Journal of Animal
Ecology 2007
76, 669–678
Evolutionary responses to harvesting in ungulates
Blackwell Publishing Ltd
G. PROAKTOR, T. COULSON and E. J. MILNER-GULLAND
Division of Biology and Centre for Population Biology, Imperial College, Silwood Park, Ascot,
Berkshire, SL5 7PY, UK
Summary
1. We investigate the evolutionary responses to harvesting in ungulates using a statedependent, stochastic, density-dependent individual-based model of red deer Cervus
elaphus (L.) females subject to different harvesting regimes.
2. The population’s mean weight at first reproduction shifts towards light weights as
harvesting increases, and its distribution changes from a single peak distribution under
very low or high harvest rates, to a bimodal distribution under intermediate harvest
rates.
3. These results suggest that, consistent with previous studies on aquatic species,
harvesting-induced mortality may drive adaptive responses in ungulates by reducing
the fitness benefits from adult survival and growth in favour of early and lightweight
reproduction.
4. Selective harvesting for heavy animals has no additional effect on the evolutionarily
stable strategy, suggesting that harvest rate is more important than the degree of selectivity
in driving adaptive responses. However, selective harvesting of light females is positively
associated with maturation weights even higher than those of a nonharvested population,
probably due to the reduction in the fitness value of the offspring.
5. The average number of weight at maturation strategies in the population declines but
the total number of strategies across all simulations increases with harvest rate, suggesting
that harvesting-induced selection on weight at maturity overcomes the increase in
strategy diversity expected from density-dependent release.
6. Yield initially increases with harvesting due to enhanced productivity of light females
experiencing density-dependent release. However, it crashes under intense harvesting
resulting in a population skewed to light, young and, therefore, less reproductive animals.
Key-words: adaptive changes, deer, hunting, reproductive strategies, selection.
Journal of Animal Ecology (2007) 76, 669–678
doi: 10.1111/j.1365-2656.2007.01244.x
Introduction
Harvesting has been linked to demographic changes in
many wild populations, such as skewed age structure
and reduced life-expectancy (Langvatn & Loison 1999),
fluctuations in population size (Myers et al. 1995;
Solberg et al. 1999) and skewed sex ratio (Ginsberg &
Milner-Gulland 1994; Saether, Solberg & Heim 2003).
Harvesting has also been implicated in evolutionary
changes in heritable traits (Ricker 1981; Stockwell,
Hendry & Kinnison 2003; Hutchings 2004). For example,
Hutchings (2005) suggested that overexploitation of
the North-west Atlantic cod Gadus morhua (L.) over
the past 40 years has caused a significant reduction in
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Correspondence: G. Proaktor, Division of Biology and Centre
for Population Biology, Imperial College, Silwood Park, Ascot,
Berkshire, SL5 7PY, UK. E-mail: [email protected]
age and length at maturity. The majority of studies on
the evolutionary consequences of harvesting have
focused on commercially important fish populations
due to the financial interest in such consequences
and the wealth of data on their biological, ecological
and demographic characteristics (Law 2000; Ratner &
Lande 2001). However, it is unclear if evolutionary
responses to harvesting observed in fish also affect
terrestrial species. Moreover, as fishing mortality is
usually selective according to one or more phenotypic
traits (Stergiou & Erzini 2002), it is yet to be established
what the relative contributions are of harvest rate
and the degree of selectivity to the overall harvestinginduced adaptive changes.
Ungulates are heavily harvested throughout the
world for both meat and trophies (Milner-Gulland &
Clayton 2002; Milner-Gulland, Coulson & CluttonBrock 2004). While numerous studies have illuminated
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G. Proaktor, T.
Coulson & E. J.
Milner-Gulland
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
669–678
the demographic consequences of harvesting for many
populations of ungulates (Gaillard, Festa-Bianchet &
Yoccoz 1998; Coulson et al. 2004), only a few studies
have focused on the evolutionary aspects of harvesting,
mainly in males (Fitzsimmons, Buskirk & Smith 1995;
Coltman et al. 2003). Regarding females, anecdotal
evidence from other terrestrial species, for example
the red kangaroo Macropus rufus (L.), suggests that
selective harvesting of large individuals may drive the
evolution of lighter weights at maturity and adulthood
(Tenhumberg et al. 2004). The key factor that may be
responsible for the evolution of lighter weights is the
increase in mortality due to harvesting, resulting in
a negative correlation between weight and age at
maturity and successful reproduction. Whether
harvesting-induced mortality drives the evolution of
a lighter weight at maturity in ungulates, or prevents
it due to the release from competition driven by the
reduced densities of harvested populations, is yet to be
established. Moreover, research on the evolutionary
implications of harvesting for management and conservation of ungulates has almost exclusively focused
on male traits. Therefore, the time-scale for genetic
recovery of female-related traits, such as the weight
at first reproduction, is unknown but important for
decision makers. Evidence from fish populations
suggests that genetic recovery from harvesting may take
much longer than demographic recovery (Hutchings
2000).
A major difficulty in addressing these issues is the
lack of detailed data sets on harvested populations that
span a sufficiently long time for evolutionary changes
to occur. This can be partially overcome using computer
models that enable investigations over evolutionary
time-scales. Another advantage is that the same model
can simulate a range of different harvesting scenarios,
and control factors such as immigration that may
interact with harvesting-induced effects. In particular,
individual-based models have been demonstrated as
a useful tool for addressing demographic and evolutionary aspects of harvested populations (Witting
2002).
In this paper, we investigate the evolutionary effects
of different types of harvesting on reproductive
strategies in red deer females. We use a state-dependent
individual-based model (IBM) that optimizes females’
reproductive strategies in a stochastic density-dependent
environment. The model excludes males because the
focus here is on female life-history traits, namely reproductive strategies. Initially, we test the hypothesis that
the mean weight at first reproduction declines when
harvest rate increases. We also test the hypothesis that
selective harvesting of heavy females selects for lighter
weights at maturity, and selective harvesting of light
females select for heavier weights at maturity. Testing
these hypotheses sheds light on whether harvestinginduced adaptive changes in ungulates are primarily
driven by the rate or the degree of selectivity of harvesting. Next, we explore the effects of harvesting on the
diversity of reproductive strategies. While moderate
levels of harvesting, like other types of anthropogenic
or natural disturbances, may increase biotic diversity
(Connell 1978), it is unclear whether harvesting generates
evolutionary changes in the diversity of reproductive
strategies within a single population, and between
different populations. Finally, we examine if these
responses to harvesting change the potential harvesting
yield, and discuss the implications for management
and conservation.
Methods
 
The IBM developed here is a state-dependent model
which is used to optimize weight-specific reproductive
strategies of red deer females in a stochastic densitydependent environment (Fig. 1). Accumulation of
weight is modelled as a proportional share of the
available food resources to all nonsuckling individuals
in the population (Appendix S1, see Supplementary
material). Offspring up to age 6 months suckle from
their mothers and therefore their weight gain is
modelled as a function of the mother’s body weight
(Appendix S1). Each offspring inherits her reproductive strategy from her mother with a certain chance
of mutation (Appendix S2). Reproduction is traded
against survival (cost of reproduction) through its
negative effect on the female’s body weight (Appendix
S2), which in turn determines the female’s probability
of survival to the next year (Appendix S3). The distribution of reproductive strategies evolves when
females with suboptimal strategies are out-competed
by females with strategies that are more suitable to
the environmental conditions. Females with better
strategies produce on average more viable copies of
their particular strategy hence, have a greater lifetime
reproductive success. Any combination of weightspecific strategy can emerge through mutation. This
enables the model to evolve the set of reproductive
strategies that is most suitable for the simulated conditions. The focus on body weight captures the link
between density-dependent and independent environmental conditions and reproduction on the one hand,
and survival and future reproduction on the other
(Hancock, Milner-Gulland & Keeling 2005). This
IBM provides a link between individual phenotypes
(reproductive strategy and state), and population
dynamic processes. It is unusual because it incorporates
inheritance of reproductive strategies within a realistic
model of population dynamics, a characteristic that
makes this model particularly suitable for understanding evolution of reproductive behaviour in complex
systems, where individual body condition is intimately
linked to reproductive decisions and success (Boyd
2000).
Two aspects of harvesting are incorporated in the
model: absolute offtake rate (harvest quota) and the
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Evolutionary
responses to
harvesting in
ungulates
Fig. 1. A schematic diagram of the weight-based individual-based model of red deer females.
level of selectivity towards animals according to their
weight. The potential of harvesting for generating
evolutionary changes in the reproductive characteristics
of red deer females is initially assessed for random
harvesting, and subsequently for selective harvesting.

© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
669–678
A given proportion, q, of the population is harvested
each year. Based on q and on the population size, n, the
total number of individuals harvested, h, is removed
from the population at the beginning of the year before
they have a chance to reproduce. Harvesting is modelled
in two ways. First, by a linear function of weight whereby
the probability of a given individual being harvested,
ζ, is:
ζ = ψ × a × Wi,t + d
eqn 1
where ψ is a scaling constant for weight selectivity, a
and d are constants, and Wi,t is the weight of individual
i at time t. When ψ = 0 harvesting is nonselective
with respect to weight and therefore individuals are
harvested at random. When ψ > 0 the probability of a
given female being harvested increases linearly with her
weight, and when ψ < 0 it declines with weight. The
degree of selectivity for harvesting heavy or light
animals is directly proportional to the value of ψ.
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G. Proaktor, T.
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Milner-Gulland
Table 1. The parameters modified under different harvesting scenarios
Parameter
Description
Values
q
a
d
ψ
Harvest rate
Slope of weight-selective harvesting
Intercept of weight-selective harvesting
Multiplication factor for weight-selective harvesting
0·1, 0·2
0·0125, –0·0125
– 0·4475, 1·6500
0, 0·8, 1·0, 1·2, 1·3
Eqn 1 is applied to individuals chosen randomly from
a uniform distribution, so each individual has an equal
probability of being harvested. This procedure continues
until the number of harvested individuals equals h.
We also model the evolutionary effects of harvesting
directed exclusively at individuals whose weight falls
within a specific range. We choose the mean weight at
first reproduction of a population randomly harvested
at a rate of 10% as a reference weight point, and calculate
harvest quotas for different weight classes above and
below that point. We chose this specific reference
weight point in order to examine whether and to what
extent harvesting-specific weight intervals may have an
additional effect to random harvesting. A given female
is therefore harvested only if her weight falls within the
specific weight interval chosen for harvesting in the
current simulation. Individuals whose weights fall
within that specific weight interval are harvested at
random and this process continues until the number of
harvested animals is either equal to h or the total
number of animals in that weight interval.
 
The effects of harvesting on model predictions are
assessed by comparing model results under different
harvesting regimes to a base-case nonharvesting
scenario. Two absolute offtake levels and a range of
values for weight selectivity are simulated by modifying
two parameters, ψ and d (Table 1). The second type of
harvesting is implemented using a range of 5 kg weight
intervals within the range of 45 –90 kg. For each scenario
the model is run for 500 simulations of 400 years, which
is sufficient for convergence in all simulations. Values
for reproductive and demographic characteristics of
the population are recorded at the end of the last year
of each simulation, and for each scenario a mean
value of each characteristic over the 500 simulations
is calculated.
 
Estimation of model parameters is based on published
data from studies of different red deer populations,
particularly data from the Isle of Rum (Clutton-Brock
1984), and from Slowinski NP in Poland (Dzieciolowski
et al. 1996). However, these data are limited in their
generality because often parameter estimates are
specific to the focal population of each study. Therefore
it is important to assess how robust the model is to
variation in parameter values. Following McCarthy,
Burgman & Ferson (1995), we fit linear regressions
between parameter values and model predictions to
determine the sensitivity of the predictions to parameter
values, after checking for linearity of response. We use
uniform distributions for generating values within
a range of 15% above and below the values specified
in Table 1. Based on these distributions we draw 200
random sets and run 50 simulations for each set of
parameters. Each of the 50 × 200 simulations is run for
200 years, sufficient for the model to converge on an
equilibrium. The mean weight at first reproduction at
the final year of each simulation is reported. We then
calculate the mean equilibrium weight at first reproduction across simulations for each set of parameter values,
and subsequently use these means as the predicted
values in the regressions.
Results
   
© 2007 The Authors.
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Ecological Society,
Journal of Animal
Fig. 2. The
Ecology,
76,distribution of weight at first reproduction that evolves under three random
harvest rates: no harvesting, 10% random harvesting, and 20% random harvesting.
669–678
The distribution of the weight at first reproduction
is strongly affected by the rate of random harvesting
(Fig. 2). The distribution’s mean declines from 79·12 kg
in a nonharvested population to 72·3 kg and 67·6 kg in
lightly (10%) and heavily (20%) harvested populations,
respectively. The distribution shifts towards lighter
weights and changes from near normal with a peak at
81 kg in the nonharvested population to a skewed
673
Evolutionary
responses to
harvesting in
ungulates
Fig. 3. Changes in the number and relative frequency of peaks
in the optimal distribution of weight at first reproduction with
harvest rate.
distribution with a peak at 65 kg in the heavily harvested
population. Under intermediate harvest rates, the
distribution consists of both peaks. This suggests that
there are two groups of strategies with different means
and distributions of weight at first reproduction.
Fig. 4. The added effects of selective harvesting to the mean weight at first reproduction
of a 10% random harvested population. The effect is calculated as the percentage
difference between the mean weight at first reproduction of the selective and randomly
harvested populations. Negative values indicate a lighter mean weight at first reproduction relative to the mean of a randomly harvested population (67·6 kg). x-axis values
show the mean weight of the selectively harvested groups of individuals. Horizontal
lines indicate the corresponding averages for the nonharvested and the 10% randomly
harvested populations.
Table 2. The additional effect on the mean weight at first reproduction of selective
harvesting over that of random harvesting, shown for 10% and 20% harvest rates. A oneway  is used to assess significant differences between means
Type of selectivity
Harvest rate
© 2007 The Authors.
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Increase
with weight
10%
© 2007 British
20%
Ecologicalwith
Society,
Decrease
weight
10%
Journal of Animal
20%
Ecology, 76,
*Indicates
669–678 a significance level of P < 0·05.
% change from the mean of
a randomly harvested population
– 0·5
0
+ 4·5*
+ 4·6*
A further examination of the evolutionary process
reveals that the transition from a single peak to a double
peak distribution occurs at harvest rates of approximately 7% (Fig. 3). As the rate of harvesting further
increases, the relative frequency of the 81 kg peak
declines in favour of the 65 kg peak. Overall, a bimodal
distribution of the weight at first reproduction can
persist at harvest rates of approximately 7–15%. Above
these rates the distribution evolves back to a single
peak.
We also assess the evolutionary potential of selective
harvesting by comparing adaptive changes under
selective harvesting with those observed under random
harvesting. There is no significant difference between
the means of the weight at first reproduction under
random and selective harvesting, when selectivity is
positively related to body weight (Table 2). However,
the mean weight at first reproduction increases when
the probability of being harvested declines with weight
under both low and high harvest rates. These results
suggest that the trade-off between the relative contribution to fitness of the mother’s survival and the
number of offspring is weak when mainly heavy animals
that have already reproduced are harvested. In contrast,
when mainly light animals are harvested, selection
favours more offspring at the expense of the mother’s
survival.
Next, we assess how the direction and extent of
the adaptive response to harvesting depend on the
deviation between the mean of selectively harvested
individuals and the mean weight at first reproduction
of a randomly harvested population (72·3 kg). There
is a strong negative effect on the weight at first reproduction, of up to 6%, when harvested animals weigh
slightly above the reference point (Fig. 4). As the mean
weight of harvested animals further deviates from that
point, the added effect becomes increasingly negative;
i.e. the mean weight at first reproduction increases
beyond the reference point. The increase in the average
weight at first reproduction of the selectively harvested
population is more rapid when the harvested animals
are lighter rather than heavier than the reference point.
When the average harvest weight is only 59·5 kg the
average weight at first reproduction increases beyond
that of a nonharvested population. When increasingly
heavy animals are harvested the resulting increase in
the weight at first reproduction is asymptotic to the
mean of a nonharvested population. This is because
increased selectivity means that fewer animals can be
harvested, hence the impact of harvesting declines.
  
An assessment of how the number of strategies varies
between populations subject to different levels of
harvesting may provide first, a qualitative assessment
of the direction and strength of the selection operating
in each population and second, an indication whether
there are just few or many possible different strategies
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Milner-Gulland
Fig. 5. The average number of weight-specific reproductive strategies in a population per simulation, and the total number of
different strategies evolved over 500 simulations, under three harvesting scenarios: no harvesting, 10% random harvesting, and
20% random harvesting.
Fig. 6. Changes in yield (mean ± SD of kg live meat) shown for random harvest and selective harvest of heavy animals (> 100 kg).
© 2007 The Authors.
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Ecological Society,
Journal of Animal
Ecology, 76,
669–678
that can persist under each level of harvesting. Harvesting has a significant negative effect (one-way :
F2,1497 = 382·41, P < 0·001) on the diversity of strategies
within a given population (Fig. 5). The average number
of strategies per population declines progressively from
> 6 strategies in the nonharvested population to < 4
in the heavy harvested population. However, the total
number of different strategies that can potentially
evolve and persist in a population increases with
harvest rate. Whereas, a total of 76 different strategies
evolved in 500 simulations in the nonharvested population, there were 101 and 113 different strategies in the
lightly and heavily harvested populations, respectively.
Harvesting, by reducing population size and thus also
the strength of density-dependent competition, enables
different yet closely related strategies to dominate
similarly harvested populations.
     
Harvest yield (kg live meat) increases with harvest
intensity at low to intermediate rates, with selective
harvesting of heavy animals generating on average
higher yields than random harvesting (Fig. 6). However, under high harvest rates the yield from the
selectively harvested population crashes sooner and
more rapidly than the randomly harvested population,
indicating that harvesting the heaviest females, who are
at their prime age, has a greater effect on productivity
than random harvesting.
 
The average hind weight is dependent primarily on the
maximum weight gain for suckling offspring Lmax, such
that an increase in Lmax results in an increase in the
average weight at first reproduction of the population
(Table 3). This relationship reflects the strong impact
a mother has on offspring survival through her contribution to offspring weight, which is limited by Lmax.
Additional increases in Lmax give the mother greater
potential, based on her weight, for enhancing her own
fitness by influencing her offspring’s survival. The
result is a delay in the onset of reproduction to heavier
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Evolutionary
responses to
harvesting in
ungulates
Table 3. The effect of variation in model parameters on
model predictions. The sensitivities are estimated using linear
regressions of model results obtained by variation in model
parameters. Description of parameters is given in Table S1
(see Supplementary material)
Parameter
Slope direction
P-value
r2
Gmax
u
y
Lmax
b
gjuvenile
gyerling
gsubadult
gadult
+
+
–
+
+
+
+
+
+
0·360
0·645
0·856
< 0·001
0·162
0·638
0·254
0·502
0·380
– 0·001
0·004
0·005
0·064
0·005
– 0·004
0·002
– 0·002
– 0·001
weights when offspring survival is higher. These fitness
benefits from a higher weight at first reproduction are
ultimately limited by the cost of delaying reproduction.
The model is robust to variation in the other parameters
(Table 3).
Hind growth rates are qualitatively comparable
with published rates from the Rum and Slowinski
populations (Fig. 7). Model predictions for young ages
approximate those on Rum and below those in
Slowinski. However, at prime ages the modelled growth
rates approximate the Slowinski rates, which are about
15% higher than on Rum. Different densities, harvesting regimes and weather conditions on Rum result in
the considerably lower weights attained by Rum females.
Discussion
Previous studies have linked observed evolutionary
changes in life histories, such as a decline over a few
generations in mean weight, length and age at first
© 2007 The Authors.
Journal compilation
©Fig.
2007
7. British
A comparison of model predictions against the data used for its
Ecological
Society, shown for mean age-specific weights evolved under 15% annual
parameterization,
Journal
Animal
harvestof
rate.
Data are from a Polish population (Slowinski; Dzieciolowski et al. 1996)
and a Scottish
population (Rum; Mitchell, McCowan & Nicholson 1976). Data are
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available for females at ages 1–10.
669–678
reproduction, to harvesting of wild populations
(Heino 1998; Jennings, Reynolds & Mills 1998; Heino
& Godo 2002). However, most of the long-term detailed
studies on wild harvested populations were conducted
on commercially important fish populations that live
under fairly stable environmental conditions, and
that are subject to strong phenotypic-based selective
harvesting according to length or weight (MartinezGarmendia 1998; Law 2000; Olsen et al. 2005). Using a
stochastic density-dependent IBM for red deer females
we have demonstrated that both random and selective
harvesting can generate adaptive responses in long-lived
iteroparous species. The mean weight at first reproduction
of the simulated harvested population declines and its
optimal distribution shifts towards lighter weights
relative to a nonharvested population, and the extent
of these adaptive changes increases with harvest rate.
The key factor that underpins these adaptive
responses is the increase in mortality due to harvesting
prior to reproduction. Under random harvesting,
individuals that begin reproduction at light weights,
thus at a young age, have on average a greater chance of
reproducing at least once than individuals that begin
reproduction at heavier weights and hence later in life.
Selection for a lighter weight at first reproduction is
therefore likely to increase as the relative contribution
of harvesting to the overall mortality rate increases.
This effect, however, is limited by the trade-off between
reproduction and survival. The fitness benefits from
reproduction at light weights are offset by the increasingly negative effect reproduction has on the mother’s
and offspring’s survival because a light mother can invest
fewer resources in herself and in her offspring than a
heavy mother (Partridge & Harvey 1988; Lindstrom
1999).
The bimodal distribution that evolves under intermediate levels of harvesting suggests that the population
consists of two groups of strategies dominated by
different selection pressures. One mediates primarily
the benefits of reproduction before harvesting and thus
selects for a lighter weight at first reproduction. The
second mediates primarily the benefits of survival and
future reproduction and therefore selects for a heavier
weight at first reproduction. The combined effects of
harvesting-induced selection and natural stochastic
density-dependent processes shift individuals from one
strategy set to the other. Therefore, when harvest rate
is very low or very high the population is dominated by
only one of the groups, meaning the optimal distribution
consists of a single peak. However, under intermediate
harvest rates there are sufficient individuals in each
strategy set to produce a bimodal distribution. These
results reflect the distribution at equilibrium and not
during the transition from a nonharvested single peak
to a harvested bimodal distribution, which depends on
factors such as heritability of traits.
Evidence from harvested red deer populations
indicates that there is considerable variation between
females of the same population in their age and weight
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Ecological Society,
Journal of Animal
Ecology, 76,
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at first reproduction (Mitchell & Lincoln 1973; Guinness,
Albon & Clutton-Brock 1978; Audige, Wilson & Morris
1999). They usually conceive for the first time between
age 2 and 4, and environmental factors experienced by
the females (such as density-dependent competition
for food, climatic conditions, and the degree of uncertainty in these factors; Clutton-Brock & Albon 1983;
Langvatn et al. 1996) interact with harvesting in affecting the individual age and weight at first reproduction.
The relative frequencies of red deer females that
reproduce for the first time at age 2, 3 or 4 can each be
over 15% in a given population, hence there is no clearcut single optimal weight at first reproduction. This
range of reproductive strategies is consistent with our
results for intermediate harvest rates.
Harvesting is often selective against certain individuals according to one or more phenotypic traits,
and different types of selective harvesting might be
expected to generate different adaptive responses
(Jennings, Greenstreet & Reynolds 1999; Law 2000).
We have shown that the probability of being harvested
increasing with weight has no additional effect to the
adaptive changes observed under random harvesting,
suggesting that the harvest rate is more important than
selectivity for weight in driving evolutionary responses
in female ungulates. Furthermore, harvesting only
heavy females reduces the overall evolutionary effect
of harvesting, because these females have already
reproduced several times. In contrast, selection against
females that have just matured should have the largest
potential for generating adaptive responses because
their reproductive potential (residual reproductive value:
Williams 1966), is expected to peak at maturity (Rose
& Charlesworth 1980; Clutton-Brock 1984; Caswell
2001). We demonstrate this as an additional decline
in the mean maturation weight when harvest targets
only recently matured females.
The evolutionary response to harvesting in this
model is mitigated when harvesting is selective for light
and therefore young animals. A reduction in offspring
survival reduces the offspring’s fitness value relative to
that of an adult. Selection is therefore predicted to
favour an increase in adult survival by spreading the
investment in reproduction over a longer time (Bell
1980; Real & Ellner 1992), resulting in the evolution of
a heavier weight at first reproduction. Moreover, when
offspring survival is low, for example due to severe
environmental conditions (Coulson et al. 1997), natural
selection tends to favour a delay in the onset of reproduction and thus, selects for an increase in the weight at
first reproduction (Hirshfield & Tinkle 1975; Stearns
1992).
The negative effect of harvesting on the variability
in weight at first reproduction within the population
suggests a very strong impact of the weight at first
reproduction on fitness. Harvesting selects on two
opposing components, the probability of reproduction
before being harvested, and the survival rates of mother
and offspring. Survival is determined by the mother’s
weight and therefore by the time she has for accumulating resources prior to reproduction. Successful
reproductive strategies under these constraints exhibit
minimal variation in weight at first reproduction, and it
is likely that only few such strategies emerge within a
single population. that the higher the harvest rate the
stronger the selective pressure, and so fewer strategies
persist in the population. The bimodality emerging
under intermediate harvest rates reflects an increase in
variability in strategy frequency, not strategy number.
Harvesting increases the number of reproductive
strategies across many simulations, because when the
population is well below carrying capacity, closely
related strategies have very similar fitness. Harvesting
reduces population size and the strength of densitydependent competition for resources between individuals. Consequently, selection on heavier females is
weaker; these conditions enable different strategies to
dominate on different occasions. Additionally, life span
under heavy harvesting is greatly reduced, implying
that reproduction late in life has on average a lower
expected contribution to fitness. The evolutionary
responses to harvesting also affect yield. It initially
increases with harvest rate due to increased productivity
attributed to lighter maturation weights and densitydependent release. Selective harvesting of heavy
animals has a greater effect on density dependence
and thus on productivity, because heavy individuals
consume more food than light individuals. Under
intense selective harvesting almost no heavy adults are
left and the population becomes skewed to light, young
and hence less reproductive animals.
Our model clearly demonstrates that harvesting can
generate evolutionary responses. However, it does not
consider the genetic level that underlies the response to
selection. The exact direction and strength of the
evolutionary response to harvesting is determined by
gene–gene interactions, and trade-offs with multiple
traits (Roff 1997). Additionally, males may affect
variation in female reproductive strategies by breeding
with females with different strategies, and by influencing females’ conception dates and their reproductive
success (Noyes et al. 2002). As harvesting of males may
generate evolutionary responses in male traits such as
antler size or body weight (Coltman et al. 2003), it may
influence evolutionary responses to harvesting in females.
This study highlights the need for management
plans to consider the potential of harvesting to generate
evolutionary change, as has been advocated in several
previous studies (Kaitala & Getz 1995; Ratner &
Lande 2001; Harris, Wall & Allendorf 2002). In longlived iteroparous species such as red deer, harvesting
should ideally focus on subadult and old females
instead of young adults and prime-age females.
Acknowledgements
We are grateful to R. Hillary and T. Carruthers for
advice on some aspects of this work. This study was
677
Evolutionary
responses to
harvesting in
ungulates
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
669–678
supported by the British Council Lord Goodman
scholarship, the UK Overseas Research Scheme, Ian
Karten scholarship and Imperial College London.
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Supplementary material
The following supplementary material is available for
this article.
Appendix S1. Body-weight.
Appendix S2. Reproductive strategies.
Appendix S3. Survival rates.
Table S1. Parameters used in the IBM of female red deer.
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http://www.blackwell-synergy.com/doi/full/10.1111/
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