Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

Abstract

Incubation temperature affects developmental rates and defines many phenotypes and fitness characteristics of reptilian embryos. In turtles, eggs are deposited in layers within the nest, such that thermal gradients create independent developmental conditions for each egg. Despite differences in developmental rate, several studies have revealed unexpected synchronicity in hatching, however, the mechanisms through which synchrony are achieved may be different between species. Here, we examine the phenomenon of synchronous hatching in turtles by assessing proximate mechanisms in an Australian freshwater turtle (Emydura macquarii ). We tested whether embryos hatch prematurely or developmentally compensate in response to more advanced embryos in a clutch. We established developmental asynchrony within a clutch of turtle eggs and assessed both metabolic and heart rates throughout incubation in constant and fluctuating temperatures. Turtles appeared to hatch at similar developmental stages, with less-developed embryos in experimental groups responding to the presence of more developed eggs in a clutch by increasing both metabolic and heart rates. Early hatching did not appear to reduce neuromuscular ability at hatching. These results support developmental adjustment mechanisms of the 'catch-up hypothesis' for synchronous hatching in E. macquarii and implies some level of embryo -embryo communication. The group environment of a nest strongly supports the development of adaptive communication mechanisms between siblings and the evolution of environmentally cued hatching.

Hatching behavior of eastern long-necked turtles ( Chelodina longicollis ): The influence of asynchronous environments on embryonic heart rate and phenotype

“…C. picta (Colbert et al, 2010)) or through metabolic compensation (eg. Eastern three-lined skink (Bassiana duperreyi) (Du et al, 2010a) and embryonic E. macquarii (McGlashan et al, 2012)). Neonatal C. longicollis show a level of developmental plasticity that allows them to hatch synchronously, but we found no significant evidence of metabolic compensation in mean daily heart rate throughout the 9 weeks of incubation, similar to Spencer (2012).…”

“…E.macquarii embryos increase metabolic rates throughout the last third of development to catch up and hatch at a similar developmental stage to more advanced clutch-mates. Metabolic compensation does not affect hatchling size and performance immediately and up to 5 months post hatching (Spencer et al, 2001;McGlashan et al, 2012). Less advanced embryos of C. picta also hatch prematurely in response to more advanced siblings, but metabolic compensation is not apparent, in terms of neonatal performance post hatching (Colbert et al, 2010).…”

“…Despite the environmental influence of temperature on incubation length, many avian and reptilian embryos are capable of altering their development and hatching time (Hoyt, 1979;Vleck et al, 1980;Thompson, 1989;Du et al, 2011;McGlashan et al, 2012). Embryos have the ability to alter time of hatching in relation to environment through phenotypic plasticity (Packard and Packard, 2000;Doody, 2011;Spencer and Janzen, 2011).…”

Locusta migratoria (Orthoptera: Acrididae) embryos monitor neighboring eggs for hatching synchrony

“…In turtles, eggs are deposited in layers within a nest, and thermal gradients create optimal developmental conditions for each egg. Interestingly, the eggs hatch in synchrony through embryo-embryo communication, and each egg is able to adjust its individual development to match the rest of the nest (McGlashan et al 2012). In red-eyed tree frogs, Agalychnis callidryas, eggs can hatch early to avoid predation by snakes and wasps in response to vibrational stimuli produced by the predators (Warkentin 1995, Warkentin et al 2007).…”

Arrested embryonic development: a review of strategies to delay hatching in egg-laying reptiles

“…However, a possible factor involved in the process may be thyroid hormone [54,110]. Thyroid hormone is vital for the growth and function of most vertebrate tissues and is capable of acting on both metabolic and nonmetabolic pathways to influence embryonic tissue accretion and differentiation [111].…”