Induced defenses in response to an invading crab predator: An explanation of historical and geographic phenotypic change

Abstract

The expression of defensive morphologies in prey often is correlated with predator abundance or diversity over a range of temporal and spatial scales. These patterns are assumed to reflect natural selection via differential predation on genetically determined, fixed phenotypes. Phenotypic variation, however, also can reflect within-generation developmental responses to environmental cues (phenotypic plasticity). For example, water-borne effluents from predators can induce the production of defensive morphologies in many prey taxa. This phenomenon, however, has been examined only on narrow scales. Here, we demonstrate adaptive phenotypic plasticity in prey from geographically separated populations that were reared in the presence of an introduced predator. Marine snails exposed to predatory crab effluent in the field increased shell thickness rapidly compared with controls. Induced changes were comparable to (i) historical transitions in thickness previously attributed to selection by the invading predator and (ii) present-day clinal variation predicted from water temperature differences. Thus, predator-induced phenotypic plasticity may explain broad-scale geographic and temporal phenotypic variation. If inducible defenses are heritable, then selection on the reaction norm may influence coevolution between predator and prey. Trade-offs may explain why inducible rather than constitutive defenses have evolved in several gastropod species. P henotypic plasticity, the capacity of an organism to produce different phenotypes in response to environmental cues, can be an important adaptive strategy in variable or changing environments (1, 2). Inducible defenses are a ubiquitous form of plasticity that involve the production of chemicals, morphologies, or behaviors by prey species in response to predator cues (3). These changes reduce prey vulnerability to inducing predators or herbivores. Inducible defenses occur in diverse taxa and examples include: production of chemical defenses in plants (4, 5), formation of spines in rotifers (6) and marine bryozoans (7) and neck teeth and helmets in cladocerans (8), diel vertical migration in marine (9) and freshwater zooplankton (10), and changes in body shape in fish (11) and shell shape and thickness in mollusks and barnacles (12-15).Despite improved understanding of the cues inducing these defenses and their immediate adaptive value (3, 16), our understanding of how this phenomenon contributes to broader temporal and spatial patterns of phenotypic variation remains poor. To date, most studies have examined inducible defenses and their costs on very localized spatial scales (3-15). In doing so, there is limited consideration of environmental complexity and the interactive inf luences of others cues that are likely to occur across a broader scale. For example, many plant and animal species have wide altitudinal and latitudinal distributions where dramatic temperature gradients occur. Because temperature can profoundly inf luence developmental and metabolic rates (17, 18) and phen...

Phenotypic convergence along a gradient of predation risk

“…Furthermore, there is evidence, as noted above, that large-scale spatial variation in traits can be attributed to plasticity (e.g. [3]). However, no study has explicitly examined whether plasticity can be responsible for convergence in phenotypes among different populations.…”

“…They thus begin to illuminate how combinations of traits function together in a plastic phenotype (a complex; cf. [3,9]) and how such a complex phenotype might change when exposed to different selection pressures [8]. But they fail to elucidate how gradients of predation risk may influence, via plasticity, the entire phenotype.…”

“…Trussell & Smith [3] showed that large-scale spatial variation in morphology could be better attributed to large-scale gradients of predation risk and inducible defences, rather than selection per se. In contrast to this evidence for divergence, there is limited (if any) evidence that phenotypic plasticity can generate convergence in phenotype among genetically distinct populations exposed to a common selective pressure.…”

What can aquatic gastropods tell us about phenotypic plasticity? A review and meta-analysis

“…These plastic responses appear ubiquitous; they have been found in multiple species (for example, Appleton and Palmer, 1988;Palmer, 1990;Trussell, 1996;DeWitt, 1998;Hoverman et al, 2005;Hollander et al, 2006;Bourdeau, 2009;Brönmark et al, 2011), in species with different dispersal capabilities (for example, Behrens Yamada, 1989;Hollander et al, 2006), from different geographic locations (for example, Trussell, 2000a, b;Trussell and Smith, 2000) and in response to several predator species (for example, Hoverman and Relyea, 2007;Bourdeau, 2009). However, populations and species often differ in their degree of shell plasticity (for example, Appleton and Palmer, 1988;Palmer, 1990;Trussell, 1996;Edgell and Neufeld, 2008;Bourdeau, 2012).…”

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

“…This approach has been instrumental in documenting the taxonomic prevalence of inducible defenses (Torllian and Harvell 1999;DeWitt and Scheiner 2004) and has shed considerable light on the adaptive value of trait plasticity (Lively 1986a,b;Kopp and Tollrian 2003a;Kishida and Nishimura 2005;Benard 2006). These insights have been further enhanced by studies of the role of inducible defenses in driving the evolution of geographic variation in prey phenotypes (Lively et al 2000;Trussell 2000a,b;Trussell and Smith 2000;Relyea 2002a;Trussell and Nicklin 2002;Laurila et al 2006;Kishida et al 2007) and the genetic basis of morphological plasticity via quantitative genetic (Relyea 2005a) and molecular genetic (Mori et al 2005(Mori et al , 2009) approaches. For example, Rana pirica frog tadpoles of the populations in the predator-common mainland have higher expression ability of defensive morph when exposed to predation risk from the salamander larvae (Hynobius retardatus) than those of a predator-free island population ).…”