future theoretical models in evolutionary
ecology.
The implications of eco-evolutionary dynamics are increasingly being
considered in theoretical and applied ecology: The American Naturalist
recently devoting a complete issue on this subject, for instance. It opens
many new doors to important contemporary ideas whose social and economic implications could be very valuable in the near future. For instance,
the development of adaptive dynamics models, and more generally the consideration of eco-evolutionary feedbacks opened many new doors in our
understanding of anti-biotic resistances (Day, 2001), of the evolution of parasite virulence (Alizon and Lion, 2011) or of vaccination strategies (Gandon
and Day, 2007) in the field of biomedical research into human health. Similarly, the development of eco-evolutionary approaches in an agricultural
context can unveil many new of the currently unknown consequences of
artificial selection, the management of crop pests, and the sustainability of
ecosystem services.
ACKNOWLEDGEMENTS
In addition to INRA, IRD, UPMC and CNRS that routinely support our research, the
authors acknowledge the financial support of the Region Ile de France (DimAstrea grant
allocated to N. L. and G. K.) and of the INRA metaprogram SMaCH (C. L.). We thank
François Massol and an anonymous referee for their interesting comments on an earlier
version of this text.
APPENDIX A. EVOLUTION OF THE INVESTMENT
INTO NUTRIENT UPTAKE, EFFECTS ON
EMERGENT FUNCTIONING
The simple three-compartment model describes the recycling of a
limiting nutrient between primary producers (V), dead organic matter
(D), and the stock of inorganic nutrient (N). Details can be found in the original article (Boudsocq et al., 2011). The nutrient is recycled within the
Eco-Evolutionary Dynamics in Agroecosystems
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ecosystem via internal recycling rates: the primary producer mortality rate
(dv), the mineralization rate of dead organic matter (md), and the uptake
of the mineral nutrient by V (g). Nutrient inputs are fixed and occur in
organic (Rd) and mineral (I) forms. Nutrients are lost from the ecosystem
with fixed rates, respectively lv, ld, and ln for the V, D and N compartments.
lv accounts for losses of nutrients through fires in terrestrial ecosystems or
harvest in agricultural systems. Dead organic matter and its content in nutrient can be lost through fires, erosion, and leaching (dissolved organic matter)
(ld). Mineral nutrients are lost through leaching or denitrification (ln).
Finally, if the limiting nutrient is nitrogen and if there are nitrogen-fixing
primary producers (leguminous plants, some cyanobacteria), we assume that
fixation leads to an inflow of nutrient proportional to the primary producer
biomass (fv). In addition, we define primary productivity as:
’ ¼ gNV þ fv V
ðA1Þ
The system of differential equations reads:
dN
¼ md D þ I ðgV þ ln ÞN
dt
dV
¼ gNV ðdv þ lv fv ÞV
ðA2Þ
dt
dD
¼ dv V þ Rd ðmd þ ld ÞD
dt
Using Eq. (A2), the formulas for the non-trivial ecological equilibrium
can be derived:
N0 ¼
V0 ¼
D0 ¼
dv þ lv fv
g
md
Rd
þ I ln N 0
md þ ld
ðdv þ lv fv Þð1 bÞ
dv
Rd þ ðI ln N 0 Þ
dv þ lv fv
ðA3Þ
ðmd þ ld Þð1 bÞ
dv
md
that can be considered as the recycling efficiency
dv þ lv fv md þ ld
of the ecosystem.
with b ¼
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We assume that the evolutionary dynamics is constrained by a trade-off
between the uptake of nutrient and nutrient losses by plants:
g ¼ g0 ebs
dv ¼ dv0 ecs
ðA4Þ
s is the evolving trait that affects positively the investment into nutrient
uptake. b and c determine, respectively, the benefit and the cost of additional
investment into mineral nutrient uptake.
To predict evolutionary dynamics, we use the Adaptive Dynamics
framework (Dieckmann and Law, 1996; Geritz et al., 1998). In adaptive
dynamics, the relative fitness of a rare mutant sm in a population s at its ecological equilibrium emerge from the demographic dynamics:
1 dVm WVm ðsm ,sÞ ¼
¼ gðsm ÞN 0 ðsÞ ðdv ðsm Þ þ lv fv Þ
ðA5Þ
Vm dt Vm !0
We thus get:
WVm ðsm ,sÞ ¼ g0 ebsm
dv0 ecs þ lv fv
ðdv0 ecsm þ lv fv Þ
g0 ebs
ðA6Þ
To reach an evolutionary equilibrium the selection gradient must be
null:
@WVm ðsm ,sÞ
¼ dv0 ecs ðb c Þ þ bðlv fv Þ ¼ 0
ðA7Þ
@sm
sm !s
If lv > fv and c > b, there is thus a unique evolutionary equilibrium or
singular strategy:
1
bðlv fv Þ
ðA8Þ
s ¼ ln
c
ðc bÞdv0
We focus here on this particular case (realized R ) but two other cases are
possible: tragic R (b > c, runaway evolution that leads to the asymptotic
extinction of the species) or explosive R (c > b and fv > lv, the evolutionary
dynamics lead to a situation where the limiting nutrient accumulates up to a
level where it is no longer limiting).
Once the evolutionary singularity is determined (Eq. A8), it is possible to
determine whether this singularity is convergent (in the sense that selective
pressures favour strategies that are closer to the evolutionary equilibrium)
Eco-Evolutionary Dynamics in Agroecosystems
401
and whether it is invasible (in the sense that alternative strategies can invade
the evolutionary singularity). Convergence and invasibility in adaptive
dynamics emerge from the second derivatives of the relative fitness
(Geritz et al., 1998). Given that:
!
@ 2 WVm
¼ bc ðlv fv Þ
@s2
sm !s!s
ðA9Þ
!
@ 2 WVm
¼ bc ðlv fv Þ
@s2m
sm !s!s
it is shown that the singular strategy is convergent and non-invasible: it is a
continuously stable strategy (CSS). This means that the evolutionary dynamics eventually lead to this strategy and stop there.
dN 0 @N 0 ds
¼
Finally, it is possible to show that the sign of
is always negdt
@s dt
ative (see appendix 4 in Boudsocq et al., 2011), so that the singular strategy s
minimizes the availability of mineral nutrient and nutrient losses. Expressing
0
0
@’
and @V
@s
@s s!s , it can also be shown that the CSS neither maximizes
s!s
primary productivity nor plant biomass (see Appendix 5 in Boudsocq
et al., 2011).
Finally, for the numerical simulations (Fig. 6.1A of the present chapter), we
use fv ¼ 0.01 year1, lv ¼ 0.1 year1, ln ¼ 0.05 year1, ld ¼ 0.0077 year1,
dV0 ¼ 0.275 year1,g0 ¼ 0.0137 ha kg1 year1, md ¼ 0.0766 year1,
I ¼ 6 kg ha1 year1, Rd ¼ 6.7 kg ha1 year1, b ¼ 1, c ¼ 1.735.
APPENDIX B. MIXING GROUP SELECTION AND
INDIVIDUAL SELECTION IN
CO-EVOLUTIONARY MODELS
The model described in Loeuille et al. (2002) considers a nutrient
explicit version, including recycling processes, of plant–herbivore
co-evolution. As shown in the original article, plant population at equilibrium is determined by the herbivore characteristics:
V0 ¼ (dh/w), where dh is the intrinsic mortality rate of herbivores and w is
the herbivore consumption rate. The model further assumes that plant
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defences sv decrease this consumption rate w, while herbivore trait sh
increases the investment of the herbivore in consumption, at the expense
of mortality costs. Incorporating such traits, one gets:
V0 ¼
dh ðsh Þ
:
wðsh ,sv Þ
Because defences decrease the consumption rate w, in terms of phenotype variation, selecting phenotypes sv that produce higher total yield V0
means selecting higher values of sv. We point out that this result is true
for many other models describing plant–herbivore interaction, provided that
they use prey-dependent functional responses for plant consumption and
that herbivore mortality is density-independent.
APPENDIX C. EFFECTS OF ENRICHMENT ON THE
CONTROL OF BIOMASS WITHIN A
TRI-TROPHIC FOOD CHAIN WHEN THE
HERBIVORE EVOLVES
We extend the model of Loeuille and Loreau (2004) by adding a
predator level. This makes the model much more relevant to some
agricultural questions, as biological control exerted by enemies of herbivores
is primordial for a sustainable agriculture. The ecological dynamics of the
system follow the set of ordinary differential equations:
8 dN
>
¼ I ln N þ ð1 vv Þdv V þ ð1 vh Þdh H þ 1 vp dp P gNV
>
>
>
dt
>
>
>
>
>
dV
>
>
>
< dt ¼ V ðgN dv wH Þ
dH
>
>
¼ H ðwV dh aP Þ
>
>
>
dt
>
>
>
>
dP
>
>
>
: dt ¼ P aH dp
ðC1Þ
where variables N, V, H and P correspond to the pool of limiting inorganic
nutrient, plant biomass, herbivore biomass and predator biomass, respectively. All compartments are expressed in mass units of limiting nutrient.
I corresponds to the mass of nutrient input per unit of time in the system,
ln is the diffusion rate of the nutrient out of the system, vx is the proportion
Eco-Evolutionary Dynamics in Agroecosystems
403
of the nutrient of species x that is recycled within the system, dx is the turnover rate of the biomass of species x (which combines the basic death rate of
individuals, but also nutrient excreted by individuals, as well as dead tissues)
and g, w, a represent the individual consumption rates of plants, herbivores
and predators, respectively.
By setting the right side of Eq. (C1) to zero it is possible to determine the
coexistence equilibrium. This equilibrium reads:
N0 ¼
wH 0 þ dv
g
aðIg dv ln Þ þ dp dh g vp vh wdp ln
V ¼
gwdp vp þ gadv vv
dp
H0 ¼
a
0
P0 ¼
ðC2Þ
wV 0 dh
a
Here exponent 0 stands for ‘ecological equilibrium’. It is possible to show
that, as soon as nutrient input is sufficient to maintain the coexistence equilibrium, that is to say, as soon as P0 > 0, this coexistence equilibrium is stable.
The critical value of nutrient input needed to maintain the full food chain is:
wdp ln þ gdh dp vh
ln dh vh
I>
þ dv
þ
ðC3Þ
ga
g
w
Once this value is reached, further enrichment affects the equilibrium
biomass of the food chain as:
@N 0
¼0
@I
@V 0
a
¼
@I
adv vv þ wdp vp
@H 0
¼0
@I
ðC4Þ
@P 0
w
¼
@I adv vv þ wdp vp
Equation (C4) is simply obtained by differentiating Eq. (C2) with respect
to nutrient input rates.
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Nicolas Loeuille et al.
Equation (C4) indicates that nutrient enrichment benefits plant and
predator biomass, while insect pests (here herbivores) are controlled by their
enemies. Therefore, the ecological dynamics of the system produces a desirable outcome from an agricultural point of view, with the cultivated organism benefitting from the enrichment and enemies are kept in check through
biological control. Such variations of the nutrient stocks are completely consistent with those uncovered in previous works on food chains (Loeuille and
Loreau, 2004; Oksanen et al., 1981).
Now, we consider that herbivores evolve. We assume a trait x that
corresponds to the investment of herbivores in defences against their
predators. We voluntarily keep this trait as general as possible. It may
simply be some toxicity or morphologies that would help the herbivore
to escape predation, but also behaviours that would allow herbivores to
escape their predators (vigilance, use of alternative habitats, etc.). The
only assumption we make is that evolution towards higher values of
this trait decreases the growth or reproduction of the herbivore. In mathematical terms, we assume that trait x can be any real value, and it affects
simultaneously w and a such that both are now decreasing functions of
the trait. That is:
x2R
w ðxÞ < 0
a0 ðxÞ < 0
0
ðC5Þ
Again, to maintain the desired level of generality, we do not explicit
functions a and w so that the following results do not depend on a priori fixed
trade-off shapes. We study the evolution of x using adaptive dynamics (see
Appendix A for the details of this technique). Individual fitness readily
emerge from population dynamics (Eq. C1):
1 dHm W ðxm ,xÞ ¼
¼ wðxm ÞV 0 ðxÞ dh aðxm ÞP 0 ðxÞ
ðC6Þ
Hm dt Hm !0
Evolutionary singularities are therefore determined by:
@W ðxm ,xÞ
¼ 0 , w0 ðx ÞV a0 ðx ÞP ¼ 0
@xm xm !x
ðC7Þ
In Eq. (C7), x corresponds to the value of the phenotype at the evolutionary singularity and V and P correspond to the plant and predator biomasses at this singular trait. Computing the exact position of x requires
Eco-Evolutionary Dynamics in Agroecosystems
405
defining more precisely the trade-off, that is to say, to define precisely the
functions a(x) and w(x). This is unnecessary for our argument, so we will
just assume that at least one value of x exists that satisfies Eq. (C7). Would
it not be the case, evolutionary dynamics would produce ever increasing or
ever decreasing values of x. Eventually, such runaway dynamics would
induce the extinction of the predator (evolutionary murder) or of the herbivore (evolutionary suicide).
Assuming that x exists, it is now necessary to check whether evolution
will lead to an end at this point or not. The strategy cannot be invaded
provided:
@ 2 W ðxm ,xÞ
< 0 , w00 ðx ÞV a00 ðx ÞP < 0
ðC8Þ
@xm 2 xm !x!x
The convergence condition can be determined from the following
condition:
@ 2 W ðxm ,xÞ
@ 2 W ðxm ,xÞ
þ
<0
@xm 2 xm !x!x
@xm @x xm !x!x
!
@V P
@P
@x x
<0
ðC9Þ
, w00 ðx ÞV a00 ðx ÞP þ a0 ðx Þ
V
@x x
If the evolutionary singularity satisfies Eqs. (C8) and (C9) simultaneously, then the evolutionary singularity is called a CSS. Selection then
drives x towards the singular strategy x and eventually stops at this point.
Note that conditions (C8) and (C9) are not necessarily fulfilled. The
trade-off shape and density-dependent effects of the trait x play a critical role
in that respect. Then, it is possible that evolution runs away from the strategy. Alternatively, it is possible that evolution leads to the singularity, but
that it is invasible, so that a diversification occurs through branching processes. These possibilities are interesting, but we can only understand
how enrichment affects the evolutionary equilibrium when this equilibrium
exists and is reached, so that we focus only on CSS cases. More complicated
dynamics are beyond the scope of the present analysis.
So we assume that conditions (C8) and (C9) are met. Phenotype x then
eventually stabilizes at x , defined by Eq. (C7), and we disturb the system by
increasing nutrient inputs. Again, differentiating equilibrium conditions (C2) together with the evolutionary equilibrium condition (C7),
one gets the following variations:
406
Nicolas Loeuille et al.
@N a0 H dh @x
¼
@I
gaV @I
@V aV ðw00 V a00 P Þ @x
¼
@I
@I
a0 dh
@H a0 H @x
¼
@I
a @I
@P
w @V ¼
@I a @I
@x
a2 a0 gdh V ¼ 02 2
@I
a dh dp ðln þ gvh V Þ a2 gV ðw00 V a00 P Þ wdp vp þ adv vv
ðC10Þ
Recalling from condition (C5) that a0 < 0, and from condition (C8) that
w V a00 P < 0, and recalling that other parameters and variables of the
model are all positive, it is easy to see from the first four lines of Eq. (C10) that
N , V , H and P all vary in the same direction as x when nutrient input rate I
is increased. Again from inequalities (C5) and (C8), it is easy to see that the
right-hand side of the last line of Eq. (C10) is positive, so that x increases
when I increases. It follows from all these considerations that when nutrient
enrichment takes place, all biomasses increase, regardless of the trophic level,
and that the herbivore trait of investment in defence increases too. Therefore,
while the herbivore pest is controlled by its predator from an ecological
dynamics point of view (see Eq. C4), it is no longer controlled when we allow
evolution of defences for this herbivore. Its population does increase throughout enrichment (Eq. C10), due to this evolutionary effect. The combination
of nutrient enrichment and of the evolutionary process decreases the biological control exerted by herbivores. Next to the qualitative analysis given here,
an example of such an effect is displayed on Fig. 6.3 in Box 6.3. To realize this
figure, we had to fix a trade-off shape. We assumed that:
00
aðxÞ ¼ a0 eka x
wðxÞ ¼ w0 ekw x
ðC11Þ
Trade-off Eqs. (C11) have the advantage that, by varying ka and kw one
can get a linear, convex or concave relationship between a and w, so that the
complete variety of evolutionary outcomes are possible, including CSSs.
Parameter values we use for the figure are the following: ln ¼ 0.06,
Eco-Evolutionary Dynamics in Agroecosystems
407
vv ¼ 0.13, vp ¼ 0.3, vh ¼ 0.3, dv ¼ 0.95, dp ¼ 0.75, dh ¼ 0.4, g ¼ 2.7, w0 ¼ 1.4,
a0 ¼ 4.5, kw¼0.12, ka¼0.13.
APPENDIX D. ECO-EVOLUTIONARY DYNAMICS IN
A PLANT–HERBIVORE–PREDATOR
CONFRONTED TO INSECTICIDES
Using ordinary differential equations we study the influence of insecticides on a three-species community as the following:
8
1 dV
>
>
¼ r aV wH
ðD1Þ
>
>
V dt
>
>
>
>
< 1 dH
ðD2Þ
¼ cwV aP dh lj
H dt
>
>
>
>
>
1 dP
>
>
ðD3Þ
>
: P dt ¼ gaH dp lh
The model describes a community composed of one plant V, one herbivore H, and one predator P. The plant dynamics (D3) is constrained by the
intrinsic growth rate (r) and intra-specific competition a. Hence, in the
absence of the herbivore, the plant has a logistic growth. We used Holling
type I functional responses to model the consumption interactions, w being
the per capita attack rate of herbivores, c the energy conversion efficiency of
the herbivore, a the per capita attack rate of predators, and g the conversion
efficiency of this predator. Herbivore and predator dynamics also decrease
through interaction-independent death rates (respectively, dh and dp) and
through an additional mortality term, due to the action of insecticides.
The parameter l represents the intensity of insecticide application and
j and h correspond to the sensitivities of herbivores and predators, respectively. The two populations are therefore confronted to the same perturbation, to which they respond differently because of their specific sensitivities.
By setting the time derivatives in Eqs. (D1), (D2) and (D3) to zero, the
equilibrium points of the three-species model can be fully determined. The
plant–herbivore–predator model has four equilibrium points. Existence
condition requires that species densities at equilibrium are positive. We also
assess the stability of these points, with the Routh–Hurwitz criterion.
The trivial equilibrium S1 ¼ (V0 ¼ 0; H0 ¼ 0; P0 ¼ 0) always exists, but it
is unstable when r > 0, a situation that is most often true given that the plant
is cultivated.
408
Nicolas Loeuille et al.
The plant equilibrium point S2 ¼ (V0 ¼ r/a; H0 ¼ 0; P0 ¼ 0) always exists
and it is stable when the perturbation by insecticides is strong enough to prevent the herbivore to invade the system. This requires:
aðlj þ dh Þ > wcr
ðD4Þ
The third equilibrium point allows the coexistence of plant and herbivores. At this equilibrium S3, plants and herbivores have the following density equations:
lj þ dh
wc
aðlj þ dh Þ þ wcr
H0 ¼
w2 c
V0 ¼
ðD5Þ
ðD6Þ
Out of Eq. (D5) one clearly sees that the plant biomass is always positive.
Therefore, existence conditions are based on the positivity of herbivore
biomass. This requires that:
aðlj þ dh Þ < wcr
ðD7Þ
The Routh–Hurwitz criterion shows that this plant–herbivore equilibrium point is stable when mortality incurred by predator population through
pesticides is high:
agaðdh þ ljÞ > w w dp þ hl þ agr c
ðD8Þ
Finally, it is possible that all three species coexist at one equilibrium,
where density equations are
w dp þ hl þ agr
0
ðD9Þ
V ¼
aga
dp þ hl
H0 ¼
ðD10Þ
ag
w w dp þ hl þ agr c agaðdh þ ljÞ
0
P ¼
ðD11Þ
a2 ga
All the three species have positive densities when predator biomass (D11)
is positive. This is ensured by the following condition:
ðD12Þ
agaðdh þ ljÞ < w w dp þ hl þ agr c
The Routh–Hurwitz criterion for a system of three ordinary differential
equations shows that the system is stable when condition (D12) is satisfied.
Eco-Evolutionary Dynamics in Agroecosystems
409
We now assume to study how these ecological equilibriums change
when more insecticides are used. By computing the partial derivatives of
equilibrium equations with respect to l, we can solve analytically how the
densities of the different species will vary with an increase in perturbation
intensity l.
When the community does not contain the predator, the partial derivatives of Eqs. (D5) and (D6) with respect to l are
@V 0 j
¼
@l
wc
0
@H
aj
¼ 2
@l
wc
ðD13Þ
ðD14Þ
Thus, when the intensity of perturbation increases, plant biomass
increases while herbivores are negatively affected.
We similarly study changes in the full coexistence equilibrium (Eqs. D9–
D11):
@V 0
wh
¼
@l
aga
0
@H
h
¼
@l
ag
0
2
@P
w hc þ agaj
¼
@l
a2 ga
ðD15Þ
ðD16Þ
ðD17Þ
At the coexistence equilibrium, the plants and predator biomasses
decrease with an increase in insecticide use, while herbivores increase.
Comparisons of Eqs. (D13 and D14) and of Eqs. (D15–D17) highlight
the fact that the efficiency of pesticide use strongly varies with the number of
trophic levels. When the system is composed of two levels, then using pesticide yields the intended result, namely the decrease of the pest population
and the increase in yield. When the system is composed of three trophic
levels and when the top trophic level is sensitive to insecticide, using them
erodes the biological control of pests and has adverse effects from an agricultural point of view.
Now that we have obtained the effects of insecticide disturbances on the
ecological equilibrium and highlighted that qualitative variations are dependent on the number of trophic levels, we study how evolution of agricultural
pests (here, herbivores) change such qualitative outcomes.
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Nicolas Loeuille et al.
As pointed out in the main text, the emergence of resistance in pests is
often associated with fitness costs (Bourguet et al. 2004; Carrière et al., 1994;
Gassmann et al., 2009). Particularly, studies have shown that resistance most
often decrease the allocation in growth or reproduction (Bourguet et al.
2004; Carrière et al., 1994). To consider this trade-off, we add in our
plant–herbivore–predator community a sensitivity trait for the herbivore
that affects both its mortality due to insecticides and its reproduction rate.
The model becomes
8
1 dV
>
>
¼ r aV wH
ðD18Þ
>
>
V
dt
>
>
>
>
< 1 dH
ðD19Þ
¼ c ðsÞwV aP dh l ðsÞj
H dt
>
>
>
>
>
1 dP
>
>
ðD20Þ
>
: P dt ¼ gaH dp lh
The two functions j(s) and c(s) are positive, increasing function of s. The
lower the value of s, the more resistant the pest is, but the higher the reproduction cost. We choose exponential functions for c and j, because they satisfy the different assumptions and also for mathematical convenience:
c ðsÞ ¼ c0 expðvsÞ
jðsÞ ¼ j0 expðzsÞ
ðD21Þ
ðD22Þ
The ratio v/z controls the shape of the trade-off. By varying their relative
values, we can have a large panel of trade-off shapes, from convexity to concavity. When the trait of interest and the associated trade-off are set, we use
adaptive dynamics to determine the resulting eco-evolutionary dynamics
(see Appendix A for an introduction of this technique).
We first study the case where only plants and herbivores coexist. The fitness
of a rare mutant s0 in a resident population of trait s can then be determined:
1 dHm 0
¼ c ðs0 Þ wV 0 ðsÞ dh ljðs0 Þ
ðD23Þ
W1 ðs , sÞ ¼
dHm dt Hm !0
with V0 ¼ (lj(s) þ m)/ac(s), the density of the plant at the equilibrium fixed by
the resident trait.
The associated fitness gradient that determines the direction of change of
the trait is
411
Eco-Evolutionary Dynamics in Agroecosystems
@W1 ðs0 , sÞ
¼ vdh þ ljðsÞðv zÞ
@s0 s0 !s
ðD24Þ
From Eq. (D24), two qualitative possibilities emerge, depending on the
trade-off shapes. If v z the fitness gradient is always positive. The sensitivity
of herbivore s always increases during the evolution. When v < z, the fitness
gradient can be positive or negative depending on the resident trait value. Singular strategies may then be obtained, at which the gradient of fitness is null.
Such a singular strategy is given by the following equation:
1
vdh
s1 ¼ log
ðD25Þ
j0 lðz vÞ
z
As in Appendices A and C, we study the invasibility and convergence characteristics of this singular strategy. Recalling that we have v < z, we obtain:
@ 2 W1 ðs0 , sÞ
dh vzðv zÞ
¼
<0
ðD26Þ
2
0
zv
@s
s0 !s!s
1
Because this second derivative is negative, the singular strategy cannot be
invaded by surrounding mutants.
It can be easily shown that:
@ 2 W1 ðs0 ,sÞ
¼0
ðD27Þ
@s0 @s s0 !s!s
1
The sum of Eqs. (D26) and (D27) is always negative, which ensures that
the singular strategy is convergent, that is, evolution drives the system
towards this point. The evolutionary singularity is therefore a CSS.
We now characterize the evolutionary dynamics when all three species
coexist. The invasion fitness of a mutant herbivore is:
W2 ðs0 , sÞ ¼ wV 0 c ðs0 Þ aP 0 ðsÞ dh ljðs0 Þ
The fitness gradient becomes
@W2 ðs0 ,sÞ
¼ wV 0 c 0 ðsÞ lj0 ðsÞ
@s0 s0 !s
The singular strategy, at which the gradient vanishes is
1
j0 lz
log
s2 ¼
vz
c0 wvV 0
ðD28Þ
ðD29Þ
ðD30Þ
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Nicolas Loeuille et al.
Note that, in Eq. (D28), plant biomass is not dependent on the resident
trait. Therefore, it is easy to see that @ 2W(s0 , s)/@s0 @s is equal to zero. Then,
as in the plant–herbivore case, characteristics of the evolutionary singularity
only depend on the second derivative with respect to s0 :
@ 2 W2 ðs0 , sÞ
2
0
2
z
ðD31Þ
¼
v
wV
c
s
lj
s2
2
2
@s0
s0 !s!s2
Inserting Eq. (D30) in Eq. (D31) shows that it is a decreasing function of
z and that it vanishes for z ¼ v. Because at the evolutionary
singularity, the system is also at equilibrium from an ecological point of
view, wV 0c(s ) ¼aP0(s ) þdh þ lj(s ). Equation (D31) becomes
@ 2 W2 ðs0 , sÞ
ðD32Þ
¼ v2 aP 0 s2 þ dh þ v2 z2 lj s2
2
0
@s
s0 !s!s2
Equation (D32) is positive for v > z.
Therefore, the second partial derivative of invasive fitness with respect to
0
s is positive for v > z, vanishes for v ¼ z and is negative for v < z. We conclude from this that the singular strategy in this model is a repellor when the
trade-off is convex (v > z) and a CSS when the trade-off is concave (v < z).
The repellor situation leads to a runaway dynamics on which we cannot easily study the influence of increased pesticides. For the CSS cases, on the
other hand, evolution eventually settles the trait at s2 and we can study
the effects of increased pesticide use by linearizing around this equilibrium
situation.
To study the influence of increased pesticide use, we differentiate
equations of the singular strategies s1 and s2 (Eqs. D25 and D30) regarding
pesticide use parameter l.
When the system only contains plants and herbivores, effects of pesticide
use on the position of the singular strategy are determined by the following
equation:
@s1 1
¼
@l
lz
ðD33Þ
In such instances, the singular strategy always decreases when pesticide
use increases. From an agricultural point of view, it means that we expect
evolution of further resistance in all instances when more insecticide is
sprayed.
413
Eco-Evolutionary Dynamics in Agroecosystems
When the three species coexist, variations in the singular strategy with
pesticide use are determined from the following equations:
wdp agr
@s2
¼ @l l w dp þ hl agr ðv zÞ
ðD34Þ
@s2 wl
¼ @h
w dp þ hl þ agr ðv zÞ
ðD35Þ
Note that again, given condition of coexistence (D12), when the singular
strategy is a CSS, it decreases with l, meaning that increased pesticide use
allows for evolution of higher levels of resistance. The sensitivity of the predator also affects on the singular strategy. The singular strategy decreases with
predator sensitivity h. In agricultural terms, it clearly indicates that sensitive
predators allows for higher levels of resistance in the pest crop.
APPENDIX E. EVOLUTION OF SPECIALIZATION RATE
OF THE PEST AND ITS ECOLOGICAL
CONSEQUENCES
We tailor the model of Leibold (1996) to fit the agricultural scenario of
an insect-pest feeding on two plant types, one weed and one crop, which in
their turn compete over a common soil resource. The ecological dynamics
of this system follow the set of ordinary differential equations:
dH
¼ H hc xc þ xοc Vc þ hw xw þ xοw Vw dh
dt
dVc
¼ Vc vc gc R wc þ woc H dc
dt
dVw
¼ Vw vw gw R ww þ wow H dw
dt
dN
¼ I lN gc NVc gw NVw
dt
ðE1Þ
Where woi and wi (i ¼ c, w) denote the plant and herbivore-dependent parts of
the plant–herbivore interaction; when the plant is maximally defended,
woi ¼ 0. Note that we suppose these density-dependent effects are additive.
The herbivore-dependent part wi can also be interpreted as degree of specialization on the target plant i. Other variables and parameters have been
defined in Appendix C. The only additional parameters appearing in this
414
Nicolas Loeuille et al.
model are the conversion efficiencies in the functional responses of the pest
and the two plant species (hc, hw, vc, vw).
Here, we make some fairly realistic and general assumptions about the crop
and the weed species. First, crop most often requires fertilization to grow and
survive, so that we assume the crop is poor competitor for the resource comdw
dc
pared to the weed (i.e.,
<
). We also assume that the crop species is
vw gw vc gc
relatively less vulnerable to herbivores owing to its enhanced herbivore resistance favoured during breeding efforts (woc < < wow so that ww þ wow > wc þ woc).
In other words, while the crop is mostly limited by the resource, the weed is
mostly limited by the pest. Theoretically, the stable coexistence of the two
competing plant species is assured when the following two conditions are
met: (i) the ratio of resource effects and herbivore effects on the per capita
growth of the crop species is higher than the same ratio of effects on the
vc gc vw gw
per capita growth of the weed (i.e.,
>
, where Xi ¼ wi þ wοi ),
Xc
Xw
(ii) the ratio of weed impacts on herbivore and resource growth is higher than
hw Xw H hc Xc H
>
) (Leibold, 1996).
the same ratio of crop impacts (i.e.,
gw R
gc R
The coexistence equilibrium of the set of Eqs. (E1) reads as follows:
0
1
hw Xw I lN 0
hc Xc I lN 0
dc dw
dh B Xc Xw C 0 dh gw
N0
g
N0
0
CV ¼
c
V
N0 ¼ B
¼
w
@vc gc vw gw A c
hc Xc hw Xw
hw Xw hc Xc
gc
gw
Xc
Xw
gc
gw
gw
gc
0
1
dc
dw
B
v
g
v
g
v
g
v
c
w
w gw C
wB c c
C
H0 ¼ c
ðE2Þ
@
v
g
v
c
w gw A
c
Xc Xw
Xc
Xw
Note that the equilibrium biomass of the crop (weed) increases
@Vw0
@Vc0
< 0,
> 0)
(decreases) linearly with the resource input rate I (i.e.,
@I
@I
whereas the equilibrium biomasses of the resource and the pest remain
@H 0 @R0
unchanged (
,
¼ 0).
@I @I
Now, we consider that the pest evolves. In specific, we assume that the
degree of specialization on the crop (wc) coevolves with the degree of specialization on the weed (ww) in a traded-off manner. This trade-off can be
Eco-Evolutionary Dynamics in Agroecosystems
415
explained in terms of energetic limitations: the energy spent in searching and
handling of one plant type comes to a cost for searching and handling of the
other one. Again we assume that a trait x affects both traits and ww such that
w0 c ðxÞ > 0, then w0 w ðxÞ < 0.
Next, we follow the methodological steps of adaptive dynamics, as introduced in appendix A. First, we define the relative fitness of a rare variant xm
in a population x as follows:
ðE3Þ
WH ðxm ,xÞ ¼ hc wc ðxm Þ þ wοc Vc0 þ hw ww ðxm Þ þ wοw Vw0 dh
The evolutionary singularity of the above fitness function is obtained by
setting the first derivative of the above fitness function to zero:
@Wh ðxm ,xÞ
¼ 0 , hc w0c ðx ÞVc þ hw w0w ðx ÞVw ¼ 0
ðE4Þ
@xm xm ¼x¼x
where x denotes the singular strategy and Vc , Vw correspond to the equilibrium biomass of the crop and the weed at the singularity, respectively.
Then, the invasibility of the singular strategy x can be determined by the
following condition:
@ 2 Wh ðxm ,xÞ
< 0 , hc w00c ðx ÞVc þ hw w00w ðx ÞVw < 0
ðE5Þ
@x2m
xm ¼x¼x
The convergence stability of the singular strategy can be determined
from the following condition:
@ 2 Wh ðxm ,xÞ
@ 2 Wh ðxm ,xÞ
þ
<0
@x2m
@xm @x xm ¼x¼x
xm ¼x¼x
ðE6Þ
@Vc Vc @Vw 00 00
<0
, hc wc ðx ÞVc þ hw ww ðx ÞVw þ hc
@x x Vw @x x
It follows that the singular strategy represents a CSS when both specialization rates saturate with increasing x (i.e., w00c ðxÞ,w00w ðxÞ are negative). We
focus on the CSS case and again look at the adaptive changes generated in the
equilibrium biomasses of the model compartments when we perturb the system by changing input rate I (e.g., due to fertilization). Noting, as in the
other appendices, the ecological equilibrium by 0 and the evolutionary equilibrium by , the adaptive responses of species biomass to the above perturbation were calculated to have the following signs (explicit formulas are not
provided because of their complexity):
416
Nicolas Loeuille et al.
@H @V 0 @V @V 0 @V @R
> 0, c > c > 0, w < w < 0,
>0
@I
@I
@I
@I
@I
@I
ðE7Þ
and
@H @Vc0 @Vc
@Vw0 @Vw
@R
< 0,
>
> 0,
<
< 0,
<0
@dw
@dw @dw
@dw @dw
@dw
Several things are worth noticing in the above line of inequalities: first,
the perturbation parameter I generates a positive effect on trait x, which
translates to a positive effect on the trait wc and a negative one on the trait
ww. Second, the ecological effect of a change in I on plant biomasses is moderated by the evolution of specialization (See Fig. 6.6). Therefore, consistent
with results detailed in other appendices, these last results suggest that using
purely ecological models may give over-optimistic results compared to the
complete eco-evolutionary feedbacks. Third, the evolution of specialization
enforces the top-down control of the herbivore, which results in a positive
response of the herbivore’s biomass to fertilization.
To realize Fig. 6.6, we had to fix a trade-off shape. We assumed that:
1=z
wc ðxÞ ¼ wmax
c x
1=z
ww ðxÞ ¼ wmax
, where x 2 ½0,1
w ð1 xÞ
ðE8Þ
The parameter z measures the strength of the trade-off; when z > 1 the
trade-off is weak (w00c ðxÞ,w00w ðxÞ are negative) and when z < 1 the trade-off is
strong (w00c ðxÞ,w00w ðxÞ are positive).
Parameter values we use for the Fig. 6.6 are the following: hc ¼ 0.5,
hw ¼ 0.7, wc max ¼ 1, wc 0 ¼ 0.01, ww max ¼ 1, ww 0 ¼ 0.1, dh ¼ 0.1, dc ¼ 0.4,
dw ¼ 0.2, vc ¼ 0.5, vw ¼ 1, gc ¼ 0.6, gw ¼ 0.3, l ¼ 0.1, z ¼ 1.5.
GLOSSARY
Ecological network a complex set of species linked by interactions of different types:
direct/indirect, trophic/non-trophic, mutualistic/antagonistic. The complexity characterizing an ecological network constrains species ecological dynamics and adaptive
responses to disturbances.
Fitness (individual) number of reproducing offspring left by an individual during its
lifetime.
Adaptability ability of a population to cope with environmental variations through genetic
change (natural selection, gene flows), phenotypic plasticity or behavioural change.
Natural selection a gradual, non-random process by which phenotypic/genotypic traits
change in frequency as a function of fitness differences among their bearers. Important
features of selection include:
Dimensionality number of selective pressures operating simultaneously,
Eco-Evolutionary Dynamics in Agroecosystems
417
Intensity difference between maximum and minimum fitness within the population. It
depends on environmental changes/fluctuation, changes in the ecological context, gene
flow, etc.
Group selection (in the case of agriculture, Artificial Group Selection) selection
based on the fitness of the group rather than individual fitness; this may result in fixation
of traits disadvantageous to the individual itself, provided there is some heritability of the
group property under selection.
Artificial selection human-driven selection of organisms favouring those with desirable
characteristics, for example, for cultivation and use. These characteristics may be negatively linked to organism fitness.
Adaptive change/response a phenotypic change (with a genetic or non-genetic basis) that
improves the fitness of individuals relative to average fitness within the population; it can
be limited by allocation or ecological trade-offs.
Allocation trade-off beneficial changes in one trait cause detrimental changes in another
due to energetic or time constraints within an individual.
Ecological trade-off beneficial changes in a species response to one interaction incur costs
from another interaction (e.g., plant defences against herbivores may have detrimental
effects on pollination); the higher the complexity of an ecological network the more
important these trade-offs are.
Domestication outcome of the artificial selection process linked with cultivation by
humans of plants and animals.
Diffuse co-evolution allelic/phenotypic changes occurring within the frame of an ecological network, that is, species evolve in response to a number of other species of the network, each of which is also evolving in response to another set of species (Janzen, 1980).
Contemporary (or rapid) evolution allelic/phenotypic change occurring in natural ecosystems on a short time frame
Eco-evolutionary feedback situation in which the ecological context constrains natural
selection, while resulting evolution affects the ecological context through changes in species density, species interactions or the environment.
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