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Swaegers Etal 2017 Animal Behaviour 124 (2017) 153e159 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Selection on escape performance during ecological speciation driven by predation * J. Swaegers a, , 1, F. Strobbe a, b, 1, M. A. McPeek c,R.Stoksa a Department of Biology, Laboratory of Aquatic Ecology, Evolution and Conservation, University of Leuven, Leuven, Belgium b Directorate Natural Environment, Biodiversity and Ecosystems Data and Information Centre, Royal Belgian Institute of Natural Sciences, Brussels, Belgium c Department of Biological Sciences, Dartmouth College, Hanover, NH, U.S.A. article info Despite the many study systems in which predation has played a major role in phenotypic diversification Article history: and speciation, the underlying selective regimes imposed by different predator assemblages have rarely Received 4 September 2016 been quantified. We did so for the damselfly genus Enallagma which strongly diverged in antipredator Initial acceptance 12 October 2016 traits when the ancestral species occupying lakes containing fish (hereafter fish lakes) repeatedly Final acceptance 24 November 2016 invaded fishless lakes with dragonfly larvae as top predators (hereafter dragonfly lakes). In two selection Available online 18 January 2017 experiments in field enclosures we quantified the selection on two key escape traits of two fish-lake MS. number: 16-00784R Enallagma species associated with survival selection by fish in the ancestral fish lakes and by drag- onfly predators in the invaded fishless, dragonfly lakes. In accordance with the different hunting modes, Keywords: fish imposed selection for a decreased swimming propensity while dragonfly larvae imposed selection antipredator behaviour for increased swimming speed in one of the two species. In two complementary quantitative genetic ecological speciation fi fl rearing experiments, we found relatively low but signi cant broad-sense heritabilities for both escape Enallagma damsel ies fi habitat shifts traits. Integrating these estimates for the selection coef cients and the heritabilities suggests that the phenotypic diversification evolutionary increase in swimming speed associated with the habitat shift may have occurred rapidly. Our study suggests that the phenotypic evolution of ecologically important traits related to habitat shifts may occur at an ecological timescale. © 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Predators are a major selective force (reviewed in Endler, 1986; 2009; Stoks & McPeek, 2006; Vamosi, 2005; Wellborn, Skelly, & Tollrian & Harvell, 1999) and their role in phenotypic diversification Werner, 1996). has attracted considerable attention both at the intraspecific level The underlying selective regimes imposed by different predator (e.g. Carlson, Rich, & Quinn, 2009; Marchinko, 2009; Urban, 2010; assemblages have been quantified in relatively few study systems Ghalambor et al., 2015; Harris, Eroukhmanoff, Green, Svensson, & in which different predator assemblages have played a major role in Pettersson, 2011; Stoks, Govaert, Pauwels, Jansen, & De Meester, phenotypic diversification and speciation (Carlson et al., 2009; 2016) and at the interspecific level, where diversification is ex- Gordon, Feit, Gruber, & Letnic, 2015; Marchinko, 2009; Nosil & pected to have occurred on a much longer timeframe (e.g. Arbuckle Crespi, 2006; Svanback€ & Eklov,€ 2011). Such studies are impor- & Speed, 2015; Langerhans, Gifford, & Joseph, 2007; McPeek, tant to rule out alternative hypotheses underlying the phenotypic Schrot, & Brown, 1996; Mikolajewski et al., 2010; Nosil & Crespi, diversification such as differential habitat use and differences in 2006). Predator assemblages that differ in hunting mode can other biotic interactions (Goodman, Miles, & Schwarzkopf, 2008; impose different selection pressures on antipredator behaviour. Irschick, Bailey, Schweitzer, Husak, & Meyers, 2007; Urban & This may lead to phenotypic diversification of prey populations Richardson, 2015). Moreover, links between the phenotype and between habitats with different predator assemblages, eventually its adaptive value against certain predators, such as the survival accumulating into ecological speciation (Nosil, 2012; Schluter, value of a higher escape speed, cannot be taken for granted (Holmes & McCormick, 2009; Walker, Ghalambor, Griset, Mckenney, & Reznick, 2005). For example, Johnson, Burt, and Dewitt (2008) showed that a higher burst swimming speed in tadpoles of Rana sphenocephala did not influence survival in the * Correspondence: J. Swaegers, Charles Deberiotstraat 32, 3000 Leuven, Belgium. presence of dragonfly predators. Of the studies explicitly quanti- E-mail address: [email protected] (J. Swaegers). 1 First and second author contributed equally. fying selective regimes imposed by contrasting predator http://dx.doi.org/10.1016/j.anbehav.2016.12.012 0003-3472/© 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 154 J. Swaegers et al. / Animal Behaviour 124 (2017) 153e159 assemblages nearly all have focused on intraspecific differentiation two fish-lake species, Enallagma geminatum and Enallagma hageni (for the only examples of incipient speciation see Marchinko, 2009; (Brown et al., 2000; McPeek & Brown, 2000; Turgeon et al., 2005), Nosil & Crespi, 2006). Moreover, no studies have reconstructed the that represent the two clades (and the associated ancestral phe- initial stages of predator-driven diversification in a system in which notypes) that independently gave rise to the dragonfly-lake Enal- the direction of the evolutionary change in predator assemblage is lagma. We quantified selection by fish on these traits in their known. Ideally, studies quantifying the predator-mediated selec- natural fish-lake habitat and by dragonfly predators in the derived tion strength should also estimate the heritability of the traits dragonfly lakes. These coupled experiments thus simulate the under selection to evaluate the potential of the selection pressures initial change in phenotypic selection regime presumably experi- to drive the evolutionary trajectories when predator regimes enced by the ancestral fish-lake species when they invaded drag- changed (Arnold, Pfrender, & Jones, 2001). onfly lakes within the last 20 000 years (McPeek & Brown, 2000; An elegant study system to explicitly quantify predator-driven Turgeon et al., 2005). We expected fish predation to select for a survival selection on escape behaviour is provided by the North lower propensity to swim but not to impose selection on escape American species of the damselfly genus Enallagma. Most Enal- swimming speed, while we expected dragonfly predation to select lagma species occur in lakes containing fish (hereafter called fish for a higher propensity to swim and a higher escape swimming lakes), the ancestral habitat, and three independent invasions have speed. In a previous paper (Strobbe, McPeek, De Block, & Stoks, occurred to fishless lakes where large predatory dragonfly larvae 2011) we quantified selection on foraging activity (number of are the top predators (hereafter called dragonfly lakes) (Brown, food items eaten) based on the enclosure experiment in the fish- McPeek, & May, 2000; McPeek & Brown, 2000; Turgeon, Stoks, lake habitat; here we focus on selection on escape traits. In Thum, Brown, & McPeek, 2005). These invasions into dragonfly another study (Strobbe et al., 2009) we documented selection on lakes were associated with the evolution of higher values for two escape speed by a derived dragonfly-lake Enallagma species in a related escape traits: swimming propensity and escape swimming dragonfly lake, allowing a qualitative comparison with ongoing speed (McPeek, 1999; McPeek et al., 1996). Escape swimming in selection pressures after the habitat shift in the evolved dragonfly- damselfly larvae occurs by moving the abdomen from side to side lake species. Moreover, by estimating the heritabilities of both (Brackenbury, 2002). This includes a behavioural component: escape behaviours for the two species of the lineages sharing most larvae swim faster if they beat their abdomens faster (McPeek, recent ancestry with current dragonfly-lake species, we were able Schrot, & Brown, 1996). The evolution of both traits is linked to to assess the scope for evolution by natural selection on these traits. the different efficacy of escape swimming as an antipredator strategy against fish and dragonfly predators. Damselfly larvae have METHODS little chance of outswimming a fish (McPeek, 2000; Stoks & De Block, 2000); moreover, swimming attracts the attention of the Selection Experiments fish predators (Baker, Elkin, & Brennan, 1999). Instead, damselfly larvae have a good chance of avoiding capture when attacked by We quantified selection by fish and by dragonfly larvae on larval dragonfly predators (McPeek, 1990b; McPeek et al., 1996; Stoks & escape traits of the two fish-lake Enallagma species in field enclo- De Block, 2000). In line with this, ongoing survival selection for a sures. We did so by contrasting trait values at the end of the higher swimming propensity and a higher swimming speed has enclosure experiment between two predator treatments: in one, been documented in a derived dragonfly-lake Enallagma species predators had been able to consume damselfly larvae (‘free-ranging using an enclosure experiment (Strobbe, McPeek, De Block, De predator’) and in the other predators had been caged (‘caged Meester,
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