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The Evolution of Cutaneous Senses In The Evolution of Cutaneous Senses in Marine Snakes (Hydrophiinae) A dissertation by Jenna Margaret Crowe-Riddell Submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy at The University of Adelaide School of Biological Sciences Department of Ecology and Evolutionary Biology January 2019 “It’s not easy when you’re not catching snakes” ˗Arne R. Rasmussen iii iv Summa ry 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 v 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. vi Declaration I certify that this work contains no material which has been accepted for the award of any other degree or diploma in my name in any university or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. In addition, I certify that no part of this work will, in the future, be used in a submission in my name for any other degree or diploma in any university or other tertiary institution without the prior approval of the University of Adelaide and where applicable, any partner institution responsible for the joint award of this degree. The author acknowledges that copyright of published works contained within this thesis resides with the copyright holder(s) of those works. I give permission for the digital version of my thesis to be made available on the web, via the University's digital research repository, the Library Search and also through web search engines, unless permission has been granted by the University to restrict access for a period of time. I acknowledge the support I have received for my research through the provision of an Australian Government Research Training Program Scholarship. Jenna Margaret Crowe-Riddell 15 January 2018 vii Contents Summary ................................................................................................................... v Declaration .............................................................................................................. vii Acknowledgements .................................................................................................... 3 Contributions ............................................................................................................. 5 Co-author affiliations ................................................................................................. 5 Chapter 1 Introduction ............................................................................................... 7 Sensory transitions that accompany major adaptive shifts ............................................ 7 Aquatic transitions in snakes ........................................................................................... 7 The skin as a sense organ .............................................................................................. 12 Broad aims ..................................................................................................................... 17 Thesis outline ................................................................................................................. 18 References ..................................................................................................................... 21 Chapter 2 The evolution of scale sensilla in the transition from land to sea in elapid snakes ..................................................................................................................... 33 Abstract ......................................................................................................................... 33 Introduction ................................................................................................................... 34 Materials and methods ................................................................................................. 35 Results ........................................................................................................................... 41 Discussion ...................................................................................................................... 46 Conclusions .................................................................................................................... 50 Acknowledgments ......................................................................................................... 50 Supplementary materials .............................................................................................. 51 References ..................................................................................................................... 51 Chapter 3 Ultrastructural evidence of a mechanosensory function of scale ‘sensilla’ in sea snakes (Hydrophiinae) ....................................................................................... 59 Abstract ......................................................................................................................... 59 Introduction ................................................................................................................... 60 Materials and methods ................................................................................................. 62 Results ........................................................................................................................... 65 Discussion ...................................................................................................................... 73 Acknowledgements ....................................................................................................... 78 Supplementary materials .............................................................................................. 78 References ..................................................................................................................... 78 Chapter 4 Up close and personal: the role of enlarged scale organs in tactile foreplay of turtle-headed sea snakes (Emydocephalus annulatus) .........................................
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