Evolution of Adaptive Plasticity: Risk‐sensitive Hatching in Neotropical Leaf‐breeding Treefrogs

Abstract

Abstract. Adaptive plasticity at switch points in complex life cycles (e.g., hatching, metamorphosis) is well known, but the evolutionary history of such plasticity is not. Particularly unclear is how a single plastic response (e.g., shifts in hatching timing) evolves to respond to different threats and cues (e.g., abiotic and biotic). We conducted a comparative phylogenetic study of hatching plasticity in a group of frogs with arboreal embryos to determine when risk-accelerated hatching evolved in the clade, whether responses to two common egg-stage risks (snake predation and flooding) evolved independently, and whether the overall capacity for hatching plasticity was evolutionarily more conservative than responses to specific cues. Red-eyed treefrogs (Agalychnis callidryas) hatch early to escape from several egg-stage risks but otherwise hatch later, improving larval survival with predators. We reconstructed a phylogeny for Agalychnis and related genera based on three mitochondrial and four nuclear genes. We quantified onset of hatching competence, spontaneous hatching timing, responses to egg-stage risks, and costs of premature hatching in Agalychnis and Pachymedusa. We also assessed hatching plasticity in a basal phyllomedusine, Cruziohyla calcarifer. The capacity to hatch ;30% before the spontaneous hatching age appears ancestral for phyllomedusines, with little change over ;34-50 million years among the species examined. A strong hatching response to flooding, with no mortality of hatching-competent eggs, is similarly ancient and conserved. Premature hatchlings of Agalychnis and Pachymedusa are more vulnerable to fish predation than are full-term hatchlings, indicating a conserved risk trade-off across hatching that would make plasticity advantageous. In contrast, the hatching response to snake attack has undergone major changes at least twice in the Agalychnis-Pachymedusa clade, with two species showing substantially lower escape success than the others. Responses to different threats have thus evolved independently. The capacity for switch point plasticity may be evolutionarily more stable than the response to individual stage-specific threats.

External gills and adaptive embryo behavior facilitate synchronous development and hatching plasticity under respiratory constraint

“…Particularly at early developmental stages, this is the predominant functional framework for investigations of embryo behavior. Research on adaptive plasticity in hatching has demonstrated that embryo behavior, and appropriate responses to environmental cues, can be also of immediate importance for survival (Warkentin, 2007;Gomez-Mestre et al, 2008;Warkentin and Caldwell, in press). Similarly, behavioral interactions of bird embryos, shortly before hatching, with parents and siblings appear to have immediate functions in care solicitation and hatching synchronization (Brua, 2002).…”

“…While solving a physiological problem, hatching earlier may, however, create an ecological one. More mature hatchlings typically have greater sensory development and/or locomotor abilities (Fuiman, 2002), both of which can reduce mortality from predation (Sih and Moore, 1993;Warkentin, 1999a;Gomez-Mestre et al, 2008). If predators or other factors in the post-hatching environment impose selection for later hatching, then mechanisms to extend embryonic development will be favored (Warkentin, 2007).…”

How embryos escape from danger: the mechanism of rapid, plastic hatching in red-eyed treefrogs

“…Agalychnis callidryas eggs are laid in masses of, on average, 40 eggs (Gomez-Mestre et al, 2008b) that are attached to a substrate by a layer of jelly. Egg masses on leaves were collected from Ocelot Pond (9°6′8.62″N, 79°40′56.96″W), Bridge Pond (9°6′50.26″N, 79°41′48.13″W) and Experimental Pond (9°7′14.77″N, 79°42′ 12.03″W) near and in Gamboa, Panamá, under permits from the Panamanian Autoridad Nacional del Ambiente (SE/A-41-08, SE/A-13-11, SC/A-19-11 and SC/A-16-12).…”

“…Other phyllomedusines can also hatch rapidly from their terrestrial eggs (e.g. Agalychnis annae, A. moreletti, Pachymedusa dacnicolor, Cruziohyla calcarifer; Gomez-Mestre et al, 2008b) and may share the rapid hatching mechanism of A. callidryas. Clades that have independently evolved terrestrial eggs and rapid escape-hatching [e.g.…”

“…However, rapid, predatorinduced hatching is not unique to A. callidryas. Two other Agalychnis species and the closely related Pachymedusa dacnicolor also have high escape success in snake attacks, and a more distantly related phyllomedusine, Cruziohyla calcarifer, hatches rapidly in response to mechanically simulated attack, suggesting that this ability may be ancestral or common in the group (Gomez-Mestre et al, 2008b). The glassfrogs, Centrolenidae, evolved terrestrial eggs independently of phyllomedusines (Gomez-Mestre et al, 2012), and some species can also hatch rapidly, to escape from predators, with no prior degradation of the membrane (J.…”