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COMMENTARY
Harvesting as a potential selective pressure on
behavioural traits
Martin Leclerc*
,1
, Andreas Zedrosser
2,3
and Fanie Pelletier
1
1
Canada Research Chair in Evolutionary Demography and Conservation & Centre for Northern Studies, D
epartement
de biologie, Universit
e de Sherbrooke, Sherbrooke, QC J1K2R1, Canada;
2
Faculty of Technology, Natural Sciences
and Maritime Sciences, Department of Natural Sciences and Environmental Health, University College of Southeast
Norway, N-3800 Bø i Telemark, Norway; and
3
Department of Integrative Biology, Institute of Wildlife Biology and
Game Management, University of Natural Resources and Applied Life Sciences, Vienna, Gregor Mendel Str. 33,
A–1180 Vienna, Austria
Summary
1. Human activities are a major evolutionary force affecting wild populations. Selective pres-
sure from harvest has mainly been documented for life-history and morphological traits. The
probability for an individual to be harvested, however, may also depend on its behaviour.
2. We report empirical studies that examined whether harvesting can exert selective pressures
on behavioural traits.
3. We show that harvest-induced selection on behavioural traits is not specific to a particular
harvest method and can occur throughout the animal kingdom.
4. Synthesis and applications. Managers need to recognize that artificial selection caused by
harvesting is possible. More empirical studies integrating physiological, behavioural, and life-
history traits should be carried out to test specific predictions of the potential for harvest-
induced selection on heritable traits using models developed in fisheries. To limit selective
pressure on behaviour imposed by harvesting, managers could reduce harvest quotas or vary
harvest regulations over time and/or space to reduce the strength of selection on a particular
phenotype.
Key-words: angling, evolutionary consequences, exploitation, fisheries, gillnet, harvest-
induced selection, hunting, passive and active gear, vulnerability
Introduction
Humans are considered as one of the major selective forces
shaping traits of species (Palumbi 2001) and may cause faster
phenotypic changes than many natural drivers (Hendry,
Farrugia & Kinnison 2008; Darimont et al. 2009). Pheno-
typic changes are particularly drastic when humans act as
predators and harvest wild populations (Darimont et al.
2009). Harvesting can induce selective pressures on wild ani-
mal populations by increasing mortality and by non-random
removal of specific phenotypes. Harvesting has been shown
to induce selective pressure in several species (Allendorf
et al. 2008) that may ultimately result in evolutionary
responses (Jørgensen et al. 2007; Pigeon et al. 2016).
Selective pressure caused by human harvest, hereafter
referred to as harvest-induced selection, has mostly been
documented for life-history and morphological traits and
can be caused by size-selective harvesting. For example,
trophy hunting of male bighorn sheep (Ovis canadensis)
selected for smaller horn size (Coltman et al. 2003; Pigeon
et al. 2016), and size-selective fishing affected the evolu-
tion of life histories in zebra fish (Danio rerio) (Uusi-
Heikkil€
aet al. 2015). In size-selective harvesting, typically
a specific phenotype is targeted leading to harvest-induced
selection. Harvest-induced selection on behavioural traits,
however, can be due to behavioural differences between
individuals affecting their probability of being harvested
(Heino & Godø 2002; Uusi-Heikkil€
aet al. 2008). This
pattern was observed in behavioural studies showing that
the probability of capturing or sampling (for scientific
research instead of harvesting) a specific individual in a
population could be biased due to consistent individual
differences in behaviour, i.e. animal personality (Biro &
Dingemanse 2009; Carter et al. 2012; Biro 2013). These
individual behavioural differences are often heritable
(Postma 2014; Dochtermann, Schwab & Sih 2015).
*Correspondence author. E-mail: martin.leclerc2@usherbrooke.ca
©2017 The Authors. Journal of Applied Ecology ©2017 British Ecological Society
Journal of Applied Ecology 2017, 54, 1941–1945 doi: 10.1111/1365-2664.12893
Humans can therefore, consciously or not, modulate the
evolution of animal behaviour by removing (harvesting)
or reproducing (breeding) specific individuals within a
population (Price 1984). Although important for wildlife
management and conservation, much less attention has
been devoted to harvest-induced selection on behavioural
traits compared to life-history or morphological traits
(Uusi-Heikkil€
aet al. 2008; Heino, D
ıaz Pauli & Dieck-
mann 2015) and to whether this selection may lead to
evolution of behaviours that are different from those
favoured by natural selection (e.g. Olsen & Moland 2011
for morphological traits).
Harvesting as a selective pressure on
behavioural traits
Most of the theoretical work and predictions for beha-
vioural harvest-induced selection are derived from the
fisheries literature. Arlinghaus et al. (2016) suggested that
harvest should select for shyer and more vigilant individ-
uals. In fisheries, predictions made on harvest-induced
selection often depend on the gear type used, and Al
os,
Palmer & Arlinghaus (2012) predicted that passive gear
should select for individuals with lower activity levels. In
sport hunting, a hunter must see an individual of the
species of interest before she/he can select a target ani-
mal based on a morphological trait or a sex/age class.
Therefore, we hypothesize that behavioural traits that
increase vulnerability or visibility, such as selection of
open areas, more active individuals during hunting
hours, or boldness, should have a strong effect on the
probability that an individual will present itself as a pos-
sible target.
Here, we report studies where harvest-induced selection
of behavioural traits was clearly investigated. We searched
the scientific literature database Scopus
Ò
for peer-
reviewed papers using different combinations of the fol-
lowing seven keywords: harvesting, hunting, fisheries,
behaviour, vulnerability, exploitation and selective pres-
sure. The literature contains numerous studies on the
immediate effects of harvesting on behaviour (i.e. plastic
response or ‘learning’) (e.g. Raat 1985; Ordiz et al. 2012)
or studies showing behavioural differences between high
and low vulnerability fish strains (e.g. Nannini et al. 2011;
Sutter et al. 2012), or studies showing behavioural differ-
ences between fish caught with different methods or lures
(e.g. Wilson et al. 2015), which suggests that harvesting
might induce a selective pressure on behaviours. Here,
however, we only retained studies that directly examined
whether harvesting acted as a selective pressure on beha-
vioural traits. The limited amount of literature examining
harvest-induced selection on behaviour likely reflects the
difficulties in collecting quantitative information on beha-
vioural traits expressed by harvested and non-harvested
individuals necessary to investigate behavioural harvest-
induced selection. This is particularly true for fish,
because it is rarely possible to make observations on fish
that are not captured (H€
ark€
onen et al. 2016, but see
Olsen et al. 2012), and longitudinal behavioural time-ser-
ies data from wild populations hardly exist (Jørgensen &
Holt 2013). We categorized the 13 retained studies in two
groups: experimental studies in the laboratory or natural
conditions, and observational studies in the wild.
Experimental studies
We found seven experimental studies showing that harvest
can act as a selective pressure on behavioural traits
(Table 1; but see Vainikka, Tammela & Hyv€
arinen 2016).
From the seven studies showing harvest-induced selection
of behavioural traits, six were conducted in fishes and one
in a crustacean. Individuals showed different vulnerability
to angling in largemouth bass (Micropterus salmoides)
(Philipp et al. 2009) and common carp (Cyprinus carpio)
(Klefoth, Pieterek & Arlinghaus 2013), and traps removed
bolder guppies (Poecilia reticulata) and common yabby
(Cherax destructor) (Biro & Sampson 2015; Diaz Pauli
et al. 2015). Trawling removed shyer guppies (Diaz Pauli
et al. 2015) and minnows (Phoxinus phoxinus) with lower
swim speed (Killen, Nati & Suski 2015). These studies
suggest that harvesting can act as a selective pressure on a
behavioural trait and that passive gear should select
against boldness and more explorative individuals, while
active gear should select against shyness, and angling
selects against more aggressive, bold and vulnerable indi-
viduals (Heino & Godø 2002; Arlinghaus et al. 2016).
Harvest-induced selection patterns obtained in laboratory
experiments appear to be consistent with those observed
in experiments conducted in natural settings (Biro & Post
2008), suggesting that harvesting can act as a selective
pressure in the wild.
Observational studies
We found six studies showing harvest-induced selection
on different behavioural traits in the wild, ranging from
the timing of migration to boldness and defensiveness
(Table 1). These studies involved fishes, snakes, birds and
mammals in Japan, Norway, United Kingdom, Canada
and the USA. Similar to experimental studies, observa-
tional studies showed that harvest-induced selection was
caused by different harvest methods (shotgun, rifle hunt-
ing, passive gear, angling), and that behavioural traits
under selection may vary in relation to the harvest
method used (Table 1). In sockeye salmon (Oncorhynchus
nerka) harvesting selected against individuals that
migrated later in the season in a population where
exploitation rates vary systematically over the course of
the fishing season (Quinn et al. 2007). In this population,
migration timing became earlier over the years (Quinn
et al. 2007). Such temporal behavioural changes could be
caused by environmental factors, but could also be, at
least partly, a response to harvest-induced selection if
migration timing is heritable (Quinn et al. 2007).
©2017 The Authors. Journal of Applied Ecology ©2017 British Ecological Society, Journal of Applied Ecology,54, 1941–1945
1942 M. Leclerc, A. Zedrosser & F. Pelletier
Consequences of behavioural harvest-induced
selection
Behavioural traits under harvest-induced selection can
only evolve if they are heritable (Postma 2014; Dochter-
mann, Schwab & Sih 2015). In addition to the changes in
migration timing of sockeye salmon discussed above
(Quinn et al. 2007), two studies suggested that harvest
might have been important in the evolution of a genetic
locus related to habitat use of Atlantic cod (Gadus mor-
hua) in Iceland (
Arnason, Hernandez & Kristinsson 2009;
Jakobsdottir et al. 2011). However, we found no observa-
tional studies that could unequivocally show evolution in
behaviour caused by harvesting. Absence of evidence for
harvest-induced evolution of behavioural traits in the
wild, however, does not imply that such evolution is unli-
kely or uncommon. Instead, it may reflect the difficulties
to obtain the necessary longitudinal data on behaviours in
harvested populations (Clutton-Brock & Sheldon 2010;
Jørgensen & Holt 2013). Even when adequate data are
available, it remains challenging to show that harvest is
the driver of evolutionary change and to disentangle phe-
notypic plasticity from genetic change (Meril€
a & Hendry
2014). Although they have not been documented in the
wild, evolutionary changes in behavioural traits due to
harvest have been shown in experimental studies (Philipp
et al. 2009). Laboratory experiments are useful to evaluate
the potential for harvest-induced selection and
evolutionary response in behavioural traits, but extrapola-
tion of results to natural systems is difficult, as some rela-
tionships observed in the laboratory might not persist in
the wild (Wilson et al. 2011).
Conclusions
Humans have harvested wild animals for millennia and
human evolution is strongly linked with harvesting. How-
ever, technological developments have increased our effi-
ciency to harvest, with many consequences (Milner,
Nilsen & Andreassen 2007; Allendorf et al. 2008; Fenberg
& Roy 2008). Morphological, life-history and behavioural
traits form the phenotype of an individual and thus affect
its vulnerability to harvest (Uusi-Heikkil€
aet al. 2008).
There is increasing evidence that behavioural traits are
correlated with physiological and life-history traits (Biro
& Stamps 2008; R
eale et al. 2010). Therefore, even if har-
vesting specifically targets a behavioural trait, changes in
life-history, morphological, and/or physiological traits can
be observed. For example, changes in behaviours were
observed due to size-selective harvesting in zebra fish
(Uusi-Heikkil€
aet al. 2015), and size-selective harvesting
of Atlantic silverside (Menidia menidia) resulted in lower
larval growth rate, food consumption rate and conversion
efficiency, and vertebrae number (Walsh et al. 2006;
Duffy et al. 2013). If individuals with certain life-history,
morphological and behavioural phenotypes are heavily
Table 1. Examples of experimental and observational studies showing that harvest can act as a selective pressure on behaviour
Species Harvest method Trait
Direction of the selective effect
ReferenceHarvest selects against individual that are:
Experimental studies in the laboratory or in natural conditions
Poecilia reticulata Trap Bold–Shy Bolder Diaz Pauli et al. (2015)
Trawl Bold–Shy Shyer Diaz Pauli et al. (2015)
Phoxinus phoxinus Trawl Swim speed Slower Killen, Nati & Suski
(2015)
Salmo trutta Fly-fishing Exploration More explorative H€
ark€
onen et al. (2014)
Cyprinus carpio Angling Vulnerability More vulnerable Klefoth, Pieterek &
Arlinghaus (2013)
Micropterus salmoides Angling Vulnerability More vulnerable Philipp et al. (2009)
Oncorhynchus mykiss Gillnet Bold/Shy–Fast/Slow Faster-bolder Biro & Post (2008)
Cherax destructor Trap Bold–Shy Bolder Biro & Sampson (2015)
Observational studies
Oncorhynchus nerka Angling Migration timing Migrated later in season Quinn et al. (2007)
Gadus morhua Passive gear Habitat use Use more shallow water Olsen et al. (2012)
Passive gear Vertical migration Have a strong diel vertical migration Olsen et al. (2012)
Passive gear Horizontal movement Have a predictable movement pattern Olsen et al. (2012)
Gloydius blomhoffii Not mentioned Flight distance Have lower flight distance Sasaki, Fox & Duvall
(2009)
Not mentioned Defensiveness More defensive Sasaki, Fox & Duvall
(2009)
Phasianus colchicus Shotgun hunting Bold–Shy Bolder Madden & Whiteside
(2014)
Cervus elaphus Rifle hunting Habitat use Use habitat with less concealing cover Lone et al. (2015)
Rifle hunting Habitat use Use open areas Ciuti et al. (2012)
Rifle hunting Habitat use Closer to roads and use flatter terrain Ciuti et al. (2012)
Rifle hunting Movement rate Have higher movement rate Ciuti et al. (2012)
©2017 The Authors. Journal of Applied Ecology ©2017 British Ecological Society, Journal of Applied Ecology,54, 1941–1945
Behavioural harvest-induced selection 1943
harvested, selection may quickly lead to the evolution of a
population with a lower harvest yield (Conover & Munch
2002), because this population will now mostly be com-
posed of individuals with lower growth rate (Conover &
Munch 2002; Biro & Sampson 2015) that are also more
difficult to harvest (Philipp et al. 2009). In many cases,
selective pressures imposed by harvesting oppose natural
selection (Conover 2007; Olsen & Moland 2011). While
some traits can genetically recover after harvest-induced
selection ceases (Conover, Munch & Arnott 2009), some
traits may not (Salinas et al. 2012; Pigeon et al. 2016),
which can impair population recovery after harvest has
ceased (Laugen et al. 2014).
Recommendations
Even though behaviours are often easier to observe and
quantify in terrestrial ecosystems, most of the literature
and predictions on behavioural harvest-induced selection
come from fisheries. Despite differences in the harvest
methods used in fisheries and hunting, behavioural data
from terrestrial harvested populations can be complemen-
tary to fisheries data and could offer an opportunity to
test predictions developed for fisheries in terrestrial
ecosystems. For example, predictions made for passive
gear in fisheries could be applied to ‘still hunting’ or ‘bait
hunting’, but might not be appropriate for ‘stalking’.
Therefore, we suggest a synergistic approach and recom-
mend to increase discussions and collaborations between
researchers studying harvest-induced selection in fisheries
and terrestrial ecosystems.
Integrating genetic and evolutionary effects of harvest-
ing into management and conservation is central for
achieving sustainable harvesting (Conover & Munch 2002;
Allendorf et al. 2008). Acknowledging that harvest is
selective by nature is the first step towards that goal. Even
if harvest is random regarding phenotypes, it increases
mortality and therefore selects for faster growing and ear-
lier reproducing individuals (rlife-history strategy) rather
than slow growing and late reproducing individuals (K
life-history strategy) (Pianka 1970). Ideally, in harvested
populations, monitoring programs should be introduced
to detect and monitor potential harvest-induced selection
and its consequences. Such programs would require longi-
tudinal data on multiple phenotypic traits, including
behavioural traits, of harvested and non-harvested indi-
viduals in the population. This would allow evaluating the
direction and strength of harvest-induced selection in
comparison to natural selection. When required, different
mitigation measures could be implemented in manage-
ment plans to reduce the impacts of harvest-induced
selection. For example, reducing harvest quotas should
reduce the strength of selection or managers could estab-
lish harvest regimes that mimic natural selection (Milner,
Nilsen & Andreassen 2007).
Such monitoring programs are challenging tasks requir-
ing a considerable amount of time and money. In the
meantime, we suggest using a precautionary approach
when harvesting natural populations. Harvest quotas
should not be based on maximum yield but rather aim at
preserving natural variation shaped by natural selection
(Fenberg & Roy 2008). We suggest, based on our results,
to vary harvest regulations (e.g. based on sex, age or
phenotypes harvested and harvest methods used) spatio-
temporally to reduce the strength of selection on a
particular phenotype.
Authors’ contributions
All authors conceived the idea; M.L. conducted the literature search and
the first draft of the manuscript. All authors contributed critically to the
drafts and gave final approval for publication.
Acknowledgements
We thank M. Festa-Bianchet and two anonymous reviewers for com-
ments on an earlier version of this manuscript. M.L. was supported
financially by NSERC and FRQNT. F.P. was funded by NSERC
discovery grant and by the Canada Research Chair in Evolutionary
Demography and Conservation. A.Z. acknowledges funding from the
Polish-Norwegian Research Program operated by the National Center
for Research and Development under the Norwegian Financial Mecha-
nism 2009-2014 in the frame of project contract no. POL-NOR/198352/
85/2013. This is paper no. 229 of the Scandinavian Brown Bear Research
Project.
Data accessibility
Data have not been archived because this article does not contain data.
References
Allendorf, F.W., England, P.R., Luikart, G., Ritchie, P.A. & Ryman, N.
(2008) Genetic effects of harvest on wild animal populations. Trends in
Ecology & Evolution,23, 327–337.
Al
os, J., Palmer, M. & Arlinghaus, R. (2012) Consistent selection towards
low activity phenotypes when catchability depends on encounters among
human predators and fish. PLoS ONE,7, e48030.
Arlinghaus, R., Al
os, J., Klefoth, T., Laskowski, K., Monk, C.T.,
Nakayama, S. & der Schr€
o, A. (2016) Consumptive tourism causes
timidity, rather than boldness, syndromes: a response to Geffroy et al.
Trends in Ecology & Evolution,31,92–94.
Arnason, E., Hernandez, U.B. & Kristinsson, K. (2009) Intense
habitat-specific fisheries-induced selection at the molecular Pan I locus pre-
dicts imminent collapse of a major cod fishery. PLoS ONE,4, e5529.
Biro, P.A. (2013) Are most samples of animals systematically biased? Con-
sistent individual trait differences bias samples despite random sam-
pling. Oecologia,171, 339–345.
Biro, P.A. & Dingemanse, N.J. (2009) Sampling bias resulting from animal
personality. Trends in Ecology & Evolution,24,66–67.
Biro, P.A. & Post, J.R. (2008) Rapid depletion of genotypes with fast
growth and bold personality traits from harvested fish populations. Pro-
ceedings of the National Academy of Sciences of the United States of
America,105, 2919–2922.
Biro, P.A. & Sampson, P. (2015) Fishing directly selects on growth rate
via behaviour: implications of growth-selection that is independent of
size. Proceedings of the Royal Society B,282, 20142283.
Biro, P.A. & Stamps, J.A. (2008) Are animal personality traits linked to life-
history productivity? Trends in Ecology & Evolution,23, 361–368.
Carter, A.J., Heinsohn, R., Goldizen, A.W. & Biro, P.A. (2012) Boldness,
trappability and sampling bias in wild lizards. Animal Behaviour,83,
1051–1058.
Ciuti, S., Muhly, T.B., Paton, D.G., McDevitt, A.D., Musiani, M. &
Boyce, M.S. (2012) Human selection of elk behavioural traits in a land-
scape of fear. Proceedings of the Royal Society B,279, 4407–4416.
©2017 The Authors. Journal of Applied Ecology ©2017 British Ecological Society, Journal of Applied Ecology,54, 1941–1945
1944 M. Leclerc, A. Zedrosser & F. Pelletier
Clutton-Brock, T. & Sheldon, B.C. (2010) Individuals and populations:
the role of long-term, individual-based studies of animals in ecology and
evolutionary biology. Trends in Ecology & Evolution,25, 562–573.
Coltman, D.W., O’Donoghue, P., Jorgenson, J.T., Hogg, J.T., Strobeck,
C. & Festa-Bianchet, M. (2003) Undesirable evolutionary consequences
of trophy hunting. Nature,426, 655–658.
Conover, D.O. (2007) Nets versus nature. Nature,450, 179–180.
Conover, D.O. & Munch, S.B. (2002) Sustaining fisheries yields over evo-
lutionary time scales. Science,297,94–96.
Conover, D.O., Munch, S.B. & Arnott, S.A. (2009) Reversal of evolution-
ary downsizing caused by selective harvest of large fish. Proceedings of
the Royal Society B,276, 2015–2020.
Darimont, C.T., Carlson, S.M., Kinnison, M.T., Paquet, P.C., Reimchen,
T.E. & Wilmers, C.C. (2009) Human predators outpace other agents of
trait change in the wild. Proceedings of the National Academy of
Sciences of the United States of America,106, 952–954.
Diaz Pauli, B., Wiech, M., Heino, M. & Utne-Palm, A.C. (2015) Opposite
selection on behavioural types by active and passive fishing gears in a
simulated guppy Poecilia reticulata fishery. Journal of Fish Biology,86,
1030–1045.
Dochtermann, N.A., Schwab, T. & Sih, A. (2015) The contribution of
additive genetic variation to personality variation: heritability of person-
ality. Proceedings of the Royal Society B,282, 20142201.
Duffy, T.A., Picha, M.E., Borski, R.J. & Conover, D.O. (2013) Circulating
levels of plasma IGF-I during recovery from size-selective harvesting in
Menidia menidia.Comparative Biochemistry and Physiology. Part A,
166, 222–227.
Fenberg, P.B. & Roy, K. (2008) Ecological and evolutionary consequences
of size-selective harvesting: how much do we know? Molecular Ecology,
17, 209–220.
H€
ark€
onen, L., Hyv€
arinen, P., Paappanen, J., Vainikka, A. & Tierney, K.
(2014) Explorative behavior increases vulnerability to angling in hatch-
ery-reared brown trout (Salmo trutta). Canadian Journal of Fisheries and
Aquatic Sciences,71, 1900–1909.
H€
ark€
onen, L., Hyv€
arinen, P., Niemel€
a, P.T. & Vainikka, A. (2016) Beha-
vioural variation in Eurasian perch populations with respect to relative
catchability. Acta Ethologica,19,21–31.
Heino, M., D
ıaz Pauli, B. & Dieckmann, U. (2015) Fisheries-induced evolu-
tion. Annual Review of Ecology, Evolution, and Systematics,46, 461–480.
Heino, M. & Godø, O.R. (2002) Fisheries induced selection pressures in the
context of sustainable fisheries. Bulletin of Marine Science,70, 639–656.
Hendry, A.P., Farrugia, T.J. & Kinnison, M.T. (2008) Human influences
on rates of phenotypic change in wild animal populations. Molecular
Ecology,17,20–29.
Jakobsdottir, K.B., Pardoe, H., Magnusson, A., Bj€
ornsson, H., Pampoulie,
C., Ruzzante, D.E. & Marteinsdottir, G. (2011) Historical changes in
genotypic frequencies at the Pantophysin locus in Atlantic cod (Gadus
morhua) in Icelandic waters: evidence of fisheries-induced selection? Evo-
lutionary Applications,4, 562–573.
Jørgensen, C. & Holt, R.E. (2013) Natural mortality: its ecology, how it
shapes fish life histories, and why it may be increased by fishing. Journal
of Sea Research,75,8–18.
Jørgensen, C., Enberg, K., Dunlop, E.S. et al. (2007) Managing evolving
fish stocks. Science,318, 1247–1248.
Killen, S.S., Nati, J.J.H. & Suski, C.D. (2015) Vulnerability of individual
fish to capture by trawling is influenced by capacity for anaerobic meta-
bolism. Proceedings of the Royal Society B,282, 20150603.
Klefoth, T., Pieterek, T. & Arlinghaus, R. (2013) Impacts of domestication
on angling vulnerability of common carp, Cyprinus carpio: the role of
learning, foraging behaviour and food preferences. Fisheries Manage-
ment and Ecology,20, 174–186.
Laugen, A.T., Engelhard, G.H., Whitlock, R. et al. (2014) Evolutionary
impact assessment: accounting for evolutionary consequences of fishing
in an ecosystem approach to fisheries management. Fish and Fisheries,
15,65–96.
Lone, K., Loe, L.E., Meisingset, E.L., Stamnes, I. & Mysterud, A. (2015)
An adaptive behavioural response to hunting: surviving male red deer
shift habitat at the onset of the hunting season. Animal Behaviour,102,
127–138.
Madden, J.R. & Whiteside, M.A. (2014) Selection on behavioural traits
during ‘unselective’ harvesting means that shy pheasants better survive a
hunting season. Animal Behaviour,87, 129–135.
Meril€
a, J. & Hendry, A.P. (2014) Climate change, adaptation, and pheno-
typic plasticity: the problem and the evidence. Evolutionary Applications,
7,1–14.
Milner, J.M., Nilsen, E.B. & Andreassen, H.P. (2007) Demographic side
effects of selective hunting in ungulates and carnivores. Conservation
Biology,21,36–47.
Nannini, M.A., Wahl, D.H., Philipp, D.P. & Cooke, S.J. (2011) The influ-
ence of selection for vulnerability to angling on foraging ecology in
largemouth bass Micropterus salmoides.Journal of Fish Biology,79,
1017–1028.
Olsen, E.M. & Moland, E. (2011) Fitness landscape of Atlantic cod
shaped by harvest selection and natural selection. Evolutionary Ecology,
25, 695–710.
Olsen, E.M., Heupel, M.R., Simpfendorfer, C.A. & Moland, E. (2012)
Harvest selection on Atlantic cod behavioral traits: implications for spa-
tial management. Ecology and Evolution,2, 1549–1562.
Ordiz, A., Støen, O.-G., Sæbø, S., Kindberg, J., Delibes, M. & Swenson,
J.E. (2012) Do bears know they are being hunted? Biological Conserva-
tion,152,21–28.
Palumbi, S.R. (2001) Humans as the world’s greatest evolutionary force.
Science,293, 1786–1790.
Philipp, D.P., Cooke, S.J., Claussen, J.E., Koppelman, J.B., Suski, C.D. &
Burkett, D.P. (2009) Selection for vulnerability to angling in largemouth
bass. Transactions of the American Fisheries Society,138, 189–199.
Pianka, E.R. (1970) On r- and K-selection. The American Naturalist,104,
592–597.
Pigeon, G., Festa-Bianchet, M., Coltman, D.W. & Pelletier, F. (2016)
Intense selective hunting leads to artificial evolution in horn size. Evolu-
tionary Applications,9, 521–530.
Postma, E. (2014) Four decades of estimating heritabilities in wild verte-
brate populations: improved methods, more data, better estimates?
Quantitative Genetics in the Wild (eds A. Charmantier, D. Garant &
L.E.B. Kruuk), pp. 16–33. Oxford University Press, Oxford, UK.
Price, E.O. (1984) Behavioral aspects of animal domestication. The Quar-
terly Review of Biology,59,1–32.
Quinn, T.P., Hodgson, S., Flynn, L., Hilborn, R. & Rogers, D.E. (2007)
Directional selection by fisheries and the timing of sockeye salmon
(Oncorhynchus nerka) migrations. Ecological Applications,17, 731–739.
Raat, A.J.P. (1985) Analysis of angling vulnerability of common carp,
Cyprinus carp L., in catch-and-release angling in ponds. Aquaculture
Research,16, 171–187.
R
eale, D., Garant, D., Humphries, M.M., Bergeron, P., Careau, V. &
Montiglio, P.-O. (2010) Personality and the emergence of the pace-of-
life syndrome concept at the population level. Philosophical Transactions
of the Royal Society B,365, 4051–4063.
Salinas, S., Perez, K.O., Duffy, T.A., Sabatino, S.J., Hice, L.A., Munch,
S.B. & Conover, D.O. (2012) The response of correlated traits following
cessation of fishery-induced selection. Evolutionary Applications,5,657–663.
Sasaki, K., Fox, S.F. & Duvall, D. (2009) Rapid evolution in the wild:
changes in body size, life-history traits, and behavior in hunted popula-
tions of the Japanese mamushi snake. Conservation Biology,23,93–102.
Sutter, D.A.H., Suski, C.D., Philipp, D.P., Klefoth, T., Wahl, D.H., Ker-
sten, P., Cooke, S.J. & Arlinghaus, R. (2012) Recreational fishing selec-
tively captures individuals with the highest fitness potential. Proceedings
of the National Academy of Sciences of the United States of America,
109, 20960–20965.
Uusi-Heikkil€
a, S., Wolter, C., Klefoth, T. & Arlinghaus, R. (2008) A
behavioral perspective on fishing-induced evolution. Trends in Ecology
& Evolution,23, 419–421.
Uusi-Heikkil€
a, S., Whiteley, A.R., Kuparinen, A. et al. (2015) The evolu-
tionary legacy of size-selective harvesting extends from genes to popula-
tions. Evolutionary Applications,8, 597–620.
Vainikka, A., Tammela, I. & Hyv€
arinen, P. (2016) Does boldness explain
vulnerability to angling in Eurasian perch Perca fluviatilis?Current
Zoology,62, 109–115.
Walsh, M.R., Munch, S.B., Chiba, S. & Conover, D.O. (2006) Maladap-
tive changes in multiple traits caused by fishing: impediments to popula-
tion recovery. Ecology Letters,9, 142–148.
Wilson, A.D.M., Binder, T.R., McGrath, K.P., Cooke, S.J. & Godin,
J.-G.J. (2011) Capture technique and fish personality: angling targets
timid bluegill sunfish, Lepomis macrochirus.Canadian Journal of
Fisheries and Aquatic Sciences,68, 749–757.
Wilson, A.D.M., Brownscombe, J.W., Sullivan, B., Jain-Schlaepfer, S. &
Cooke, S.J. (2015) Does angling technique selectively target fishes based
on their behavioural type? PLoS ONE,10, e0135848.
Received 25 October 2016; accepted 17 February 2017
Handling Editor: Marc-Andr
e Villard
©2017 The Authors. Journal of Applied Ecology ©2017 British Ecological Society, Journal of Applied Ecology,54, 1941–1945
Behavioural harvest-induced selection 1945