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Genetic Variation in Parental Effects Contributes to the Evolutionary Potential of Prey Responses to Predation Risk

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Genetic Variation in Parental Effects Contributes to the Evolutionary Potential of Prey Responses to Predation Risk vol. 197, no. 2 the american naturalist february 2021 Genetic Variation in Parental Effects Contributes to the Evolutionary Potential of Prey Responses to Predation Risk Natasha Tigreros,1,* Anurag A. Agrawal,1,2 and Jennifer S. Thaler1,2 1. Department of Entomology, Cornell University, Ithaca, New York 14853; 2. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14850 Submitted March 22, 2020; Accepted September 16, 2020; Electronically published January 19, 2021 Online enhancements: supplemental PDF. abstract: Despite the ubiquity of parental effects and their poten- and Kruuk 2007; Donelson et al. 2018). Yet understanding tial effect on evolutionary dynamics, their contribution to the evo- theevolutionaryconsequencesofparentaleffectsiscompli- lution of predator-prey interactions remains poorly understood. cated by the fact that parents are themselves shaped by the Using quantitative genetics, here we demonstrate that parental ef- environmental conditions that they experience, as well as fects substantially contribute to the evolutionary potential of larval by genetic differences among parents (McAdam et al. antipredator responses in a leaf beetle (Leptinotarsa decemlineata). 2014; Kong et al. 2018). While predictions for the evolution Previous research showed that larger L. decemlineata larvae elicit of parental effects depend on genetic (and nongenetic) com- stronger antipredator responses, and mothers perceiving predators improved offspring responses by increasing intraclutch cannibal- ponents and selective forces acting on both the parental and ism—an extreme form of offspring provisioning. We now report offspring phenotype, little empirical work to date has substantial additive genetic variation underlying maternal ability partitioned their relative contribution to variation in off- to induce intraclutch cannibalism, indicating the potential of this spring traits (Wolf and Wade 2001, 2016; Räsänen and adaptive maternal effect to evolve by natural selection. We also Kruuk2007),especiallythoseinvolvingresponsestonatural show that paternal size, a heritable trait, affected larval responses ecological stressors. to predation risk but that larval responses themselves had little ad- The triggering of environmental parental effects may ditive genetic variation. Together, these results demonstrate how fl larval responses to predation risk can evolve via two types of paren- re ect a passive consequence of stress or the resource en- tal effects, both of which provide indirect sources of genetic varia- vironment that parents experience, or it may involve adap- tion for offspring traits. tive responses counter to those conditions (Ghalambor et al. 2013). Research over the last two decades indicates Keywords: transgenerational plasticity, maternal effects, inducible that parental effects can function as a form of adaptive defenses, cannibalism, predation risk. transgenerational plasticity—commonly referred to as “an- ticipatory parental effects” (Wade 1998; Agrawal et al. 1999; Introduction Galloway and Etterson 2007; Marshall and Uller 2007; Love and Williams 2008; Sheriff and Love 2013). Here, fl Parents in uence the phenotype of their offspring through parents improve their offspring’s fitness by matching the the direct inheritance of genes (additive genetic effects) as offspring’s phenotype to environmental challenges that well as through parental effects (Kirkpatrick and Lande they will likely experience (e.g., Marshall and Uller 2007; 1989; Räsänen and Kruuk 2007), the latter ranging from Sheriff and Love 2013). Despite growing evidence of the parental care to the transfer of hormones and antibodies to adaptive nature of parental effects on offspring (Agrawal young. Such parental effects constitute an important com- et al. 1999; Sheriff et al. 2010; Storm and Lima 2010; Jensen ponent of phenotypic variation that may facilitate rapid et al. 2014), evidence of genetic variation in anticipatory evolutionary responses to a number of ecological stressors parental effects (i.e., maternal genotype by environment in animals and plants (Mousseau and Fox 1998; Räsänen interaction) is scarce in both animals (but see Fox et al. 1999) and plants (Galloway 2005). As a consequence, sup- * Corresponding author; email: [email protected]. port for the evolutionary potential of anticipatory parental ORCIDs: Tigreros, https://orcid.org/0000-0002-4030-2391; Agrawal, https:// orcid.org/0000-0003-0095-1220; Thaler, https://orcid.org/0000-0002-3716-9622. effects to date is limited (reviewed in Wade 1998; Räsänen and Kruuk 2007; McAdam et al. 2014). Am. Nat. 2021. Vol. 197, pp. 000–000. q 2021 by The University of Chicago. 0003-0147/2021/19702-59858$15.00. All rights reserved. Variation in parental provisioning to offspring, by di- DOI: 10.1086/712341 rectly feeding young or through investment of nutritional 000 The American Naturalist resources in eggs and seeds, is perhaps one of the most risk using a modified half-sib design (Falconer and Mackay ubiquitous sources of parental effects in animals and plants 1996; Fox et al. 1999) that allowed us to estimate altogether (Roach and Wulff 1987; Bernardo 1996a; Fox and Czesak (1) the additive genetic (VA) and maternal (VM) effects on 2000). While females facing stressful conditions may re- larval responses to predation risk (fig. 1, question 1), (2) the duce offspring provisioning to save energy for other func- influences of maternal and paternal body size on larval re- tions (e.g., self-maintenance) or for future reproduction sponses to predation risk (fig. 2, question 2), and (3) the (Sheriff and Love 2013), females can also increase provi- variance components of maternal responses to predation sioning to improve offspring chances of surviving stressful risk (fig. 1, question 3). conditions. In oviparous species, mothers experiencing the risk of predation can improve provisioning and survival of General Breeding Design their young by increasing egg size/quality as well as by pro- moting intraclutch egg cannibalism (Giesing et al. 2011; Sires and dams for this half-sib breeding design were the Segers and Taborsky 2012; Tigreros et al. 2017, 2019). For first generation of 25 females collected from a field popu- example, in the leaf beetle, Leptinotarsa decemlineata, fe- lation in Ithaca, NY, which were allowed to lay eggs in the males perceiving the risk of predation increase egg canni- laboratory; their offspring, once mature, were considered balism within their clutches by producing unviable trophic the parental generation (fig. 1), from which sires and dams eggs (Tigreros et al. 2017). Such an extreme form of mater- were selected. All sires, dams, and offspring from the differ- nal provisioning improves cannibals’ nutritional condition ent sire by dam crosses were reared separately from birth— and allows them to reduce foraging activity under the risk which minimizes common environmental effects—and of predation (Tigreros et al. 2017). Leptinotarsa decemli- maintained in standardized conditions with 18-L∶6-D neata larvae, like many other prey species, are more vul- photoperiod and corresponding temperatures of 237∶217C. nerable to predation during foraging (reviewed in Lima Larvae and adults were reared on Solanum tuberosum L, and Dill 1990; Lima 1998; Verdolin 2006). Thus, promot- Yukon Gold variety, which we know to be a high-quality va- ing intraclutch egg cannibalism, even though this entails riety of host plant for Leptinotarsa decemlineata (N. Tigre- a reduction in the number of offspring produced, consti- ros, personal observations). The half-sib families were ini- tutes an anticipatory maternal effect that increases fitness tially established with 22 males (sires) each randomly mated of offspring, and likely the mother, in high-predation en- tothreeunrelatedfemales(dams).Siresthatfailedtoinsem- vironments (Tigreros et al. 2017). inate at least two females were excluded, and final analyses Here, we use classic quantitative genetics to examine included fewer sires and dams, which is specified in each sec- the relative importance of within- and between-generation tion below. genetic and environmental effects influencing traits associ- ated with antipredator responses in L. decemlineata larvae. Question 1: Are There Genetic and Maternal Effects Specifically, we first estimate the relative contributions of Influencing Larval Responses to Predation Risk? maternal (VM), additive genetic (VA), and environmental fi effects (VE) for larval responses to predation risk, includ- In a rst step, we followed a variance partitioning strategy ing decreased foraging activity (leaf consumption) and in- to quantify the amount of variance in offspring’straits— creased assimilation efficiency. Second, we test whether larval leaf consumption and assimilation efficiency—that larval responses to predation risk, which are known to de- is explained by maternal identity (VM), while accounting ’ fl pend on the larva s initial size, are in uenced by variation for the contributions of additive genetic inheritance (VA) in maternal or paternal body size, a key trait that affects and environmental variances (VE; McAdam et al. 2014). offspring phenotype in many systems (Fox 1994; Bernardo Final analysis included 19 sires mated to 47 dams (with 1996a; Fox and Czesak 2000; Bennett and Murray 2014). two to three dams per sire). We estimated larval plastic re- Finally, we estimate the relative contribution of additive sponses to predation risk by measuring changes in larval fi genetic and environmental variances
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