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Inherited Parasites in the Butterfly Hypolimnas Bolina (Lepidoptera: Nymphalidae)

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Inherited Parasites in the Butterfly Hypolimnas Bolina (Lepidoptera: Nymphalidae) Inherited Parasites in the Butterfly Hypolimnas bolina (Lepidoptera: Nymphalidae) by Emily Ann Dyson A thesis submitted for the degree of Doctor of Philosophy of the University of London September 2002 Department of Biology University College London ProQuest Number: 10010111 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest. ProQuest 10010111 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 “The first sight of such a thing as the big Hypolimnas bolina,Linn., black, flashing with violet-blue, excited an emotion better imagined then described. At all events, the creatures took me fairly by storm: collect I must!” G.B. Longstaff ‘Butterfly hunting in many lands: notes of a field naturalist’, 1912 Inherited parasites in the butterfly Hypolimnas bolina Abstract Male killing bacteria are known to be widespread in insects, but the factors determining their presence and effects on natural populations are little studied. Studies of the island- inhabiting Hypolimnas bolina were therefore conducted to elucidate the causes and consequences of prevalence variation. Initial investigation of//, bolina in Fiji revealed the presence of a male killing Wolbachia bacterium associated with low egg hatch rates and all-female broods. The prevalence of the male killing Wolbachia is heterogeneous between islands. Sampling in the islands of Independent Samoa indicated the continued presence of highly female-biased populations in this country, associated with the same male killing Wolbachia strain identified from Fiji. The prevalence of the male killer in Independent Samoa is extreme, and this has severe implications on the host population: the lack of males is associated with increased female virginity and decreased female fertility. The effect of infection on female host survival was examined in Fiji: larvae infected with the male killing Wolbachia bacterium show significantly higher survivorship and are significantly heavier as adults indicating a direct benefit to infection. A prevalence survey was carried out using//, bolina samples from eight different countries. Prevalence is heterogeneous across the butterfly’s range. Another strain of Wolbachia (that does not kill males) is identified from H. bolina populations in both American Samoa and Fiji. The history of the two different Wolbachia infections was investigated through sequence analysis of the mitochondrial COI genes from butterflies deriving from each of the populations. It is concluded that whilst the male killer has undergone a recent selective sweep, the non male killing Wolbachia strain is ancient. The data also indicated that horizontal transmission of the male killing symbiont must be rare. Inherited parasites in the butterfly Hypolimnas bolina Acknowledgements One of the most amazing aspects of this Ph.D. study has been working for such long periods of time in so many different countries. Of course this increased the numbers of people - not only who made the work side of things possible - but, equally importantly, made me feel welcome and at home on the other side of the world. Moving around so much has meant adjusting to new places and new ways of life constantly. There are many people to whom Pm indebted for making this last three years an unforgettable experience, here are a few of them: In Fiji: the Ministry of Forestry provided a laboratory, equipment, friends and assistance. Everyone made me feel welcome and included. Particular thanks go to Eminoni, Eliki, Peni, Willi and Rashmi for their carpentry, butterfly-catching, caterpillar^feeding, sweet potato growing and grog-drinking skill’s. Wilco Liebregts and Madhu Kamath made it possible for me to work at Forestry and provided invaluable advice throughout my 7. months with them. Lashings of gratitude to Suzie, Joe and Joshua without whom I might have had a place to stay/but I wouldn’t have had a home and family. Thanks to you guys and the regular. faces at the Colonial Lodge: Amelia, Emosi, Tina, Paul, Sue and Yolanda...and, of course, to Angelina. To my bodyguards Craig, Glen and Rob and my friends Tanja, Lynette, Diana and Louisa. Wayalailai Island will always be my epitome of paradise - huge thanks to Glenbo for introducing us, and for all the entertaimnent. To the islanders, especially Si and Big Jerry for putting up with all the butterflies and ferrying me between islands to collect. Thanks to all at the Nadi Bay for always finding room for me and the bugs, especially to Elanoa and Mariah. To Mai and Vani in Taveuni for all their help with collection and to Andrew, Angela and all at Matareva, Kadavu for teaching me to dive, breaking my foot and saving my life. In Independent Samoa: the biggest basket of thank yous must go to Paul Davies and Raema Von Reiche - my landlords, advisors, drinking partners and friends. Also to their children: Chris, Blake, Jordon and especially Luana ‘demon-butterfly-catcher’ Milroy. Finally thanks to my friends Oscar, Christine and Helen. In American Samoa: thanks to Barry and Charles for all the advice, transport around the islands and rescuing me from the killer dogs. In Australia: thanks to Darrell Kemp for his collaboration, help and interest and also to Sarah and Brad Love for a fantastic week’s break and silliness. Menno Shilthuizen and Sabah University, Borneo: for arranging my work permit, collecting butterflies, driving us around and attempting to drown us with the aid of a landrover and deceptively large puddle...thanks Menno! To Walter and Lalith in Sri Lanka, and of course the countless children throughout the countries I visited who helped out with the collecting side of things...not always the correct species, but catching butterflies using a fishing net is never easy!! Thanks to Niklas Wahlberg and El in Claridge for providing butterflies from areas that I didn’t make it to. Inherited parasites in the butterfly Hypolimnas bolina In the UK: Firstly to the BBSRC, without whom none of this would have been possible. To Gwyneth and Bernard Johnston for their help and fascinating stories about carrying out the original survey oiH. bolina with Sir Cyril Clarke. Mike Majerus and Frank Jiggins in Cambridge provided advice to a novice butterfly hunter, thanks for all the help and information on all aspects of my research. A huge thank you to all at UCL, particularly Claire, Imogen, Michelle, Mel, and Jim Mallet, my second supervisor. To the past and present chosen elite of room 417, Wolfson House: infinite thank yous to Mary Webberly because she’s fantastic...for her unstinting kindness, generosity, support, advice and friendship. Also to Jo Bentley for putting up with me and my various crises, and being lovely. Everyone has down times doing a Ph.D., but it’s hard when you’re thousands of miles from home, so a big thank you to all my friends for their support, via e-mail and back at home: To Miki, Kevin, Adam, Dan, Tim, Nick, Olivia, Vicky, Rachel, Marc, Erica, Charlie, JP, Robj the UCL girls and of course the Seth Effrikans: Ben, Paul, Taryn, Shannon, Marc, Jules, Craig, Heidi and Ma and Pa Travis. To my housemates Adam, Tam and Andrew for putting up with me and all my papers scattered around the place in various states of disarray. Massive thank you hugs to my mum and dad for being so supportive, wonderful and keeping calm when their daughter kept disappearing to the other side of the world chasing insects, and to Tom who is, and always will be, the fattest brother in the world. Throughout all the island-hopping, round-the-world travelling and long frustrating spells in the lab in London, one person constantly provided support and direction, had cheeky ‘holidays’ in the sun, showed endless patience in teaching not the most natural molecular biologist the world will ever see, and made this last 3 years enjoyable and successful: my supervisor, Greg Hurst. As the first of (I’m sure) many Ph.D. students, a huge thank you to Greg. This thesis is dedicated to Adrian Travis for more reasons than you can shake a stick at: his excellence at butterfly catching (whilst obtaining a perfectly even tan), advice, constant support, putting up with my tantrums, always making me laugh and of course the best chicken impressions this side of the Watford Gap. Kuo la na kana, my Adrian: this one’s for you... Inherited parasites in the butterfly Hypolimnas bolina Declaration This dissertation represents, except where specifically mentioned in the text, the results of my own research. The dissertation is not substantially the same as any that I have submitted for a degree or other qualification this or any other University. No part of my dissertation has already been or is being currently submitted for any such degree or other qualification. Emily Dyson Dr. Gregory Hurst Candidate Supervisor Inherited parasites in the butterfly Hypolimnas bolina Contents List of abbreviations ................................................................................................... 16 Glossary.......................................................................................................................
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