Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T16:35:12.429Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional significance of elaborate secondary sexual traits and their evolution in the water strider genus Rheumatobates1

Published online by Cambridge University Press:  02 April 2012

Locke Rowe ,
Kathleen P. Westlake  and
Douglas C. Currie
Locke Rowe*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada M5S 3G5 and Department of Natural History, Royal Ontario Museum, Toronto, Ontario, Canada M5S 2C6
Kathleen P. Westlake
Affiliation:
Department of Natural History, University of Toronto, Toronto, Ontario, Canada M5S 3G5
Douglas C. Currie
Affiliation:
Department of Natural History, Royal Ontario Museum, Toronto, Ontario, Canada M5S 2C6
*
2 Corresponding author (e-mail: [email protected]).
Get access Rights & Permissions [Opens in a new window]

Abstract

Sexual conflict may drive the evolutionary elaboration of sexually antagonistic traits that function in mating interactions. One of the most striking cases of elaboration of male morphology occurs in the water strider genus Rheumatobates Bergroth (Hemiptera: Gerridae). The functional significance of the bizarre modifications of appendages in this group is not known. Here we focus on one of the more elaborate of the species, R. rileyi Bergroth. We conduct observational and experimental studies aimed at determining the general sequence of mating behaviour, the role of females in the outcome of sexual interactions, and the functional significance of the highly modified appendages of males. We also map these traits on a known phylogeny of the genus to determine their pattern of evolution. Males repeatedly harass females and females respond with evasive skating or, if the male successfully grasps her, with a premating struggle. The dynamics of the struggle determine the success of mating attempts. Short struggles typically lead to mating, and long struggles typically result in disengagement of the pair. Following a short period of copulation, males withdraw their genitalia and dismount. Females that have been isolated from males for a period of time become less reluctant to mate. During the premating struggle, the antennae of males are used to grasp the females around the head, and the rear legs are used to lift the females' rear legs off the water surface. Neither antennae nor rear legs are used during copulation, thus they are not used for copulatory courtship. Mapping of these traits on the phylogeny indicates multiple independent origins and a pattern of escalation (16 origins, 7 losses). We conclude that these bizarre traits of males are sexually antagonistic and have evolved repeatedly in the genus.

Résumé

Les conflits sexuels peuvent favoriser le développement au cours de l'évolution de caractères sexuels antagonistes qui servent durant les interactions de l'accouplement. Un des cas les plus remarques de l'élaboration de caractères morphologiques chez le mâle s'observe chez les patineurs du genre Rheumatobates Bergroth (Hemiptera : Gerridae). La signification fonctionnelle des modifications bizarres des appendices dans ce groupe reste inconnue. Nous traitons ici principalement d'une des espèces les plus développés à ce titre, R. rileyi Bergroth. Des observations et des expériences nous servent à déterminer la séquence générale du comportement d'accouplement, le rôle des femelles dans l'issue des interactions sexuelles et la signification fonctionnelle des appendices fortement modifiés du mâle. Nous plaçons ces caractères sur un arbre phylétique reconnu du genre afin de déterminer leur patron d'évolution. Les mâles harcellent les femelles à répétition et les femelles réagissent en s'éloignant en patinant; cependant, si le mâle réussit à l'attraper, il se produit une échauffourée pré-copulatoire. La dynamique de l'échauffourée détermine le succès de la tentative d'accouplement. Les échauffourées courtes mènent normalement à l'accouplement, alors que les échauffourées prolongées se terminent généralement par la séparation du couple. Après une courte période de copulation, le mâle retire ses organes génitaux et débarque de la femelle. Les femelles qui ont été tenues à l'écart des mâles pendant un certain temps sont moins réticentes à l'accouplement. Durant l'échauffourée pré-copulatoire, les antennes des mâles servent à entourer la tête de la femelle et les pattes postérieures sont utilisées pour soulever les pattes postérieures de la femelles au-dessus de la surface de l'eau. Ni les antennes, ni les pattes postérieures ne servent durant la copulation; elles ne sont donc pas impliquées dans la cour associée à l'accouplement. En reliant ces caractéristiques à la phylogénie, on observe de multiples origines indépendantes et un pattern d'escalade (16 origines et 7 pertes). Nous concluons que ces caractères bizarres des mâles sont des caractères sexuels antagonistes et qu'ils sont apparus à plusieurs reprises chez ce genre.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 138 , Special Issue/Numéro spécial 4: Honouring Geoffrey G. E. Scudder/En hommage à Geoffrey G.E. Scudder , August 2006 , pp. 568 - 577
Copyright
Copyright © Entomological Society of Canada 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1

This paper is part of a special issue honouring Geoffrey G.E. Scudder for his significant contributions to entomology in Canada.

References

Andersen, N.M. 1982. The semiaquatic bugs (Hemiptera, Gerromorpha): phylogeny, adaptations, biogeography and classification. Entomonograph 3. Scandinavian Science Press, Klampenborg, Denmark.CrossRefGoogle Scholar
Andersen, N.M. 1997. A phylogenetic analysis of the evolution of sexual dimorphism and mating systems in water striders (Hemiptera: Gerridae). Biological Journal of the Linnean Society, 61: 345–368.CrossRefGoogle Scholar
Arnqvist, G. 1989. Sexual selection in a water strider: the function, mechanism of selection and heritability of a male grasping apparatus. Oikos, 56: 344–350.CrossRefGoogle Scholar
Arnqvist, G. 1992. Precopulatory fighting in a water strider: intersexual conflict or mate assessment? Animal Behaviour, 43: 559–567.CrossRefGoogle Scholar
Arnqvist, G. 1997. The evolution of water strider mating systems: causes and consequences of sexual conflicts. In The evolution of mating systems in insects and arachnids. Edited by Choe, J.C. and Crespi, B.J.. Cambridge University Press, Cambridge. pp. 146–163.CrossRefGoogle Scholar
Arnqvist, G., and Nilsson, T. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour, 60: 145–164.CrossRefGoogle ScholarPubMed
Arnqvist, G., and Rowe, L. 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proceedings of the Royal Society of London Series B: Biological Sciences, 261: 123–127.Google Scholar
Arnqvist, G., and Rowe, L. 2002. Antagonistic coevolution between the sexes in a group of insects. Nature (London), 415: 787–789.CrossRefGoogle Scholar
Arnqvist, G., and Rowe, L. 2005. Sexual conflict. Princeton University Press, Princeton, New Jersey.CrossRefGoogle Scholar
Bergsten, J., Toyra, A., and Nilsson, A.N. 2001. Intra-specific variation and intersexual correlation in secondary sexual characters of three diving beetles (Coleoptera: Dytiscidae). Biological Journal of the Linnean Society, 73: 221–232.CrossRefGoogle Scholar
Chapman, T., Arnqvist, G., Bangham, J., and Rowe, L. 2003. Sexual conflict. Trends in Ecology and Evolution, 18: 41–47.CrossRefGoogle Scholar
Eberhard, W.G. 1985. Sexual selection and animal genitalia. Harvard University Press, Cambridge, Massachusetts.CrossRefGoogle Scholar
Eberhard, W.G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, New Jersey.CrossRefGoogle Scholar
Gavrilets, S., Arnqvist, G., and Friberg, U. 2001. The evolution of female mate choice by sexual conflict. Proceedings of the Royal Society of London Series B: Biological Sciences, 268: 531–539.CrossRefGoogle ScholarPubMed
Holland, B., and Rice, W.R. 1998. Perspective: Chaseaway sexual selection: antagonistic seduction versus resistance. Evolution, 52: 1–7.Google ScholarPubMed
Hungerford, H.B. 1954. The genus Rheumatobates Bergroth (Hemiptera–Gerridae). University of Kansas Science Bulletin, 36: 529–588.Google Scholar
Koene, J.M., and Schulenburg, H. 2005. Shooting darts: coevolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology, 5: 25.CrossRefGoogle ScholarPubMed
Lauer, M.J. 1996. Effect of sperm depletion and starvation on female mating behavior in the water strider, Aquarius remigis. Behavioral Ecology and Sociobiology, 38: 89–96.CrossRefGoogle Scholar
Maddison, W.P., and Maddison, D.R. 1992. MacClade version 3: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Ortigosa, A., and Rowe, L. 2002. The effect of hunger on mating behaviour and sexual selection for large male size in Gerris buenoi. Animal Behaviour, 64: 369–375.CrossRefGoogle Scholar
Ortigosa, A., and Rowe, L. 2003. The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider. Animal Behaviour, 65: 851–858.CrossRefGoogle Scholar
Parker, G.A. 1979. Sexual selection and sexual conflict. In Sexual selection and reproductive competition in insects. Edited by Blum, M.S. and Blum, N.A.. Academic Press, New York. pp. 123–166.Google Scholar
Rowe, L. 1992. Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Animal Behaviour, 44: 189–202.CrossRefGoogle Scholar
Rowe, L. 1994. The costs of mating and mate choice in water striders. Animal Behaviour, 48: 1049–1056.CrossRefGoogle Scholar
Rowe, L., and Day, T. 2006. Detecting sexual conflict and sexually antagonistic coevolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 361: 277–285.CrossRefGoogle ScholarPubMed
Rowe, L., Arnqvist, G., Sih, A., and Krupa, J. 1994. Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends in Ecology and Evolution, 9: 289–293.CrossRefGoogle ScholarPubMed
Rowe, L., Cameron, E., and Day, T. 2005. Escalation and retreat during sexually antagonistic coevolution. American Naturalist, 165(S5): 5–18.CrossRefGoogle ScholarPubMed
Sakaluk, S.K., Bangert, P.J., Eggert, A.K., Gack, C., and Swanson, L.V. 1995. The gin trap as a device facilitating coercive mating in sagebrush crickets. Proceedings of the Royal Society of London Series B: Biological Sciences, 261: 65–71.Google Scholar
Silvey, J.K. 1931. Observations on the life-history of Rheumatobates rileyi. (Berg.) (Hemiptera: Gerridae). Papers from the Michigan Academy of Science, Arts and Letters, 13: 433–446.Google Scholar
Thornhill, R. 1984. Alternative hypotheses for traits believed to have evolved by sperm competition. In Sperm competition and the evolution of animal mating systems. Edited by Smith, R.L.. Academic Press, Orlando, Florida.Google Scholar
Vepsäläinen, K., and Savolainen, R. 1995. Operational sex ratios and mating conflict between the sexes in the water strider Gerris lacustris. American Naturalist, 146: 869–880.CrossRefGoogle Scholar
Weigensberg, I., and Fairbairn, D.J. 1994. Conflicts of interest between the sexes: a study of mating interactions in a semiaquatic bug. Animal Behaviour, 48: 893–901.CrossRefGoogle Scholar
Westlake, K.P. 1998. Sexual conflict and the evolution of male elaboration in the water strider genus Rheumatobates (Heteroptera: Gerridae). M.Sc. thesis, University of Toronto, Toronto, Ontario.Google Scholar
Westlake, K.P., and Rowe, L. 1999. Developmental costs of male sexual traits in the water strider Rheumatobates rileyi. Canadian Journal of Zoology, 77: 917–922.CrossRefGoogle Scholar
Westlake, K.P., Rowe, L., and Currie, D.C. 2000. Phylogeny of the water strider genus Rheumatobates (Heteroptera: Gerridae). Systematic Entomology, 25: 125–145.CrossRefGoogle Scholar
Wing, S., Lloyd, J.E., and Hongtrakul, T. 1983. Male competition in Pteroptyx fireflies: wing-cover clamps, female anatomy, and mating plugs. Florida Entomologist, 66: 86–91.CrossRefGoogle Scholar