Abstract

During biotic invasions, native communities are abruptly exposed to novel and often severe selective pressures. The lack of common evolutionary history with invasive predators can hamper the expression of effective anti-predator responses in native prey, potentially accelerating population declines. Nonetheless, rapid adaptation and phenotypic plasticity may allow native species to cope with the new ecological pressures. We tested the hypothesis that phenotypic plasticity is fostered when facing invasive species and evaluated whether plasticity offers a pool of variability that might help the fixation of adaptive phenotypes. We assessed behavioural and morphological trait variation in tadpoles of the Italian agile frog (Rana latastei) in response to the invasive crayfish predator, Procambarus clarkii, by rearing tadpoles under different predation-risk regimes: non-lethal crayfish presence and crayfish absence. After two-month rearing, crayfish-exposed tadpoles showed a plastic shift in their body shape and increased tail muscle size, while behavioural tests showed no effect of crayfish exposure on tadpole behaviour. Furthermore, multivariate analyses revealed weak divergence in morphology between invaded and uninvaded populations, while plasticity levels were similar between invaded and uninvaded populations. Even if tadpoles displayed multiple plastic responses to the novel predator, none of these shifts underwent fixation after crayfish arrival (10–15 years). Overall, these findings highlight that native prey can finely tune their responses to invasive predators through plasticity, but the adaptive value of these responses in whitstanding the novel selective pressures, and the long-term consequences they can entail remain to be ascertained.

Highlights

  • Phenotypic plasticity is among the most pervasive and fascinating products of natural selection, and can provide a given genotype the possibility to produce different phenotypic outcomes depending on the environmental conditions experienced (Pigliucci 2001)

  • Understanding the role of phenotypic plasticity is generally complex, because plasticity can occur in multiple traits, can be expressed at different levels in different life history stages, and often trade-offs exist between modifications of one trait and its effects on the regulation of other traits (West-Eberhard 2003; Relyea 2007)

  • We evaluated tadpole responses to the invasive crayfish by assessing a combination of behavioural and morphological traits that typically respond to predators and can be under strong selection in tadpoles (Van Buskirk and Arioli 2002; Relyea 2003; Kishida et al 2010)

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Summary

Introduction

Phenotypic plasticity is among the most pervasive and fascinating products of natural selection, and can provide a given genotype the possibility to produce different phenotypic outcomes depending on the environmental conditions experienced (Pigliucci 2001). Plasticity is often favoured when the environmental context is heterogeneous, such as in environments where conditions are highly variable in time and / or space (Pigliucci 2001; Van Buskirk 2017; Reger et al 2018, but see Leung et al 2020). Under these circumstances, plasticity can allow species to adjust their responses and match challenges posed by changing selective pressures. Plastic responses to novel environmental pressures may not always be adaptive, as plastic shifts not matching the favoured phenotypic optimum can occur (i.e., wrong sign plasticity, hyperplasticity, see Ghalambor et al 2007; Stamp and Hadfield 2020). By interacting with genetic variation in determining phenotype expression, plasticity may broaden the pool of variability on which natural selection acts, and eventually can favour refinement and fixation of traits showing particular adaptive value through genetic assimilation (Pigliucci et al 2006; Levis et al 2018; Levis and Pfennig 2019)

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