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Interspecific variation in larval anuran anti-parasite behavior: a test of the adaptive plasticity hypothesis

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Abstract

Identifying drivers of interspecific differences in trait plasticity is a major goal in ecology and evolution. For instance, understanding why species invest in constitutive or induced defenses against pathogens is critical for developing accurate models of host-parasite interactions. The adaptive plasticity hypothesis (APH) suggests that, due to costs associated with plasticity, species with greater heterogeneity in their association with an enemy should be more likely to exhibit a plastic (i.e., induced) defense. Here, I tested whether the APH can explain variation among eight co-occurring anuran species in a plastic defense (change in activity level after parasite exposure) against a common trematode parasite (Digenea: Echinostomatidae). The species examined vary in life history, habitat use and phenology—traits that influence the frequency of encounters with parasites in natural ponds. Laboratory experiments were used to measure the proportional change in species’ activity in response to parasites and infection levels, and experimental results were then coupled to data from a field survey. Consistent with the APH, the activity change was greatest for species that vary most in their association with parasites, even when accounting for species phylogeny. Habitat use may thus have influenced the evolution of parasite avoidance, comparable to a similar pattern in species’ defenses against predators. Infection levels, however, correlated with species’ baseline activity levels rather than the change in activity post-exposure. General activity levels may thus contribute more strongly to species-level differences in infection rates than plasticity. Overall, these findings suggest that the APH and consideration of behavior generally enhances understanding of interspecific variation in defenses and susceptibility to parasitism, with implications for community-scale interactions and amphibian conservation.

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Acknowledgments

I thank Ariel Heldt, Jared Vitala, and Alexandria Novo for assistance in the field and laboratory; Chris Davis and Mike Benard for assistance with animal collection, phylogenetic analysis, and data collection; Earl Werner, Deborah Goldberg, Manja Holland, and members of Meghan Duffy’s laboratory provided helpful suggestions that greatly improved this manuscript. I thank members of the long-term ESGR pond survey group for sharing their data. This work was supported by the National Science Foundation (DEB 1110137) and the University of Michigan Edwin S. George Reserve Scholarship Award.

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  1. John A. Marino Jr.

    Present address: Department of Statistics, University of Michigan, 431 West Hall, 1085 S. University Ave., Ann Arbor, MI, 48109, USA

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  1. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

    John A. Marino Jr.

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Correspondence to John A. Marino Jr..

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Figure S1

Phylogeny of the anurans used in this study. PT = Pseudacris triseriata, PC = P. crucifer, HV = Hyla versicolor, BA = Bufo americanus, RCL = Rana clamitans, RCA = Rana catesbeiana, RS = Rana sylvatica, RP = Rana pipiens. Phylogeny was constructed based on established relationships among taxa and published divergence times (see “Methods” for details; Bossuyt et al. 2006; Frost et al. 2006; Hillis and Wilcox 2006) (TIFF 500 kb)

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Marino, J.A. Interspecific variation in larval anuran anti-parasite behavior: a test of the adaptive plasticity hypothesis. Evol Ecol 30, 635–648 (2016). https://doi.org/10.1007/s10682-016-9831-x

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