The Conduit / Cul-De-Sac Hypothesis
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Spider Sperm Competition: The Conduit I Cul-De-Sac Hypothesis- A Route To Understanding Or A Dead End? By Paul James Yo ward DPhil. Thesis University of York Department of Biology September 1996 IMAGING SERVICES NORTH Boston Spa,Wetherby West Yorkshire, lS23 7BQ www.bl.uk PAGE NUMBERING AS ORIGINAL IMAGING SERVICESNORTH , Boston Spa,Wetherby West Yorkshire, LS23 7BQ www.bl.uk MISSING PAGES ARE UNAVAILABLE For Atnina 2 "Let the arachnologist watch his spiders in the life before he kills them to describe their carcasses, and the facts of structure will have a richer and more inspiring influence" "This is the reason why mothers are more devoted to their children than fathers: it is that they suffer more in giving them birth and are more certain that they are their own". Aristotle 4th Century BC (my emphasis) "...But this does not mean that the sperm from the first copulation is only instrumental in the fertilization of eggs. The sperms are retained in the female's spermathecee, and ... they are kept alive for long periods. Where several copulations take place the spermathecee will contain the sperms from each copulation mixed together, so, as spiders are polygamous, the males which mate most frequently will leave the largest number of offspring". Bristowe (1929) 3 0.0 Abstract This thesis is an evaluation of the hypothesis that the spennathecae of spiders affects the sperm precedence patterns in a predictable way (Austad 1984). Spermathecae come in two varieties: cul-de-sac and conduit. Cul-de-sac spennathecae, according to the hypothesis, are supposed to lead to second male sperm priority and conduit to first male sperm priority . The hypothesis was evaluated both directly and indirectly. Direct measurements were made of paternity in two species, Pholcus phalangioides and Tetragnatha montana, both of which are cul-de-sac species. It was found that P. phalangioides complies with the predicted precedence pattern and thus does not disprove the hypothesis. This second male priority pattern was despite a much shorter mating time by second mating males. In T. montana no precedence pattern was found, with equal likelihood of first or second mating males of gaining paternity. There was in T. montana a possible influence of the duration of mating affecting the precedence pattern, with longer mating males gaining a higher paternity no matter what order they mated in. It is discussed whether or not this is due to sperm loading or genitalic stimulation (Eberhard 1985). Indirect evaluation of the hypothesis included an analysis of mating behaviour in Zygiella x-notata which is a conduit species and was chosen as a comparison to the two cul-de-sac species. In Z. x-notata it was found that there was no difference between mating duration in first and second mating males. Mating persistence is thus the same in first and second mating males, suggesting that the males cannot detect that the female is a denuded 4 resource to second mating males. Hence first male priority may not be a factor in this species. Other indirect methods of evaluating the hypothesis involved charting the incidence of mate-guarding and mating-plugs. The expected pattern of mate-guarding was for conduit species to pre-mate guard and for cul-de-sac species to post-mate guard, because of the predicted sperm precedence patterns associated with the spermathecae. The predicted pattern was not found. In the case of mating-plugs it was predicted that these should be deployed by cul-de-sac species because it is in these species that second males are able to usurp paternity to a large extent. The opposite pattern was found with mating-plugs of various design being utilized by conduit species. It is postulated that mating-plugs are the mechanism by which first male priorities are established in conduit species, where this pattern is found. The absence of plugs in cul-de-sac species is possibly the reason that second males can cuckold. The additional data collected since 1984 reveal that patterns of paternity found in spiders seem to be more complex than was originally assumed by Austad (1984). Spermathecae are species-specific in character and this may reflect a species specificity in sperm precedence patterns. Thus the conduit I cul-de-sac dichotomy may not reflect a useful prediction of patternity patterns. 5 Table of contents 0.0 Abstract. 4 0.1 Acknowledgements. 6 1.0 General Introduction. 12 12 1.1 Sexual Selection And Spiders: Early Enthusiasm, Later Neglect. 12 1.1.1 Male-Male Competition. 15 1.1.2 Female Choice. 1.2 The Expansion Of Sexual Selection Into The Realm Of Primary Sexual Characteristics: A Controversial Chapter Of Sexual Imperialism. 16 16 1.2.1 Primary And Secondary Sexual Characters. 19 1.2.2 Sperm Competition. 1.2.3 Genitalia 20 1.3 Sperm Competition In Spiders: Sexual Selection Continuing After Copulation. 23 1.4 Spermathecal Architecture And Sperm Precedence Patterns: The History Of An Idea. 26 1.4.1 Insects. 26 1.4.2 Spiders. 28 1.5 The Entelegynae And Haplogynae: Shifting Definitions, Shifting Phylogeny. 34 6 1.6 Differences Between Spider And Insect Reproductive Systems: Importance To Sperm Competion And Spermathecal Influence Over Sperm Precedence. 36 41 1.7 Project Aims And Intoducing The Study Species. 2.0 Sperm Precedence Measurements In Pholcus phalangioides (Fuesslin) (Araneae, Pholcidae). 45 45 2.1 Introduction. 45 2.1.1 Distribution And Population Structure. 2.1.2 Phenology And Life History. 48 51 2.1.3 Morphology Of Body And Gametes. 2.1.4 Implications From The Biology Of Pholcus phalangioides For Sexual Selection. 53 55 2.2 Specimen Collection. 2.3 Mating Experiments. 56 2.3.1 Mating Observations And Data. 59 67 2.4 Rearing Methods. 70 2.4.1 Rearing Data. 2.5 Specimen Harvest, Storage And Preparation. 74 2.6 Electrophoresis. 75 2.6.1 Zymogram Interpretation. 78 89 2.6.2 Trends In P2 Data. 7 2.6.3 Incidence Of Multiple Paternity In The Wild And Genetic Variation At Collection Sites. 92 100 2.7 Discussion. 3.0 Sperm Precedence Measurements In Tetragnatha montana (Simon) (Araneae, Tetragnathidae). 105 105 3.1 Introduction. 105 3.1.1 Phylogeny. 106 3.1.2 Distribution, Habitat And Population Structure. 107 3.1.3 Phenology, Life History And Activity Periods. 108 3.1.4 Morphology Of Body, Spermathecae And Palps. 112 3.2 Mating Experiments. 113 3.3 Rearing. 114 3.4 Analysis Of Genetic And Paternity Data. 114 3.4.1 Genetic Data. 119 3.4.2 Wild Collected Specimens. 119 3.4.3 Paternity Data. 124 3.4.4 Wild Matings. 126 3.5 Mating Behaviour. 137 3.6 Discussion and Conclusions. 8 4.0 Mating Observations On Zygiella x-notata (Clerck 1757) (Araneae, Araneidae). 139 139 4.1 Introduction. 141 4.1.1 Relevant Natural History. 143 4.2 Mating Experiments. 150 4.3 Results. 150 4.3.1 Qualitative Results. 151 4.3.2Quantitative Results. 168 4.4 Discussion And Conclusions. 171 5.0 Sperm Competition And Its Evolutionary Consequences In The Spiders. 171 5.1 Introduction. 5.2 Incidence Of Polyandry And Other Preadaptations Towards High Levels Of Sperm Competition. 171 174 5.2.1 Sex Ratios. 175 5.2.2 Females' Sperm Storage Organs And Sperm Longevity. 176 5.3 A Re-evaluation Of Current Measurements OfP2' 5.4 Additional Sources Of Evidence Pertaining To Sperm Precedence: Peri-reproductive behaviours. 178 5.4.1 Mate Guarding. 178 182 5.4.2 Grasping Organs: A Novel Suggestion For Their Evolution. 9 5.4.3 Mating Plugs. 183 5.4.4 Single Palp Usage. 186 5.5 The Logic Of Stratification. 186 5.6 The Breakdown Of Stratification. 187 5.7 Sperm Utilization Strategies: Phyletic Limitation Or Adaptation? 189 225 6.0 General Discussion. 240 7.0 Glossary 243 8.0 Bibliograpby. 10 0.1 Acknowledgements I would like to acknowledge the assistance of a number of people in the completion of this project. Firstly I would like to thank Geoff Oxford for invaluable supervision, provision of facilities at the University of York and for securing a research studentship awarded by the Science and Engineering Research Council. Secondly I would like to thank those who responded to my requests for help on various questions pertaining to the thesis: Steven Austad, Dave Bilton, Jean Dennison, Raymond Forster, Rosemary Gillespie, Paul J. Watson, John Prenter, Nancy Reagan, Jeremy Searle, Mike Siva-Jothy, Dave Thompson, Soren Toft, Gabriele UbI and Fritz Vollrath. Thirdly I would like to thank everybody who sent me spider samples: A.E. ('Joddy') Cooper, Stan Dobson, Francis Farr-Cox, Chris Felton, Martin Filmer, E. Gardiner, Basil Harley, Dick Jones, Frank Katzer, Paul Lee, Cynthia Merrett, Andrew Sedman, the late Clifford Smith, Peter Smithers, Yvone Western and James Wright. Finally Iwould like to thank my parents who gave me both financial and emotional support during the completion of this thesis. 11 1.0 General Introduction! 1.1 Sexual Selection And Spiders: Early Enthusiasm, Later Neglect. Within two decades of Darwin's 'The Descent of Man, and Selection in Relation to Sex' (1871) the Peckhams were using spiders as study animals to investigate empirically sexual selection. Their work was summarised in two monographs on the Attidae (= Salticidae) (Peckham & Peckham 1889, 1890). In the years following this early enthusiasm, and up until the nineteen sixties, both araneology .and sexual selection were relatively neglected. In the case of araneology the neglect was a result of a lack of commercial interest, for sexual selection it was a lack of a theoretical framework. Despite the neglect a number of strands in spider sexual selection research have become evident since the nineteen sixties.