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The Multipredator Hypothesis

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CURRENT ISSUES – PERSPECTIVES AND REVIEWSThe Multipredator Hypothesis and the Evolutionary Persistenceof Antipredator BehaviorDaniel T. BlumsteinDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USAIntroductionStudies of geographic variation in behavior illustrateboth remarkable plasticity and remarkable persist-ence when a population becomes isolated from pred-ators (Diamond 1990; Berger 1998, 1999; Coss 1999;Magurran 1999; Berger et al. 2001). For instance,reduction in predation pressure allows animals toforage more and allocate less time to antipredatorvigilance (e.g. Catterall et al. 1992; Hunter & Skin-ner 1998; Blumstein et al. 2001), be choosier whenlooking for mates (e.g. Forsgren 1992; Berglund1993; Briggs et al. 1996), spend less time with others(Magurran & Seghers 1994), modify group sizes(Heard 1992), aggressively defend breeding terri-tories (Huntingford 1982), or forage in other places(e.g. Werner et al. 1983; Bland & Temple 1990;Suhonen 1993). Very costly traits, such as those thatreduce reproductive success (e.g. those subject tosexual selection), seem to respond quickly to relaxedselection brought about by the removal of predators(Endler 1980; Endler & Houde 1995). However,some antipredator behavior persists for many thou-sands of years after isolation (Byers 1997; Coss 1999;Blumstein et al. 2000; Blumstein & Daniel 2002),and there is no adequate model to account for thisvariation.Existing Hypotheses to Explain PersistenceThere are several inter-related hypotheses to explainthe persistence of antipredator traits under relaxedCorrespondenceDaniel T. Blumstein, Department of Ecologyand Evolutionary Biology, University ofCalifornia, 621 Young Drive South, LosAngeles, CA 90095-1606, USA.E-mail: [email protected]: September 30, 2005Initial acceptance: November 1, 2005Final acceptance: November 11, 2005(S. Forbes)doi: 10.1111/j.1439-0310.2006.01209.xInvited ReviewAbstractIsolation from predators affects prey behavior, morphology, and life his-tory, but there is tremendous variation in the time course of theseresponses. Previous hypotheses to explain this variation have limitedpredictive ability. I develop a ‘multipredator’ hypothesis to explain theevolutionary persistence of antipredator behavior after the loss of some,but not all, of a species’ predators. The hypothesis assumes pleiotropy,whereby elements of antipredator behavior may function in non-predat-ory situations, and linkage, such that genes influencing the expressionof antipredator behavior do not assort independently. The hypothesis isrestricted to species with multiple predators (most species) and aims topredict the conditions under which antipredator behavior will persistfollowing the loss of one or more of a species’ predators. I acknowledgethat the relative costs of non-functional antipredator behavior will influ-ence the likelihood of linkage and therefore persistence. The hypothesismakes two main predictions. First, genes responsible for antipredatorbehavior will not be scattered throughout the genome but rather maybe found close together on the same chromosome(s). Secondly, thepresence of any predators may be sufficient to maintain antipredatorbehavior for missing predators. Advances in behavioral genetics willallow tests of the first prediction, while studies of geographic variationin antipredator behavior provide some support for the second.EthologyEthology 112 (2006) 209–217 ª 2006 The AuthorJournal compilation ª 2006 Blackwell Verlag, Berlin209selection; however, they act at different levels(Tinbergen 1963) of biological organization and arenot necessarily mutually exclusive. All assume somedegree of heritable variation in antipredator behavior(e.g. Seghers 1974; Magurran 1990; Riechert &Hedrick 1990). Much antipredator behavior requiressome experience for proper performance (Griffinet al. 2000), and I acknowledge that mechanisms ofantipredator behavior can influence the phenotypicresponse to isolation from predators (Blumstein2002). Specifically, relatively hard-wired traits willhave evolutionary responses, while relatively experi-ence-dependent traits will have an immediateresponse to the loss of experience with predators.However, hypotheses that explain the evolutionaryresponse to relaxed selection treat experience as anobscuring variable (i.e. it increases phenotypic vari-ation).The ‘ghost of predators past’ hypothesis (Peckarsky& Penton 1988; Byers 1997) simply says that aspecies subject to past selection for antipredatorbehavior will retain antipredator behavior if it is nottoo costly to do so (e.g. Neill 1990). This hypothesis,while descriptive, does not enable us to explain vari-ation in how different species and populationswithin a species respond to relaxed selection withoutspecific knowledge of selection differentials (i.e. dif-ferential costs) and heritability estimates (Falconer1981). However, it does highlight the importance ofcosts, which will be developed further below.Darwin (1859) recognized that vestigial structureswill become more variable after selection is relaxedbecause they are no longer checked by natural selec-tion. Haldane (1933) noted that mutations will accu-mulate on non-selected traits causing an increase invariation. Decay (Coss 1999) of non-selected traits isnot inevitable, however, and is less likely for traitswith pleiotropic effects (Byers 1997).A second hypothesis suggests that antipredator be-havioral traits have pleiotropic effects on other traits,which will be functional regardless of the presenceor absence of predators (Byers 1997; Coss 1999). Atthe genomic level proteins that are centrally locatedin networks (Hahn & Kern 2004) are buffered fromchange, and this centrality may provide a mechan-ism by which pleiotropy may constrain the rate ofevolutionary change. Pleiotropy occurs at higherlevels of organization as well. For instance, localguidance molecules are used for both axonal anddendritic organization (Kim & Chiba 2004), and thesame genes are responsible for the organization ofthe visual cortex and the thalamus (Sestan et al.2001). For all of these reasons, pleiotropy seems tobe a reasonable mechanism explaining persistence.Unfortunately, without detailed knowledge ofbehavioral genetics (e.g. Brodie 1989), the ‘pleio-tropic’ hypothesis does not enable us to predict howa given species or population will respond to relaxedor modified selection.A third, but related, hypothesis


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