Heartbeat, embryo communication and hatching synchrony in snake eggs

Abstract

Communication is central to life at all levels of complexity, from cells to organs, through to organisms and communities. Turtle eggs were recently shown to communicate with each other in order to synchronise their development and generate beneficial hatching synchrony. Yet the mechanism underlying embryo to embryo communication remains unknown. Here we show that within a clutch, developing snake embryos use heart beats emanating from neighbouring eggs as a clue for their metabolic level, in order to synchronise development and ultimately hatching. Eggs of the water snake Natrix maura increased heart rates and hatched earlier than control eggs in response to being incubated in physical contact with more advanced eggs. The former produced shorter and slower swimming young than their control siblings. Our results suggest potential fitness consequences of embryo to embryo communication and describe a novel driver for the evolution of egg-clustering behaviour in animals.

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

“…In snakes, developing embryos use heart beats emanating from neighboring eggs as a clue for their metabolic level, to synchronize development and ultimately hatching (Aubret et al 2016). Although such a mechanism may explain how the embryos adjust their development to one another, there might be an additional embryo-embryo communication signal to make the final decision to hatch in synchrony.…”

“…For embryo-embryo communication in vertebrates, cues such as sound production, egg vibration, increase in heart rates, odors, or carbon dioxide levels within the nest have been proposed as potential communication signals (Spencer et al 2001, Aubret et al 2016. In S. gregaria, synchronous hatching is observed when the eggs are incubated in a mass, but not when separated (Nishide and Tanaka 2016).…”

“…Recently, the mechanisms controlling timing of hatching have been intensively studied in various species, mainly in vertebrates (Doody 2011, Spencer and Janzen 2011, Webster et al 2015, Aubret et al 2016, Cohen et al 2016. In turtles, eggs are deposited in layers within a nest, and thermal gradients create optimal developmental conditions for each egg.…”

Seeds integrate biological information about conspecific and allospecific neighbours

“…The timing of emergence of a neighbour sibling seed was better synchronized in the presence of 3-and 5-day extracts of T. repens seeds than in their absence (x 2 2 ¼ 12.97, p ¼ 0.002; figure 1d ). Because the 3-day extract had no significant effect on emergence timing, but had a significant effect on synchronization, the results of the extract experiment suggest that synchronization is independent of the acceleration of emergence ( figure 1c,d); Such synchrony suggests that the P. asiatica sibling seeds are able to sense the developmental stage of neighbouring conspecific seeds, thereby altering their development rate, through 'embryonic communication' [23,24]. Why do P. asiatica seeds accelerate their emergence when encountering other species only in the presence of sibling seed?…”

Environmentally induced phenotypic plasticity explains hatching synchrony in the freshwater turtleChrysemys picta

“…In contrast, Murray river short‐necked turtles ( Emydura macquarii ) and eastern long‐necked turtles ( Chelodina longicollis ) both hatch synchronously as a predator avoidance strategy (Tucker et al, ) through metabolic compensation, which is evident through an increased rate of oxygen consumption (O 2 ), and altered heart rate patterns during development (McGlashan et al, , ). Circadian rhythms in heart rate also appear during development, and embryos might be able to detect the heart rate rhythm of their clutch‐mates to communicate developmental stage, and thus respond to perceived differences by metabolically compensating (Aubret, Blanvillain, Bignon, & Kok, ; Loudon, Spencer, Strassmeyer, & Harland, ; McGlashan et al, ).…”