To hatch and hatch not: does heterochrony in onset of vestibular mechanosensing explain species differences in escape-hatching success of Agalychnis embryos in snake attacks?

Abstract

Phyllomedusid treefrogs hatch prematurely to escape egg predation, but escape success varies among species. Snake attacks elicited 55% less escape hatching in spontaneously hatching Agalychnis spurrelli than in less developed A. callidryas. Agalychnis callidryas use their vestibular system and, secondarily, their lateral line to sense physical disturbances that cue hatching. Since A. spurrelli develop faster, we hypothesized that heterochronic shifts in the onset timing of vestibular mechanosensory function, relative to hatching ability, might explain their lower escape response to mechanosensory cues. To test this, we compared onset timings of hypoxia- and mechanosensory-cued hatching (MCH) and vestibular mechanosensory function in developmental series of both species. Across species, most sibships began responding to each cue at the same developmental stage and vestibular function development, measured by the vestibulo-ocular reflex (VOR), was similar. These results demonstrate that low escape-hatching success in A. spurrelli is not caused by a delay in the onset of vestibular mechanosensory function. MCH onset in A. spurrelli was associated with VOR, but with a higher threshold than in A. callidryas. The absence of MCH before strong vestibular function suggests multimodal mechanosensing may not contribute to antipredator responses of A. spurrelli embryos. Our observations of higher escape success of larger clutches in snake attacks and hatching complications in flooded A. spurrelli suggest that differences in clutch and egg capsule structure may contribute directly to species differences in escape-hatching success. Moreover, hatching complications in A. spurrelli may select against false alarms, increasing the stringency of hatching decision rules.

Significance statement

Hatching is an essential life-stage transition during development. For some species, it also functions as an effective defense against egg-stage risks. However, the causes for variation in environmentally cued hatching responses are poorly understood. We assessed why two closely related treefrogs exhibit different escape-hatching responses to snake attacks. Comparing the onset of induced-hatching responses and vestibular function in Agalychnis callidryas and A. spurrelli revealed that the primary mechanism for mechanosensing and its developmental timing are conserved within this group, but the sensory function threshold for behavioral response differs. It also revealed that egg-clutch properties, including egg-clutch size and individual egg structure, affect the escape-hatching response. This motivates further research assessing the role of egg-clutch properties and their biomechanics in embryo escape-hatching responses.