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A condition-dependent male sexual signal predicts adaptive predator-induced plasticity in offspring

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Abstract

The possibility that sexual selection promotes adaptive evolution in variable environments remains controversial. In particular, where the scale of environmental variation results in parents and their offspring experiencing different environmental conditions, such variation is expected to break down associations between adult sexual traits and adaptive offspring traits. However, when adaptive offspring plasticity in nonsexual traits acts as an indirect benefit of mate choice, then mate choice for males that produce more plastic offspring could promote adaptation to variable environments. This hypothesis assumes that male sexual signals predict offspring plasticity, which has rarely been tested. To test this assumption, we used spadefoot toads (Spea multiplicata) to investigate whether variation in male sexual signals predicts the expression of tadpole tail-fin plasticity in response to predation cues. Such plasticity has been shown to be adaptive in numerous amphibian taxa. We found that condition-dependent male call characteristics predicted offspring plasticity. Generally, both phenotypic plasticity and female mate choice are ubiquitous in nature; therefore, adaptive associations between male sexual signals and offspring plasticity such as the one reported here might be common.

Significance statement

Sexual signals can indicate individuals’ capacity to sire high-quality offspring, which provides a mechanism by which sexual selection can contribute to adaptive evolution. Whether this occurs in variable environments is unclear, however, because variable environments can expose parents and their offspring to different selection pressures. To address this uncertainty, we investigated the possibility that sexual signals can signal the capacity to sire offspring that express adaptive phenotypic plasticity in response to prevailing selective pressures. Using spadefoot toads, we found that condition-dependent male sexual signals predict the expression of tadpole tail-fin plasticity in response to predation cues. Because this form of plasticity has been demonstrated to be adaptive in several amphibian taxa, our results suggest that associations between sexual signals and adaptive offspring plasticity can allow sexual selection to promote adaptive evolution in variable environments.

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Data availability

Data from this study are available via DRYAD (DOI: 10.5061/dryad.t4b8gtj0w).

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Acknowledgments

We are grateful to J. Sundermann for help with tadpole care, G. Calabrese, C. Chen, and E. Harmon for help with field recordings and collections, and A. Monson for performing tadpole measurements. We are additionally grateful to M. Jennions, R. Fox, A. Baugh, and three anonymous referees for helpful comments on the manuscript.

Funding

Funding was provided by an American Museum of Natural History Theodore Roosevelt Memorial Fund Grant and the National Science Foundation (DEB 1753865 and IOS 1555520).

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Contributions

DWP, PWK, and KSP conceived of the study. PWK performed field recordings and collections, the experiment, and the analyses. PWK drafted the manuscript with help from DWP and KSP. All authors revised and approved the manuscript.

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Correspondence to Patrick W. Kelly.

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The authors declare that they have no conflict of interest.

Ethics approval

All procedures were approved by UNC’s IACUC (IACUC ID 20-016.0 and 20-036.0). Field collections were performed in accordance with permits granted by the Game and Fish Departments of Arizona and New Mexico. All applicable international, national, and/or institutional guidelines for the use of animals were followed.

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Our manuscript is not under consideration for publication elsewhere, and all authors have seen and approved the manuscript for submission. All persons entitled to authorship have been so named.

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Communicated by A. Taylor Baugh

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Kelly, P.W., Pfennig, D.W. & Pfennig, K.S. A condition-dependent male sexual signal predicts adaptive predator-induced plasticity in offspring. Behav Ecol Sociobiol 75, 28 (2021). https://doi.org/10.1007/s00265-021-02968-8

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  • DOI: https://doi.org/10.1007/s00265-021-02968-8

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