Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-21T00:01:11.824Z Has data issue: false hasContentIssue false

Sexual morphology of male Sepsis cynipsea (Diptera: Sepsidae): lack of support for lock-and-key and sexually antagonistic morphological coevolution hypotheses

Published online by Cambridge University Press:  02 April 2012

William G. Eberhard
Affiliation:
Smithsonian Tropical Research Institute and Escuela de Biologia, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica (e-mail: archisepsis@biologia.ucr.ac.cr)

Abstract

Traits that function in male–female sexual interactions tend to diverge rapidly compared with other traits. Several hypotheses attempt to explain this evolutionary pattern. Predictions of two of these hypotheses, lock-and-key and sexually antagonistic morphological co-evolution, were tested by examining how two sets of species-specific male structures fit with female structures during courtship and copulation in the fly Sepsis cynipsea (L., 1758). Contrary to predictions of both hypotheses, neither the species-specific modifications of the male's front legs nor those of his genitalic surstyli were matched by modifications of the female structures with which they meshed (wing bases, 6th abdominal sternite); males damaged small patches of microtrichia on the female's wings with their legs, but the morphology of the female's wings and abdomen showed no sign of the defensive designs expected under antagonistic morphological co-evolution. Data regarding the alternative hypothesis of sexually antagonistic behavioral co-evolution by females in response to male morphology were less conclusive, but this hypothesis failed to explain the sustained, apparently stimulatory rhythmic squeezing by the male genitalia and the lack of female defensive responses to this squeezing. These movements of the male surstyli during copulation suggest that they function to stimulate the female. The wing base of the female has apparent sense organs near the sites contacted by the male, as expected under the alternative hypothesis of traditional female choice to explain rapid divergent evolution. The male's genitalic surstyli were also used in novel precopulatory interactions. A pair of previously undescribed processes at the bases of the surstyli probably grasp and may also rhythmically squeeze the female during copulation.

Résumé

Les caractères impliqués dans les interactions sexuelles entre les mâles et les femelles ont tendance à diverger plus rapidement que les autres caractères. Plusieurs hypothèses cherchent à expliquer ce patron évolutif. L'examen de l'appariement de deux appareils mâles spécifiques aux structures femelles durant la cour et l'accouplement chez la mouche Sepsis cynipsea (L., 1758) a permis de vérifier les prédictions de deux de ces hypothèses, celle de la serrure et de la clé et celle de la coévolution morphologique sexuelle antagoniste. Contrairement aux prédictions des deux hypothèses, les femelles ne possèdent pas de modifications des structures (bases des ailes, 6e sternite abdominal) qui sont en interaction avec les modifications spécifiques des pattes antérieures des mâles, ni avec celles de leurs surstyles génitaux. Les mâles endommagent de petites plages de microtriches sur les ailes des femelles avec leurs pattes; la morphologie de la femelle ne montre, cependant, aucune signe des adaptations de l'aile et de l'abdomen prévues par la coévolution morphologique antagoniste. Les données concernant l'hypothèse de rechange de la coévolution du comportement sexuel antagoniste chez la femelle en réaction à la morphologie du mâle sont encore moins claires; l'hypothèse ne réussit pas à expliquer la compression rythmique soutenue, apparemment stimulatrice, exercée par les génitalias mâles et l'absence de réactions de défense de la part de la femelle à cette compression. Les mouvements des surstyles mâles durant l'accouplement laissent croire qu'ils servent à stimuler la femelle. La base de l'aile de la femelle possède, semble-t-il, des organes sensoriels près des surfaces palpées par le mâle, tel que prévu par l'hypothèse de rechange traditionnelle du choix de la femelle pour expliquer l'évolution divergente rapide. Les surstyles génitaux du mâle servent aussi à des interactions précopulatrices inédites : une paire de processus, encore non décrits, à la base retiennent probablement la femelle et la compriment aussi sans doute rythmiquement durant la copulation.

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2005

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.)

References

Alexander, R.D., Marshall, D.C., and Cooley, J.R. 1997. Evolutionary perspectives on insect mating. In Mating systems in insects and arachnids. Edited by Choe, J. and Crespie, B.. Cambridge University Press, Cambridge. pp. 431.Google Scholar
Allen, G.R., and Simmons, L.W. 1996. Coercive mating, fluctuating asymmetry and male mating success in the dung fly Sepsis cynipsea. Animal Behaviour, 52: 737741.Google Scholar
Blanckenhorn, W.U. 1999. Different growth responses to temperature and resource limitation in three fly species with similar life histories. Evolutionary Ecology, 13: 395409.Google Scholar
Blanckenhorn, W.U., Muhlhauser, C., Morf, C., Reusch, T., and Reuter, M. 2000. Female choice, female reluctance to mate and sexual selection on body size in the dung fly Sepsis cynipsea. Ethology, 106: 577593.Google Scholar
Blanckenhorn, W.U., Hosken, D.J., Martin, O.Y., Reim, C., Teuschl, Y., and Ward, P.I. 2002. The costs of mating in the dung fly Sepsis cynipsea. I. Costs of copulation. Behavioral Ecology, 13: 353358.Google Scholar
Chapman, T., Arnqvist, G., Bangham, J., and Rowe, L. 2003. Sexual conflict. Trends in Ecology and Evolution, 18: 4147.Google Scholar
Cordero, C., and Eberhard, W.G. 2005. Interaction between sexually antagonistic selection and mate choice in the evolution of female responses to male traits. Evolutionary Ecology, 19: 111122.Google Scholar
Ding, A., and Blanckenhorn, W.U. 2002. The effects of sexual size dirmorphism on mating behaviour in two dung flies with contrasting dimorphism. Evolutionary and Ecological Research, 4: 259273.Google Scholar
Duda, O. 1925. Monographie der Sepsiden (Dipt.). I. Annalen des Naturhistorischen Museums in Wien, 39: 1153.Google Scholar
Duda, O. 1926. Monographie der Sepsiden (Dipt.). II. Annalen des Naturhistorischen Museums in Wien, 40: 1110.Google Scholar
Eberhard, W.G. 1985. Sexual selection and animal genitalia. Harvard University Press, Cambridge, Massachusetts.Google Scholar
Eberhard, W.G. 2001 a. The functional morphology of species-specific structures on the front legs of male Archisepsis and Palaeosepsis flies (Diptera, Sepsidae). Zoological Journal of the Linnean Society, 133: 335368.Google Scholar
Eberhard, W.G. 2001 b. Species-specific genitalic copulatory courtship in sepsid flies (Diptera, Sepsidae, Microsepsis) and theories of genitalic evolution. Evolution, 55: 93102.Google Scholar
Eberhard, W.G. 2001 c. Courtship before and during copulation, and multi-stage transfer of material to the female's wings in Microsepsis armillata (Diptea: Sepsidae). Journal of the Kansas Entomological Society, 74: 7078.Google Scholar
Eberhard, W.G. 2001 d. Multiple origins of a major novelty: moveable abdominal lobes in male sepsid flies (Diptera: Sepsidae), and the question of developmental constraints. Evolutionary Development, 3: 206222.Google Scholar
Eberhard, W.G. 2002 a. The relation between aggressive and sexual behavior and allometry in Palaeosepsis dentatiformis. Flies (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 75: 317332.Google Scholar
Eberhard, W.G. 2002 b. Physical restraint or stimulation? The function(s) of the modified front legs of male Archisepsis diversiformis (Diptera, Sepsidae). Journal of Insect Behavior, 15: 831850.Google Scholar
Eberhard, W.G. 2002 c. Female resistance or screening? Male force vs. selective female collaboration in intromission in sepsid flies and other insects. Revista de Biología Tropical, 50: 485505.Google Scholar
Eberhard, W.G. 2003. Sexual behavior and morphology of Themira minor (Diptera: Sepsidae) males and the evolution of male sternal lobes and genitalic surstyli. The Canadian Entomologist, 135: 569581.Google Scholar
Eberhard, W.G. 2004. Rapid divergent evolution of sexual morphology: comparative tests of sexually antagonistic coevolution and traditional female choice. Evolution, 58: 19471970.Google Scholar
Eberhard, W.G., and Huber, B.A. 1998. Copulation and sperm transfer in Archisepsis flies (Diptera: Sepsidae) and the evolution of their intromittent genitalia. Studia Dipterologica, 5: 217248.Google Scholar
Eberhard, W.G., and Pereira, F. 1996. Functional morphology of male genitalic surstyli in the dungflies Archisepsis diversiformis and A. ecalcarata (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 69(Suppl. 4): 4360.Google Scholar
Holland, B., and Rice, W.R. 1998. Chase-away selection: antagonistic seduction vs. resistance. Evolution, 52: 17.Google Scholar
Martin, O.Y., and Hosken, D.J. 2002. Strategic ejaculation in the common dung fly Sepsis cynipsea. Animal Behaviour, 63: 541546.Google Scholar
Martin, O.Y., and Hosken, D.J. 2003. The evolution of reproductive isolation through sexual conflict. Nature (London), 423: 979982.Google Scholar
Martin, O.Y., Leugger, R.R., Zeltner, N., and Hosken, D.J. 2003. Male age, mating probability and mating costs in the fly Sepsis cynipsea. Evolutionary Ecological Research, 5: 119129.Google Scholar
Meier, R. 1993. Cladistic analysis of the Sepsidae (Cyclorrhapha: Diptera) based on a comparative scanning electron microscope study of larvae. Systematic Entomology, 20: 99128.Google Scholar
Ozerov, A.L. 1992. New data on the neotropical sepsids (Diptera, Sepsidae). Russian Entomology Journal, 1: 8186.Google Scholar
Ozerov, A.L. 1993. Six new species of the genus Palaeosepsis Duda (Diptera Sepsidae). Russian Entomology Journal, 2: 6371.Google Scholar
Ozerov, A.L. 1998. A review of the genus Themira Robineau-Desvoidy, 1830 (Diptera: Sepsidae) of the world, with a revision of the North American species. Russian Entomology Journal, 7: 169208.Google Scholar
Parker, G.A. 1972 a. Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae). I. Preliminary analysis of the reproductive strategy and its associated behaviour patterns. Behaviour, 41: 172206.Google Scholar
Parker, G.A. 1972 b. Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae). II. The significance of the precopulatory passive phase and emigration. Behaviour, 41: 241250.Google Scholar
Pont, A. 1979. Sepsidae. Handbook for the Identification of British Insects, 10(5): 135.Google Scholar
Shapiro, A., and Porter, A. 1989. The lock-and-key hypothesis: evolutionary and biosystematic interpretation of insect genitalia. Annual Review of Entomology, 34: 231245.Google Scholar
Silva, V.C. 1993. Revisão da familia Sepsidae na região neotropical. III. Os géneros Palaeosepsis Duda, 1926, Archisepsis gen. n. e Microsepsis gen. n.; chave para os géneos neotropicais (Diptera, Schizophora). Ihringia, Serie Zoológica, Porto Alegre, 75: 117170.Google Scholar
Steyskal, G. 1987. Sepsidae. In Manual of Nearctic Diptera. Vol. 2. Edited by McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, J.J., Vockeroth, J.R., and Wood, D.M.. Research Branch Monograph 28, Canada Department of Agriculture, Ottawa, Ontario. pp. 945950.Google Scholar
Šulc, K. 1927. Biologicky vyznam vyzbroje prednich samcich nohou u sepsid (Muscidae). Biologické Spisy Vysoké Školy Zvěrolékařské, Brno, 7: 181194.Google Scholar
Ward, P.I. 1983. The effects of size on the mating behaviour of the dung fly Sepsis cynipsea. Behavioral Ecology and Sociobiology, 13: 7580.Google Scholar
Ward, P.I., Hemmi, J., and Röösli, T. 1992. Sexual conflict in the dung fly Sepsis cynipsea. Functional Ecology, 6: 649653.Google Scholar