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.

Egg-clustering and communal nesting behaviours provide advantages to offspring. Advantages range from anti-predatory benefits, maintenance of moisture and temperature levels within the nest, preventing the eggs from rolling, to enabling hatching synchrony through embryo communication. It was recently suggested that embryo communication may extend beyond development fine-tuning, and potentially convey information about the quality of the natal environment as well as provide an indication of forthcoming competition amongst siblings, conspecifics or even heterospecifics. Here we show that preventing embryos from communicating not only altered development rates but also strongly influenced post-natal social behaviour in snakes. Clutches of water snakes, Natrix maura, were split evenly into half-clutches and incubated as (1) clusters (i.e. eggs in physical contact with each other) or (2) as single eggs placed in individual goblets (i.e. no physical contact amongst sibling eggs). Single incubated eggs produced less-sociable young snakes than their siblings that were incubated in a cluster: the former were more active, less aggregated and physically contacted each other less often than the latter. Potential long-term effects and evolutionary drivers for this new example of informed dispersal are discussed.

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Hatching synchrony is wide-spread amongst egg-laying species and is thought to enhance offspring survival, notably by diluting predation risks. Turtle and snake eggs were shown to achieve synchronous hatching by altering development rates (where less advanced eggs may accelerate development) or by hatching prematurely (where underdeveloped embryos hatch concurrently with full-term embryos). In Natricine snakes, smaller eggs tend to slow down metabolism throughout incubation in order to hatch synchronously with larger eggs. To explore the underlying mechanism of this phenomenon we experimentally manipulated six clutches, where half of the eggs were reduced in mass by removing 7.2% of yolk, and half were used as the control. The former experienced higher heart rates throughout the incubation period, hatched earlier and produced smaller hatchlings than the latter. This study supports the idea that developmental rates are related to egg mass in snake eggs and demonstrates that the relationship can be influenced by removing yolk after egg-laying. The shift in heart rates however occurred in the opposite direction to expected, with higher heart rates in yolk-removed eggs resulting in earlier hatching rather than lower heart rates resulting in synchronous hatching, warranting further research on the topic.