Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
Behavioral Ecology (2014), 25(5), 1019–1021. doi:10.1093/beheco/aru082
Anniversary Essay
Behavioral ecology and the successful
integration of function and mechanism
Pat Monaghan
Institute of Biodiversity, Animal Health and Comparative Medicine, Graham Kerr Building, University of
Glasgow, Glasgow G12 8QQ, UK
Received 1 April 2014; accepted 4 April 2014; Advance Access publication 16 May 2014.
Key words: adaptation, biomedicine, causal factors, variation, zoology.
Broadly speaking, researchers working in the field of animal biology can be divided into 2 camps: those who seek to understand
the processes that will enable us to identify, alleviate, and if possible cure, human ailments—that is, the biomedical sciences, and
those who want to understand the processes responsible for the
diversity that we see in animal form and function—that is, the zoological sciences. The approach to variation differs greatly between
the two (Monaghan and Birkhead 2013). For biomedical scientists,
commonality is what they are after, pathways that are highly conserved across species and hence can be easily studied in relatively
simply animals; variation muddies the waters and is something to
be avoided. For the zoological-based scientists, variation within and
among species is a central focus, and an evolutionary framework is
used as the scaffold on which to build an understanding of the origins, consequences, and maintenance of variation. Both approaches
are immensely valuable, but, to the detriment of both, communication between these camps has not been what it should be.
The discipline of behavioral ecology very much has its roots in the
zoology camp. It emerged in the 1970s as an offshoot of ethology
that focused much more on “why” rather than on “how” questions.
The basic approach centered on identifying, quantifying, modeling,
and predicting the fitness costs and benefits of behavior, enabling
good, often surprisingly good, predictions of who does what and
when. The discipline had a bumpy start. It was almost suffocated
at birth by political controversy, criticized for a lack of mechanistic
realism and its growth was retarded by overly simplistic, speculative,
and naive approaches and interpretations (Birkhead and Monaghan
2010). But despite the difficult birth and unsupportive parenting,
behavioral ecology survived and has been tremendously successful.
Surprisingly, Gordon (2011) criticized behavioral ecologists for having an “ambivalent” attitude to variation. She suggested that this
was a legacy from the early ethologists who were not much interested in variation, being focused on “species-specific” behaviors. But
Address correspondence to P. Monaghan. E-mail: Pat.Monaghan@
glasgow.ac.uk.
© The Author 2014. Published by Oxford University Press on behalf of the
International Society for Behavioral Ecology. All rights reserved. For permissions,
please e-mail: [email protected]
ethologists were very interested in interspecific variation and in how
such differences had evolved. It was the move away from detailed
studies of behaviors with low intraspecific variation, such as courtship behavior and imprinting, to behaviors that often differ between
individuals, such as foraging and antipredator behavior, that initially
characterized behavioral ecology (Birkhead and Monaghan 2010;
Westneat 2011). Understanding both inter- and intraspecific variation in behavior and life histories has always been at the heart of
behavioral ecology—whether studies are on the factors shaping
foraging decisions, mate choice, social interactions, host–parasite
interactions, personality, or whatever. The focus on explaining differences enables us to provide new insights into function. Although
there are challenges ahead for the discipline, not least changes in
our understanding of how phenotypic variation is generated and
inherited, this does not include a lack of appreciation of the importance of variation. The broadening of the scope of behavioral ecology, the reuniting of studies from “why” and “how” perspectives,
has resulted in it emerging as one of the most integrative areas of
modern biology. It is important that “market forces,” that is, funding
body preferences and prejudices, do not give rise to a narrowing of
the range of species and phenomena studied.
Why Mechanisms Matter
In the early days of behavioral ecology, 2 of Tinbergen’s 4 questions were largely ignored; the mechanisms underlying variation
in behavior and how behavior developed (Owens 2006; Bateson
and Laland 2013). The focus was on fitness outcomes and the
individual, group, and population level consequences. But the casting aside of these kinds of mechanistic questions was too hasty.
Increasingly, behavioral ecologists have realized that we do need to
understand mechanisms if appropriate trade-offs are to be postulated (Blumstein et al. 2010) and constraints are to be identified.
Partly as a result of the lack of mechanistic investigations, some
trade-offs were postulated and investigated that turned out not to
1020
have a sound physiological basis, such as that between the allocation of carotenoids to sexual coloration and antioxidant defenses in
birds. It was assumed that carotenoids were a limiting resource but
crucial to oxidative defense, when in fact they are not major players
in the avian antioxidant system (Costantini and Moller 2008). The
role of carotenoids in honest signaling appears to be much more
complex than simple trade-off models would suggest (Metcalfe and
Alonso-Alvarez 2010). Understanding of mechanisms can also help
us understand why animals appear to behave in a nonadaptive
way. For example, the multiple functions of hormones could create trade-offs if they have antagonistic effects on fitness traits, constraining what options the animal has (Lessells 2008). To study this
we need to know about hormone action in order to identify what
these trade-offs and constraints might be. For example, the hormone prolactin in birds increases during incubation and promotes
parental behaviors. We know, from detailed studies by early ethologists, that contact with the eggs in many bird species is involved
in the maintenance of high prolactin levels (Vleck 2002). But
prolactin also causes testicular regression. Many male starlings do
not assist their mate with incubation, even though when males do
provide even a small amount of help, breeding success is improved
(Reid et al. 2002). Understanding the mechanistic processes that
constrain the male’s options could help us understand what initially
seems like a nonadaptive behavior. Although the time that males
would need to invest in incubation would not prevent them seeking
other mating opportunities, the act of incubation itself is likely to
shut down sperm production. A trade-off could, therefore, occur
between the fitness benefits for males of remaining fertile and seeking other mating opportunities and the fitness benefits of time spent
incubating. Whether this does occur, and is a direct consequence of
the hormone action, requires more comparative and experimental
studies coupled with a clear understanding of hormone action.
Understanding the development of behavior has also come to be
seen as important for behavioral ecologists. For example, how early
life conditions can shape phenotypic development and influence later
life performance, possibly in a context dependent way, has become
an important area of research. That trade-offs might operate over
long timescales, for example, between the pace of growth and the
pace of late life deterioration, requires us to understand the mechanisms that might produce such links (Metcalfe and Monaghan 2003).
New mechanistic processes that are uncovered by researchers
in other disciplines can open new areas of research in the field of
behavioral ecology. This is particularly marked in the recent studies
that have expanded our understanding of phenotypic development
and inheritance. Understanding the processes whereby genotypes
can display different phenotypes is central to understanding adaptive phenotypic plasticity. Recent work on epigenetic inheritance is
expanding our views on evolutionary processes and has led to call
for an extended theory of evolution (Danchin et al. 2011). Central
tenets of current evolutionary theory—that the transfer of DNA
sequences across the generations is the way in which genome-based
information is transferred from parents to offspring, that changes to
this genetic information occur at random, and that the germ line
and the soma are entirely separate—are being challenged by recent
research on epigenetics, much of which is carried out in the biomedical field (Richards 2006). We now know that, although the DNA
sequence itself might only change as a result of random mutations,
the instructions on how the genome is to be read can be rewritten as
a consequence of environmental effects and that this rewrite appears
to be transferred across the generations. Parent of origin silencing of
gene expression has been known for sometime, but thought not to be
widespread and to be confined, at least in most animals with separate
Behavioral Ecology
germ lines and soma, to a few specific genes. However, recent research
suggests that information acquired during an individual’s lifetime can
be transmitted to offspring by parental gametes. Male mice trained to
associate a particular odor with an aversive stimulus, then mated with
unexposed females, were able to transmit sensitivity to this odor to
their offspring and grand offspring; the intergeneration transfer was
found even when in vitro fertilization was used. The changes were
tracked to hypomethylation of the specific receptor gene for this odor
(Olfr151) in the males’ sperm (Dias and Ressier 2014). How can this
gene expression information get from the soma to the gametes and
remain with the embryos after fertilization when much DNA methylation has been stripped away? The detailed mechanistic processes
underlying this intergenerational transfer remain unknown. But this
expansion of our understanding of the processes of inheritance—
how culture meets genes—provides new and exciting opportunities
for behavioral ecologists to investigate its adaptive significance and the
conditions that have promoted its evolution.
Model Organisms and the Genomic
Age
One potential threat to behavioral ecology and the study of variation is the focus on “model organisms” in the biomedical sciences,
and how this influences research funding bodies. The US National
Institute of Health provides a list of recognized model species, which
comprises 1 plant, 1 fungus, the social amoeba, 2 species of yeast, and
the following 8 animals: 1 nematode (Caenorhabditis elegans), 1 crustacean (Daphnia pulex), 1 insect (Drosophila melanogaster), 1 fish (the zebrafish Danio rerio), 1 amphibian (Xenopus laevis), the chicken (Gallus gallus
domesticus), and 2 mammals (the mouse Mus musculus and the rat Rattus
norvegicus). Taxonomically, it is an odd list. However, these species have
been chosen because they are conveniently small, short lived, have
rapid development and simple social lives, are easy to keep and breed
in captivity, and in some cases, such as the mouse, have a genome that
is easier to manipulate (Bolker 2012). Further selective breeding and
intensive inbreeding have taken place to standardize the animals—
minimize genomic and phenotypic variation within and between individuals and reduce their sensitivity to environmental effects—so that
sample sizes can be kept small. When you buy BALB/c mice, you
know what you are getting. Model organisms are considered good surrogates for many kinds of cellular processes in humans and are generally assumed to represent much more than themselves. Obviously,
for highly conserved cellular pathways, they have proved invaluable.
Fantastic toolkits have been developed that allow detailed studies
of genetic effects on many traits including behavior. But the limited
number of species, their unnaturally low genetic variability, and their
insensitivity to their environment are likely to mean that genomic
effects are overemphasized (Bolker 2012). It also means that they offer
little to the behavioral ecologist because they lack the variability that
enables key questions about function to be addressed.
For behavioral ecologists, the concept of the “representativeness”
embodied in the model species concept seems somewhat ludicrous.
Even among closely related species, we see substantial variation in
behavior and life histories. The surrogate aspect too is difficult to
justify for behavioral studies in particular. Would we consider studying humans in order to get an insight into mouse behavior? I think
not. Nonetheless, Owens in his 2006 paper “Where is behavioural
ecology going” reported with dismay that, between 2001 and 2005,
less that 2% of papers published in the 3 main behavioral ecology
journals used model species. Owens felt that, in order to get the
genetic information he considered essential to the discipline, behavioral ecologists must join “mainstream biology” and make greater
Monaghan • Successful integration of function and mechanism
use of model organisms in order to make progress. Has this happened? A quick check in Behavioral Ecology from 2007 to the present
shows that it has not; the recognized model organisms feature as the
main study organisms in less than 0.5% of papers. In fact, the use
of Drosophila is considered by some to have held back progress in the
study of sexual selection (Zuk et al. 2014), and several researchers
in other areas have recently called for an increase in the diversity of
species studied and for more comparative research (Blumstein et al.
2010; Price et al. 2011; Kronfeld-Schor et al. 2013). Interestingly, the
use of the term “model organism” or “model species” has increased.
Prior to 2000, this was a rarely used phrase but now many authors
refer to their study animal as being a good “model organism” or
“model species.” What exactly is meant by this is rarely clarified.
A wide range of unusual species have been described in this way
in the journal Behavioral Ecology in the past 10 years or so—ranging
from geckos to great bustards, social spiders, and so on. Often, what
the authors probably mean is that the species represents a good
animal in which to test a particular theory because it has a certain
unusual attribute or is easy to study, rather than that it is in some
way representative of a taxon, a way of living or a surrogate for
human studies. Possibly also the use of the term “model species” is
thought to help raise the status of the study species in the eyes of
potential funders (Leonelli and Ankeny 2013).
Combining Function and
Mechanism—The Most Integrative of
the Animal Biology Disciplines
By integrating studies of function and mechanism, working at many
levels of biological enquiry on a wide range of organisms, the discipline of behavioral ecology has grown into the most integrative area
of the biological sciences. It is important that we ensure that it continues to grow and that new frontiers are identified. The value of
the integrative approach that now characterizes behavioral ecology
has recently been recognized for studies of mammalian social behavior (Blumstein et al. 2010). We need to spread the word on its value
more widely and champion the value of studying diversity. We need
to deploy the toolkits provided by the biomedical sciences where we
can and harness studies of mechanisms to help us understand function and evolution. This will involve collaborations with scientists in
many other disciplines and, particularly, biomedical researchers with
whom we might appear to have less in common than with, say, ecologists. Improving communication with biomedicine will enrich both
camps—providing new explanations and approaches to the phenomena under study (Sedivy 2009; Wells and Stock 2011), whether this
be to understanding variation in longevity, responses to parasites, or
to adversity at different life-history stages. We should not be afraid to
apply our knowledge and approach to the study of humans where
appropriate, remembering of course that the extent to which we
can generalize from one species to another is limited, especially for
behavior. But studies of one species can generate predictions that
can be tested in other carefully chosen species. It is important that
behavioral ecology retains its zoological roots, by studying variation
rather than eliminating it, by choosing appropriate study species that
provide new insights and understanding of function and evolution,
and by not losing sight of the fitness outcomes that it seeks to explain.
1021
Funding
European Research Council (AdG 268926).
I thank K. Metcalfe for useful discussions.
Editor-in-Chief: Leigh Simmons
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