The evolution of extended parental care in glassfrogs: Do egg-clutch phenotypes mediate coevolution between the sexes?

Abstract

Many animals improve offspring survival through parental care. Research on coevolution between parents has provided key insight into the genesis and maintenance of biparental care. However, understanding family dynamics more broadly requires assessing potential male–female coevolutionary processes in the more widespread and common context of uniparental care. Here, we explore how pre-zygotic maternal contributions, jelly coats and oviposition sites, influence offspring dependency and change with the evolution of male-only care in glassfrogs. Egg care appears ubiquitous among glassfrogs, with repeated evolutionary transitions from brief female-only to extended male-only care. Glassfrogs also exhibit a diversity of sex-specific parental traits involving maternal egg-jelly contributions, oviposition-site choice, and egg-attendance behaviors. We hypothesize these form functionally interchangeable suites of traits that mediate embryos' susceptibility to environmental risk. First, using parent-removal field experiments, egg-hydration assays, and comparative analyses, we found no evidence that evolutionary transitions in caring sex or care duration alter the adaptive functions or overall benefits of care (across eight species). Rather, the jelly contributions and oviposition-site use associated with brief care influence embryo susceptibility to the same risks that are reduced by prolonged care. Next, we examined the diversity and evolutionary history of pre- and post-zygotic parental traits, applying phylogenetic comparative methods to literature records and our field observations of 40 species (71 total, ~ 47 % of the family). Because pre-zygotic maternal contributions determine embryo requirements, the evolution of male care might enable and/or compensate for reduced maternal contributions. Supporting this hypothesis, we found that the repeated evolution of complex male care is always associated with reductions in egg-jelly and changes in oviposition sites. This phylogenetic pattern suggests that clutch phenotype might provide a general mechanism for the coevolution of parental investment in species with uniparental care. If different combinations of egg phenotypes and post-zygotic care are ecologically equivalent, their interchangeability could allow parental traits to coevolve between the sexes without compromising offspring survival. Male-only care is widespread in oviparous metazoans, occurring among annelids, molluscs, arthropods, fishes, and amphibians. Investigations of egg and clutch phenotypes offer new prospects for broadening research on the coevolutionary dynamics of parental care.