Evidence of weaker phenotypic plasticity by prey to novel cues from non-native predators Johan Hollander1 & Paul E. Bourdeau2 1Department of Biology, Aquatic Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden 2Department of Biological Sciences, Humboldt State University, 1 Harpst St., Arcata, California 95521 Keywords Abstract Coevolution, inducible defensive traits, meta-analysis, naive interactions. A central question in evolutionary biology is how coevolutionary history between predator and prey influences their interactions. Contemporary global Correspondence change and range expansion of exotic organisms impose a great challenge for Johan Hollander, Department of Biology prey species, which are increasingly exposed to invading non-native predators, Aquatic Ecology, Lund University, Ecology with which they share no evolutionary history. Here, we complete a compre- Building, SE-223 62 Lund, Sweden. hensive survey of empirical studies of coevolved and naive predatorÀprey inter- Tel: +46 46 222 34 73; Fax: +46 46 222 45 36; actions to assess whether a shared evolutionary history with predators E-mail: [email protected] influences the magnitude of predator-induced defenses mounted by prey. Using marine bivalves and gastropods as model prey, we found that coevolved prey Funding Information and predator-naive prey showed large discrepancies in magnitude of predator- JH was funded by a Marie Curie European induced phenotypic plasticity. Although naive prey, predominantly among Reintegration Grant (PERG08-GA-2010- bivalve species, did exhibit some level of plasticity – prey exposed to native 276915) and the Swedish Research Council predators showed significantly larger amounts of phenotypic plasticity. We dis- (2015-05001). cuss these results and the implications they may have for native communities Received: 21 January 2016; Revised: 25 May and ecosystems. 2016; Accepted: 31 May 2016 Ecology and Evolution 2016; 6(15): 5358– 5365 doi: 10.1002/ece3.2271 Introduction reciprocally affect each other’s evolution (Ehrlich and Raven 1964; Dawkins and Krebs 1979; Brodie and Brodie Phenotypic plasticity is a developmental strategy where an 1999). Thus, the chemical signature of a coevolved preda- individual’s genotype has the ability to interact with its tor is likely to represent a reliable cue indicating risk to a environment and produce different phenotypes. The prey organism. However, since rapid globalization of the resulting phenotypic flexibility may increase an organ- world has increased species mobility and led to a growing ism’s fitness in a heterogeneous environment and it is a number of alien introductions of both animals and plants, common attribute across many taxa (Schlichting 1986; including many predatory species, prey species are Appleton and Palmer 1988; Whitman and Ananthakrish- increasingly being exposed to cues from predators with nan 2008; Hollander and Butlin 2010). which they share no evolutionary history (so-called naive Phenotypic plasticity is not considered likely to evolve interactions). Native prey species that are naive to cues if accessible cues are not reliable predictors of environ- and unable to alter their phenotype in response to novel mental change to the organism (Moran 1992; Tufto predators, or native prey that are less flexible in their abil- 2000). Indeed, in order for adaptive phenotypic plasticity ity to alter their phenotype in response to novel predators to evolve, predictable environmental cues, such as sea- will accordingly experience reduced fitness and a poten- sonal or systematic environmental change, or chemical tially larger extinction risk when exposed to non-native signals indicating the presence of a coevolved predator, invading, or range-expanding predators. are essential. Coevolution is the result of a shared evolu- In accordance with theory, which predicts that adaptive tionary history between two or more species that phenotypic plasticity will fail to evolve without reliable 5358 ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. J. Hollander & P. E. Bourdeau Phenotypic Plasticity to Novel Cues cues (Moran 1992; Tufto 2000), there are a number of history) to predators. Studies that did not meet our crite- examples where naive prey fail to produce phenotypically ria were omitted from the data set. A number of studies plastic defensive traits (i.e., inducible defenses) when were rejected during this process because they were not exposed to novel predators (Edgell and Rochette 2007; related to the topic of bivalve or gastropod phenotypic Edgell and Neufeld 2008). However, in other cases, naive plasticity or they focused on the plasticity of predators prey have also been shown to respond plastically to novel rather than on the plasticity of bivalve or gastropod prey. predators (Freeman and Byers 2006; Rawson et al. 2007; The publication records in our data set covered from 1987 Bourdeau et al. 2013; Freeman et al. 2014; Hooks and to 2014 (Table 1) and identified 274 studies. In addition Padilla 2014). Thus, the general importance of evolution- to our literature exclusion process, we also searched the ary history/novelty in mediating plastic prey responses to references in the collected papers for supplementary litera- predators is still not well understood; accordingly, a more ture that was missed through keyword search. The data set comprehensive approach is called for to improve our has been submitted to DOI: doi:10.5061/dryad.b06f9. understanding concerning the evolution of adaptive phe- In order to summarize and quantify large sets of data, notypic plasticity in novel predatorÀprey interactions. meta-analysis has proved to be a powerful statistical tool. Marine molluscs such as bivalves and gastropods have a To create a consistent estimate of the quantitative mea- long history in the study of inducible defensive traits sure of phenotypic plasticity, we calculated a common (Appleton and Palmer 1988; Leonard et al. 1999; Trussell unit, the effect size, using the same methodology as in and Nicklin 2002; Edgell and Neufeld 2008; Bourdeau Hollander (2008); implementing Hedge’s d (Gurevitch 2009, 2010a; Freeman and Hamer 2009; Hollander and and Hedges 1993) as an effect size to quantify plasticity Butlin 2010). These taxonomic groups have served as a for each study. The data set was additionally divided into model owing to a number of beneficial characteristics, such four different variables in order to assess each variable as their accessibility on rocky and sandy shore habitats, separately. The four variables were as follows: life-history well-defined defensive traits that can easily be quantified, (comprising growth rate), behavior, shell morphology, and amenability to rearing in laboratory environments. For and soft tissue morphology. The soft tissue morphology that reason, there are numerous studies available in the describes the soft part of the animal, and in bivalves this published literature. Here, we provide a test where we syn- is often adductor mussel size or ‘meat’. We analyze these thesize previously published data, with the purpose of variables separately for both taxa together, and in examining whether prey species that are exposed to non- gastropods and bivalves exclusively. native predators (those without a shared evolutionary his- Hedge’s d uses arithmetic means of the phenotype from tory), whether prey show reduced phenotypic plasticity in the experimental group and correspondingly from the con- response to novel predators (those without a shared evolu- trol group’s mean phenotype. The equation to calculate tionary history) compared to prey that are exposed to Hedge’s d also requires the standard deviation and the native predators (with which they share an evolutionary sample size for each study from both the experimental and history). A benefit of this study system is the fact that sev- the control group. Studies are likely to vary in the degree eral of the species included in the present analysis are repre- of difference between treatments, which may influence the sented in each of the two contrasting groups: (1) naive phenotypic effect observed, but meta-analysis is robust to native prey exposed to non-native predators; and (2) expe- such variation(Rosenthal 1991) and it is unlikely to be rienced native prey exposed to native predators. confounded with the origin of the predator (native vs. non-native). Moreover, since we assumed a random com- Methods ponent of variation among effect sizes (Rosenthal et al. 2000), we used a mixed model. The analyses were con- We used ISI Web of Science (WoS) database and search ducted in the statistical software MetaWin 2.0 (Rosenthal engine to sample multiple independent studies published et al. 2000). Additionally, we used what is termed ‘Reversal in the peer-reviewed scientific literature. We used the fol- marker’ in the software, which enables the direction of the lowing search string to identify relevant papers by: effect between the control and the experimental treatments Topic = (snail* OR gastropod*) AND (plastic* OR phe- to always be positive (Gurevitch et al. 1992). In order to notyp* plastic* OR induce*) and (bivalve* or mussel* or test for the robustness of data due to publication bias (i.e., clam* or oyster*) AND (plastic* OR phenotyp* plastic* when negative results have a