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The Behavioural and Molecular Ecologies of the Southern Blue-Ringed Octopus, Hapalochlaena Maculosa (Cephalopoda: Octopodidae)

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The Behavioural and Molecular Ecologies of the Southern Blue-Ringed Octopus, Hapalochlaena Maculosa (Cephalopoda: Octopodidae) ResearchOnline@JCU This file is part of the following work: Morse, Peter (2017) The behavioural and molecular ecologies of the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: octopodidae). PhD thesis, James Cook University. Access to this file is available from: https://researchonline.jcu.edu.au/52679/ Copyright © 2017 Peter Morse. The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please email [email protected] The Behavioural and Molecular Ecologies of the Southern Blue-Ringed Octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae) Thesis submitted by Peter Morse, BSc (Hons) in July 2017 for the degree of Doctor of Philosophy in Zoology College of Science and Engineering James Cook University Townsville, Queensland Australia & The Australian Institute of Marine Science Perth, Western Australia Australia ACKNOWLEDGEMENTS I would like to thank my supervisors, Em/Prof Rhondda Jones and the graduate research school at James Cook University for their advice, support and patience over the previous five years. I STATEMENT OF CONTRIBUTION BY OTHERS Nature of Contribution Contributors Assistance Experimental design Em/Prof Rhondda Jones, James Cook University A/Prof Kyall Zenger, James Cook University Dr. Christine Huffard, Monterey Bay Aquarium Research Institute Statistical analyses Em/Prof Rhondda Jones, James Cook University Interpretation and analysis of A/Prof Kyall Zenger, James Cook University genetic data Shannon KJeldsen, James Cook University Intellectual Dr. Monal Lal, James Cook University support Maria Nayfa, James Cook University Document production and editing A/Prof Kyall Zenger, James Cook University Prof Mark McCormick, James Cook University Dr. Christine Huffard, Monterey Bay Aquarium Research Institute Dr. Mark Meekan, Australian Institute of Marine Science Dr. David Reid, editor for the Journal of Molluscan Studies Tuition fee offset Australian Postgraduate Award, Australian Government Stipend Australian Postgraduate Award, Australian Government Graduate Research School, James Cook University Doctoral completion grant College of Science and Engineering, James Cook University Financial Research funding The Australia and Pacific Science Foundation support and Workspace provision The Fremantle Octopus Company infrastructure Provision of aquaria The Fremantle Octopus Company Reef OneTM biOrb Access to commercial vessels and by- João dos Santos catch Peter Stanitch Ocean Foods International Pty. Ltd. Tasmanian Octopus Products Provision of research vehicles Dr. Mark Meekan, Australian Institute of Marine Science The University of Western Australia Field assistance Kirk Hardes Timo Staeudchen Assessment of polarised signalling Prof Justin Marshall, University of Queensland Acquisition of genetic samples from Data South Australia, Victoria and New Dr. Julian Finn, Museums Victoria collection South Wales Assistance with DNA extractions Shannon KJeldsen, James Cook University Dr. Jose Domingos, James Cook University Genotype sequencing and library Diversity Arrays Technology Pty. Ltd. preparation II CONTRIBUTION OF AUTHORSHIP Thesis title: The behavioural and molecular ecologies of the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae) Name of I confirm the candidate’s contribution to Nature and extent of the intellectual input of candidate: Publishable unit: this paper and consent to the inclusion of each author, including the candidate: Peter Morse the paper in this thesis: Chapter: Morse, P. and Huffard, C.L. (unpubl.) A review P. Morse compiled the literature and was the Name: Signature: of reproductive behaviour among the primary author. C. Huffard provided an expert Dr. Christine 2 Cephalopoda. In preparation for Frontiers review of content and revisions to the original Huffard in Ecology and Evolution. manuscript. Morse, P., Zenger, K. R., McCormick, M. I., Collectively, all authors contributed to the Dr. Kyall Meekan, M. G. & Huffard, C. L. (2015). interpretation of data, revisions of the text and Zenger Nocturnal mating behaviour and dynamic content of the final article. P. Morse and C. Huffard Dr. Mark male investment of copulation time in the contributed to the experimental design. P. Morse McCormick 3 southern blue-ringed octopus, and K. Zenger arranged funding. P. Morse Hapalochlaena maculosa (Cephalopoda: organised facilities for this research, collected the Dr. Mark Octopodidae). Behaviour, 152(14), 1883- data, performed data analysis and was the Meekan 1910. primary author. Dr. Christine Huffard Morse, P., Huffard, C. L., Meekan, M. G., Collectively, all authors contributed to the Dr. Christine McCormick, M. I. & Zenger K. R. (in press) interpretation of data, revisions of the text and Huffard Mating behaviour and postcopulatory content of the final manuscipt. P. Morse, C. Huffard Dr. Mark fertilisation patterns in the southern and K. Zenger contributed to the experimental Meekan 4 blue-ringed octopus, Hapalochlaena design. K. Zenger supervised the analysis of maculosa. Animal Behaviour. genetic data. P. Morse and K. Zenger arranged Dr. Mark funding. P. Morse organised facilities for this McCormick research, collected the data, performed data Dr. Kyall analysis and was the primary author. Zenger III Morse, P., Zenger, K. R., McCormick, M. I., Collectively, all authors contributed to the Dr. Kyall Meekan, M. G. & Huffard, C. L. (2017). interpretation of data, revisions of the text and Zenger Chemical cues correlate with agonistic content of the final article. P. Morse and C. Huffard Dr. Mark behaviour and female mate choice in the contributed to the experimental design. P. Morse McCormick 5 southern blue-ringed octopus, and K. Zenger arranged funding. P. Morse Hapalochlaena maculosa (Hoyle, 1883) organised facilities for this research, collected the Dr. Mark (Cephalopoda: Octopodidae). Journal of data, performed data analysis and was the Meekan Molluscan Studies, 83(1), 79-87. primary author. Dr. Christine Huffard Morse, P., Kjeldsen, S. R., Huffard, C. L., All authors contributed to revisions of the text and Shannon Meekan, M. G., McCormick, M. I., Finn, J. K. the final content of the manuscript. P. Morse and Kjeldsen & Zenger K. R. (in press) Genome-wide K. Zenger contributed to the experimental design. Dr. Christine comparisons reveal a clinal species P. Morse and J. Finn collected genetic samples. M. Huffard pattern within a holobenthic octopod - Meekan provided a research vehicle for fieldwork. the Australian southern blue-ringed S. Kjeldsen and P. Morse performed DNA Dr. Mark octopus, Hapalochlaena maculosa extractions and analysed data under guidance Meekan 6 (Cephalopoda: Octopodidae). Ecology and from K. Zenger. P. Morse and K. Zenger organised Dr. M. Evolution. funding for this research. P. Morse was the McCormick primary author. Dr. Julian Finn Dr. Kyall Zenger IV SUMMARY The cephalopods (Mollusca: Cephalopoda) provide a unique animal group for studying the mechanisms and genetic consequences of sexual selection. This is because: i) both males and females can be selective of their mates; ii) males can employ complex phenotypic-conditional mating strategies to secure copulations; iii) promiscuity of both sexes is widespread across this taxon despite no paternal care or resource provisioning by males for the females they mate with; and iv) females store sperm from multiple males until egg-laying, suggesting that sperm competition and cryptic female choice might be strong determinants of resulting fertilisation patterns. Additionally, nearly all cephalopods are relatively short-lived and invest heavily into their reproductive cycles. These characteristics suggest that sexually selected traits and behaviours can evolve rapidly within some cephalopods, making these taxa useful models for the examination animal mating system evolution and exploring mechanisms of speciation based on assortative mating, and pre- or postzygotic reproductive isolation. The southern blue-ringed octopus (Hapalochlaena maculosa) is an endemic Australian octopod that displays several distinctive life-history traits making it an ideal study species for addressing hypotheses related to sexual selection and population divergence. This species has a seven-month life cycle, ending in a synchronous semelparous breeding season. Gametes are limiting for H. maculosa, with males and females possessing approximately 50 spermatophores or eggs per individual respectively. The females hold their small egg-clutches in their arms to protect and clean them until the time of hatching. The young are direct-developing, and so there is no planktonic dispersal phase. Together, these aspects of life history in H. maculosa suggest both that ensuring offspring quality might be particularly important for this species, and that short generation times with no larval dispersal might lead to rapid divergence of heritable traits and behaviours among geographically distant populations. The present study addressed the mating behaviour and genetic structuring of H. maculosa by combining investigations of four separate components of behavioural and molecular ecology in this species. Precopulatory mate choice behaviours were investigated through focal animal observations in the laboratory. Postcopulatory fertilisation processes were assessed through paternity analyses using genotyped V candidate parents. The roles of olfaction
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