Anuran hatching mechanisms and their role in adaptive plasticity
Cohen, Kristina Luisa
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Across animals, embryos regulate hatching timing in response to environmental cues. This is well-documented in frogs, where some species accelerate hatching to escape threats such as egg-predators, pathogens, flooding, and dehydration, while others delay hatching until cues indicate favorable conditions for larvae. The diversity of reproductive modes and cued hatching responses make anurans excellent subjects for the study of environmentally cued hatching (ECH). Nonetheless, the mechanisms by which frogs alter hatching timing were unknown. The hatching process has been described for only a few aquatic-breeding species: hatching gland cells (HGCs) secrete hatching enzyme (HE) that gradually digests the vitelline membrane. I investigated hatching mechanisms and their regulation in two anurans with well-documented hatching plasticity. Obligately terrestrial embryos of Agalychnis callidryas hatch early to escape flooding, drying, and fungus, and within seconds in predator attacks. I discovered that their hatching mechanism is novel: two types of HGCs mediate hatching at different developmental stages and differ in their distribution, morphology, and timing of appearance and regression, but produce the same HE, storing it for acute release. The vitelline membrane is digested locally at hatching, with no prior degradation. Facultatively terrestrial Dendropsophus ebraccatus embryos hatch early to escape drying and ant attacks. We found that HGC abundance and HE gene expression peak early, then decline before hatching, and that vitelline membranes degrade gradually, as described in aquatic eggs. Drying-induced acceleration of hatching is not mediated by changes in HGC development, HE gene expression, or embryo behavior. However, in simulated attacks, rapid enzyme release leads to local vitelline membrane rupture and embryos escape. Thus, both species use acute HE release to escape acute threats, despite other differences in hatching mechanisms. Agalychnis callidryas shows greater control of the timing of HE-release and a novel HGC type that extends the developmental period when hatching is possible. Mechanisms that enable and regulate hatching shape embryos’ capacities for adaptive shifts in hatching timing. Ancestral flexibility may be elaborated or further modified in species with more dynamic plastic responses. The diversity of anuran hatching mechanisms revealed here will facilitate comparative work to understand the evolutionary diversity of hatching strategies.