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Sex in Southern African Spirostreptida Millipedes: Mechanisms of Sperm Competition and Cryptic Female Choice

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Sex in Southern African Spirostreptida Millipedes: Mechanisms of Sperm Competition and Cryptic Female Choice SEX IN SOUTHERN AFRICAN SPIROSTREPTIDA MILLIPEDES: MECHANISMS OF SPERM COMPETITION AND CRYPTIC FEMALE CHOICE MANDY 8ARNETI University of Cape Town A THESIS PRESENTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN THE ZOOLOGY DEPARTMENT UNIVERSITY OF CAPE TOWN FEBRUARY 1997 The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University of Cape Town ACKNOWLEDGMENTS I am grateful to a large number of people who inspired, guided, assisted and supported me during the various phases of this work. Sincere thanks to Mark Cooper, Mark Dangerfield, Willem Ferguson, Chido Mparnhanga and the many others who helped collect millipedes from around southern Africa, to Peter Croeser for help in animal identification and for the introduction to the South African millipede collection, and to Dr Leo Braak of the Kruger National Park for kind permission to work and collect animals in the park. Thanks also to Solly, Lindy, Jess and Kira Levy for accommodation during the Zimbabwe fieldwork, to Prof. John Loveridge for the use of his laboratory space at the University of Zimbabwe, and to Prof. Gerhard van der Horst for the use of his laboratory space and photographic equipment at the University of the Western Cape. To the staff of the Electron Microscopy Units at the Universities of Pretoria (Prof. Jan Coetzee and Chris van der Merwe) and Cape Town (Miranda Waldron, Dane Gerneke and especially Charlie Bruintjies ), I am grateful for guidance and assistance in specimen preparation. Thanks also to Dane for initially teaching me to drive the S200. Thanks to Babsie Potgieter and Wendy Sutton for advice and assistance in histological preparation, Adrian Baron for inspiration in micro-dissection techniques, to Brian Tibbles for initially introducing me to the use of radioisotopes and to Bruce Dell for technical assistance and the custom made light box. Special thanks to Neville Eden for all the technical support, photography and general patience with my inability to focus! Thanks also to Mark Cooper for the millipede chats, Daniel Polakow for statistical advice, Veronique Suiro for translating the French literature, and especially to Andreas Tadler for sending me copies of much needed scarce papers, deciphering the German literature and helpful discussion. In particular, I would like to thank my principal supervisor Dr Steven Telford for the many hours of discussion, assistance and guidance, and for his invaluable contribution to my academic development. Thanks also to my co-supervisors Dr Sue Nicolson and Prof. Alec Brown for administrative advice and support. Finally, special thanks to my family and Dana, Dena, Franz and especially Marco for logistical, moral and spiritual support. Financial support from the Universities of Cape Town and Pretoria and the F.R.D. is gratefully acknowledged. ii ABSTRACT Spirostreptida millipedes comprise three families, the Harpagophoridae, Spirostreptidae and Odontopygidae. They are polygynandrous. Males transfer sperm via species­ specific accessory genitalia called gonopods, that comprise three components, two of which, the emote and telopodite, are involved in processes of sperm transfer. The emotes function to translocate ejaculates from the penes to the vulvae, where they are stored. A delay between insemination and fertilisation provides an arena for syn- and postcopulatory sexual competition. These operate at the gametic level via sperm competition and cryptic female choice. By combining studies of genital form and function with single and double mating experiments, this study elucidates these processes in some southern African Spirostreptida millipedes. Scanning electron and light microscopy are used to describe gonopod morphology for 26 Spirostreptida species (6 Harpagophoridae, 13 Spirostreptidae, 7 Odontopygidae). For five of these, gonopod functional morphology is also described. The association of gonopod components is similar within families and more particularly within genera, and it is predicted that the functional morphology and mechanisms of competition are conserved within these groups. With the exception of the Spirostreptidae coxites, which are spined, Spirostreptida telopodites are the most complex regions of the gonopods. Gonopod form and function is not accounted for by sperm transfer alone. Structural evidence implicates both cryptic female choice and sperm competition in their evolution. (Chapter 2). Sperm morphology is described for 18 species (8 Harpagophoridae, 7 Spirostreptidae, 3 Odontopygidae) using bright field and phase contrast microscopy. Sperm are non­ motile and either disc- or triangle-shaped. Sperm immotility has implications for the mechanisms of competition because it precludes independent sperm movement into or within the sperm stores (Chapter 2). External vulval morphology is described for 20 Spirostreptida species (8 Spirostreptidae spp; 6 Harpagophoridae spp; 6 Odontopygidae spp ), and a detailed histological account is provided for representative taxa of each family. In all three families, bursae are located in deeply invaginated vulval sacs. Sperm are stored in the bursae in a series of interconnecting ampullae that are associated with bursal glands and iii muscles. Muscles fan out from the spermathecae to the bursal walls. Bursal muscles may "sanction" cryptic female choice via control of ejaculate storage and manipulation. In A. uncinatus (Spirostreptidae), females store sperm for protracted periods and the non-gametic component ofthe ejaculate, the granules, may function as mating plugs. In the Harpagophoridae, bursae protrude from the gonopore. However, the spermathecal ampullae themselves are not directly accessible to the gonopods because the distal telopodites are broader than they are. In both the Spirostreptidae and Odontopygidae, bursae are situated at the bottom of the vulval sacs, some distance from the gonopores. In spite of this, Spirostreptidae telopodites reach the bursal furrow that gives rise to the spermathecal ampullae. Due to the orientation of the bursae and the size of the distal telopodites, gonopods do not enter the ampullae. The orientation of the bursae and their distance from the gonopore suggest that Odontopygidae telopodites do not have direct access to the sperm stores either (Chapter 3). Processes of ejaculate transfer are quantified for two Spirostreptida species, Alloporus uncinatus (Spirostreptidae) and Poratophilus diplodontus (Harpagophoridae). By radiolabelling ejaculates with tritiated thymidine, and separating copula pairs at varying time intervals from the onset of copulation, it is shown that sperm transfer occurs at the beginning of copulation and the proportion of ejaculate at the bottom of the vulvae increases with time. Early insemination has implications for the mechanisms of competition because males cannot manipulate rival ejaculates without also affecting their own. The adaptive significance of prolonging copulation beyond insemination is discussed (Chapter 4). Radioactive labelling techniques are used to examine mechanisms of competition, and to test whether sperm storage is affected by a temporal delay between successive matings (P. diplodontus and A. uncinatus). Because P2 cannot be inferred from a measure of ejaculate volume, the term V 2 is proposed to describe the proportion of ejaculate contributed to the sperm stores of the female by the second of two males to mate with her. Genital manipulation experiments were performed to test the hypothesis that telopodites function in ejaculate placement and displacement. In P. diplodontus, V2 ::::: 0.62 following a double mating. Ejaculate storage is not affected by a 24 hour delay between matings. Vulval capacity is reached with single ejaculates and for subsequent ones to be accommodated, at least 64.52% of prior iv ejaculates must be removed. Removal is partially effected by the distal telopodites (26.46%) but is not totally accounted for by direct male processes. The balance may be effected by ejaculate flushing, a strategy that concurs with smaller ejaculate volumes remaining within the vulvae than are initially transferred. Partial removal may be a consequence ofboth the early onset of insemination (males would be unable to remove rival ejaculates without also affecting their own) and the storage of ejaculates in inaccessible spermathecal ampullae (Chapter 5). In A. uncinatus, vulval capacity is greater than that of P. diplodontus and single ejaculates are apparently too small to fill the vulvae. Coincident with this is a greater number of spermathecal ampullae. Later males do not affect prior ejaculates. Following a double mating V2 ::::: 0.5, unless a temporal delay is imposed between matings in which case females have been shown to reduce the contribution of the first male and V2 ~ 0.71. Spirostreptidae telopodites are implicated in ejaculate transfer, but not in the movement of ejaculates to the bottom of the vulvae. Only in the Spirostreptidae does complete telopodite retraction bring the distal telopodite in contact with the coxite, and the coxal spines may function to temporarily suspend the sperm during copulation (Chapter 6). Preliminary data from mating experiments on the Odontopygidae are discussed. Patterns of insemination are similar to those of A.
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