The Evolution of Cutaneous Senses in Marine Snakes (Hydrophiinae)

Abstract

Front-fanged elapid snakes (subfamily: Hydrophiinae) have invaded marine habitats twice: the oviparous sea kraits that diverged approximately 18 million years ago and the viviparous sea snakes that diverged approximately six million years ago. Due to these recent marine transitions, marine hydrophiine snakes are embedded within closely-related and extant terrestrial lineages. Within this phylogenetic context, I investigated two questions concerning two cutaneous senses in marine snakes: 1) How has the sense of touch evolved in the transition from land to sea? and 2) How has a novel phototactic trait arisen in sea snakes? Marine snakes possess small scale organs (‘sensilla’) that are presumptive mechanoreceptors widely thought to be co-opted for detecting water motion (i.e. hydrodynamic reception in homoplasy with the lateral line of fish). To test this hypothesis and infer ancestral and derived functions for scale sensilla, I used morphological techniques (quadrate sampling, scanning electron microscopy) to quantify sensilla traits (number, density, area, coverage) among 19 species of terrestrial and marine elapids. After accounting for effects of allometry (head size) and phylogeny (shared descent), I used Bayesian analyses to reconstruct ancestral sensilla traits in sea kraits and sea snakes. I also characterised ultrastructure (histology, immunohistochemistry, transmission electron microscopy) of scale sensilla on the head and tail of two species of sea snakes, Aipysurus laevis and Hydrophis stokesii, which indicate interspecific variation but overall structural similarities with mechanosensory sensilla in terrestrial snakes. These results provide the first evidence for a mechanosensory function for scale sensilla among sea snakes, and a basis for further studies to test for physiological and behavioural responses to water motion among marine snakes. In addition to scale mechanoreceptors, many lineages of sea snakes have conspicuous scale protuberances (e.g. spines, rugosities) with various purportedly sensory and non-sensory adaptive functions. I examined the morphology (scanning electron microscopy, histology) of sexually-dimorphic scale protuberances in turtle-headed sea snakes, Emydocephalus annulatus. Taken together with behavioural data, these morphological results suggest complex mechanosensory roles related to courtship and mating behaviours in this species. Finally, I investigated the evolution and molecular basis of a novel phototactic trait in sea snakes. The movement of tail in response to light detection via the skin (‘tail phototaxis’) is a sensory trait shared by aquatic vertebrates with secretive habits, elongate bodies and paddle-shaped tails, i.e. hagfish, lamprey, aquatic amphibians and sea snakes. I conducted behavioural tests in eight species of sea snakes, developing a preliminary hypothesis for the evolutionary origin of this trait within a small clade of Aipysurus sea snakes. I also quantified tail damage in museum specimens to test whether the probability of sustaining tail injuries is influenced by tail phototactic ability in snakes. I then profiled skin transcriptomes of phototactic snakes to identify candidate phototaxis genes, which can be used to understand the parallel evolution of this trait among vertebrates. This thesis provides the basis for future research on the sensory ecology and evolution of marine snakes. The integrative methods employed speaks to power of these approaches in resolving fundamental questions in evolutionary biology, particularly how novel traits can arise from existing variation.