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Regressive Evolution of Vision and Speciation in the Subterranean Diving Beetles from Western Australia

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Regressive Evolution of Vision and Speciation in the Subterranean Diving Beetles from Western Australia Regressive Evolution of Vision and Speciation in the Subterranean Diving Beetles from Western Australia Barbara Langille A thesis submitted for the Degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology School of Biological Sciences, Faculty of Sciences The University of Adelaide January 2020 2 Table of Contents Abstract…………………………………………………………………………………….6 Declaration………………………………………………………………………………...8 Full citations of publications that appear in this thesis……………………………….8 Acknowledgements……………………………………………………………………..10 Chapter 1: The evolution of subterranean diving beetles (Dytiscidae) from Western Australia………………………………………………………………….……13 Regressive evolution…………………………………………………………….14 Neutral mutation theory………………………………………………..16 Natural selection………………………………………………………...18 Direct natural selection: Positive and negative……………….19 Indirect natural selection: pleiotropy and linkage…………...20 Difficulties distinguishing the neutral and selection hypothesis for regressive evolution……………………………………………………..21 Photophobic behaviour in subterranean animals……………………………23 The evolution of eyes in subterranean animals………………………………24 The general mechanism behind sight…………………………………25 Genes involved in eye regression……………………………………...26 Light detecting opsin genes………………………………….....27 Light absorbing genes: Pigmentation of the eye……………..29 Eye regression in cavefish Astyanax…………………………………………...31 Subterranean ecosystems in Australia………………………………………...33 Arid Australia and calcrete aquifers…………………………………..33 Stygofauna and troglofauna in calcretes……………………………...35 Subterranean diving beetles: An excellent candidate system for future regressive evolutionary studies………………………………..37 Aims of the project……………………………………………………………………...42 3 References………………………………………………………………………………..44 Chapter 2: How blind are they? Phototactic responses in stygobiont diving beetles (Coleoptera: Dytiscidae) from calcrete aquifers of Western Australia……………..59 Chapter 3: Evidence for speciation underground in diving beetles (Dytiscidae) from a subterranean archipelago………………………………………………………69 Chapter 4: Darwin’s dilemma: Neutral evolution drives vision-gene loss in blind beetles………………………………………………………………………………….....99 Chapter 5: General Discussion………………………………………………………..123 Retained negative phototaxis and the importance of this discovery……………..124 Modes of speciation in subterranean beetles: evidence for speciation underground from a neutrally evolving gene……………………………………………………….126 Comparative genomic study reveals neutrally evolving vision genes…………...128 Regressive evolution and the importance of the subterranean diving beetle system…………………………………………………………………………………...130 Future directions……………………………………………………………………….132 References………………………………………………………………………………136 Appendix 1: Publications relating to this project…………………………………...146 Appendix 2: Conference presentations relating to this project……………………147 Appendix 3: Chapter 2: Appendix 1…………………………………………………………………148 Chapter 2: Appendix 2…………………………………………………………………157 Appendix 4: Chapter 3: Supplementary Table 1…………………………………………………...163 Chapter 3: Supplementary Table 2…………………………………………………...164 Chapter 3: Supplementary Figure 1………………………………………………......165 Appendix 5: Chapter 4: Supplementary information: Table SI1………………………………….168 Chapter 4: Supplementary information: Table SI2………………………………….171 Chapter 4: Supplementary information: Table SI3………………………………….184 4 Chapter 4: Supplementary information: Figure SI4………………………………...186 Chapter 4: Supplementary information: Figure SI5………………………………...189 Chapter 4: Supplementary information: SI6…………………………………………190 Chapter 4: Supplementary information: SI7…………………………………………194 Chapter 4: Supplementary information: SI8…………………………………………196 5 Abstract Subterranean animals are highly specialized for life underground, having converged on regressive traits such as on loss of eyes/vision and pigmentation. Despite centuries of study, understanding the evolutionary processes and genetic basis for regressive characters is still the subject of considerable debate, with two main evolutionary drivers at the forefront: natural selection and neutral evolution. An assemblage of independently-evolved beetle species (Dytiscidae), from a subterranean archipelago in Western Australia, converged on eye/vision loss, providing a powerful system to explore the genetic basis of adaptive and regressive evolution in parallel. I conducted a behavioural light-dark study of six subterranean beetle species in the genera Paroster and Limbodessus, and revealed evidence for one light avoiding species. This study suggested that highly troglomorphic beetles may have evolved from an ancestor that exhibited negative phototaxis as a pre-adaptation to living in permanent darkness. To investigate whether genes specifically involved in vision showed patterns of neutral evolution, I carried out exon capture analyses on a suite of phototransduction genes, from a total of 36 beetle species (32 stygobionts and 4 surface beetles). I found evidence for pseudogenisation of six genes in multiple species, supporting the neutral theory. Finally, an 18 base pair deletion and a shared stop codon were found in the long wavelength opsin gene of a phylogenetic sister triplet of beetle species from one calcrete. I sequenced long wavelength opsin in other Paroster species and mapped the mutations to a robust multi-gene phylogeny, to show that the mutation was unique to these three sister species. These analyses provide strong evidence that the three species evolved underground from a common 6 ancestor that was already adapted to living underground. My studies add to the growing body of evidence supporting the neutral theory as the mode of eye regression and the potential for speciation underground, and further highlight that subterranean dytiscids provide a unique model system for exploring fundamental questions on the evolution of subterranean animals. 7 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 text. In addition, I certify that no part of this work will, in 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. I acknowledge that copyright of published works contained within this thesis resides with the copyright holder(s) of those words. Full citations of publications that appear in this thesis: Langille BL, Tierney SM, Austin AD, Cooper SJB (2019) How blind are they? Phototactic responses in stygobiont diving beetles (Coleoptera: Dytiscidae) from calcrete aquifers of Western Australia. Austral Entomology. doi: 10.1111/aen.12330 Tierney, SM, Langille BL, Humphreys WF, Austin AD, Cooper SJB (2018) Massive parallel regression: A précis of genetic mechanisms for vision loss in diving beetles. Integrative and Comparative Biology, 58, 465-479. doi: 10.1093/icb/icy035 I also 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. 8 I acknowledge the support I have received for my research through the provision of an International Postgraduate Research Scholarship and an Australia Postgraduate Award. Signed: Barbara Langille Date: 16/01/2020 9 Acknowledgements Many important people have helped me through this grand PhD adventure, with my supervisor, Steve Cooper at the top of the list. Thank you to Steve for his great advice, countless chats, endless hours reading and editing my manuscripts and abstracts, his support and positive demeanour, his patience when explaining theories or writing plans, and his mentorship in this daunting field. Steve made this journey memorable and enjoyable and I couldn’t imagine a better supervisor. I also had the amazing luck to have two brilliant co-supervisors; Simon Tierney and Andy Austin. I would like to thank Simon for helping me with my various analyses, editing my written work, and for the many chats over the years. Thank you to Andy Austin for always being positive and supportive, and for polishing my manuscripts to perfection. Thank you to the University of Adelaide for the International Postgraduate Research Scholarship and the Australia Postgraduate Award, that were essential in allowing me to undertake this project. I would like to thank Kathy Saint and Tessa Bradford for the support they gave in the molecular labs, and particularly to Kathy for guiding me through many complicated lab protocols. Thank you to Terry Bertozzi for spending countless hours explaining bioinformatics to me and actually making sense of it all. Without Terry, I could never have handled or even understood my data. Many thanks to Bill Humphreys for editing many manuscript drafts with a positive, reassuring attitude, and Andrea Crowther for supporting my research through the South Australian Museum. I would also like to thank Chris Watts, Karl Jones, and 10 Mark Haase for the photographs of beetles they allowed me to use in my publications and my thesis. Through my years in Adelaide, I
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