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Hatching plasticity and the adaptive benefits of extended embryonic development in glassfrogs

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Abstract

Phenotypic plasticity in hatching age has been documented in many animals. A growing body of research indicates that embryos can rapidly hatch to escape egg-stage risk. However, fewer studies have tested whether selective tradeoffs in post-hatching stages favor trait plasticity. We assessed hatching plasticity and its benefits to the larval stage in five species of Neotropical glassfrogs (Centrolenidae). Glassfrog embryos develop on terrestrial vegetation and larvae in benthic stream sediments; thus hatching involves a dramatic habitat shift, when hatchlings must dive past stream fish to reach larval refuges. We found that all five species have extensive plasticity in hatching age and can delay hatching to more than double their minimum embryonic period. Along a stream in Panama, we found evidence that early hatching is induced by the risk of embryo predation, dehydration, and fungal infections. Differences in hatching timing were coupled with changes in hatchling phenotypes, such that younger hatchlings were smaller and less developed than older individuals. To assess locomotor function we measured diving speed, a key performance trait for newly hatched larvae. Older hatchlings dove 1.4–3.8 times faster than younger ones, which would reduce their exposure to predators in the water column. To assess the potential for exotrophic growth, we measured digestive system morphology and feeding onset across hatching ages. Younger hatchlings had intact yolk sacs and spent 4.5–6 days as larvae before feeding, while older hatchlings entered the water with well-developed guts and fed immediately. Therefore, while early hatching enables embryos to escape egg-stage risk, it is associated with initial performance costs and a lag before feeding in the larval stage. We recovered consistent results across multiple genera of glassfrogs, supporting that hatching plasticity is widespread, ancient, and has been maintained by shared selective trade-offs in this family.

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Acknowledgements

We are grateful to L Bravo-Valencia for assisting with field monitoring, and to C Brown, and E Moody, MA Seid, and JFA Traniello for identifying glassfrog predators. P Buston, Lisa Schulte, the associate editor, and an anonymous reviewer kindly provided important feedback on an early version of this manuscript. Funding to JD was provided by the Smithsonian Tropical Research Institute, Boston University, National Science Foundation (DDIG, IOS-1501531), Lewis and Clark Foundation, American Society of Naturalists, Society for the Study of Evolution, Animal Behavior Society, and Society for the Study of Amphibians and Reptiles; to JRO by an REU site Grant to STRI (1359299); and to MSN and KMW by the National Science Foundation (IOS-1354072 to KMW).

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Authors and Affiliations

  1. Department of Biology, Boston University, Boston, MA, USA

    Jesse Delia, María José Salazar-Nicholls & Karen M. Warkentin

  2. Department of Biology, University of Washington, Seattle, WA, USA

    Juana Maria Rivera-Ordonez

  3. Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Quito, Ecuador

    María José Salazar-Nicholls

  4. Smithsonian Tropical Research Institute, Panama, Republic of Panama

    Karen M. Warkentin

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  1. Jesse Delia
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Correspondence to Jesse Delia.

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All research was conducted in accordance with approved IACUC protocols from the Smithsonian Tropical Research Institute (2011-0426-2014-04, 2014–0601-2017-2-A4), and permits provided from the Ministerio de Ambiente, Panama (SE/A-47-11, SC/A-24-12, SE/A-65-13, SE/A-70-13, SE/A-51-14, SEX/A-93-14, SE/A-63-15, SC/A-28-16).

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Delia, J., Rivera-Ordonez, J.M., Salazar-Nicholls, M.J. et al. Hatching plasticity and the adaptive benefits of extended embryonic development in glassfrogs. Evol Ecol 33, 37–53 (2019). https://doi.org/10.1007/s10682-018-9963-2

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