Abstract
Asymmetric mating preferences occur in two closely related species, if females of one species are highly selective against males of the second, while females of the second show less selection against males of the first species. It has been suggested that such asymmetry is an indicator of common ancestry between the two species, but actual observations are contradictory and inconclusive. We developed a scenario of speciation history and asymmetric mating preference, incorporating invasion dynamicsvia frequency-dependent interspecific sexual competition. A newly isolated (derived) species may form at the periphery of the ancestral species’ distribution by invading a new range. Only a few closely related species would be expected in the new area, while many related species are expected to coexist with the ancestral species. In a peripherally derived species, female mating preferences should be relaxed through sexual character release, owing to a lack of sympatric species and a scarcity of intraspecific mating opportunities. Secondary contacts may then happen as: 1. repeated invasions, i.e. subsequent invasion by the ancestral species into the new range or, 2. backward invasions, i.e. derived species incursions into the ancestral range. Repeated invasions could lead to the coexistence of both the derived species and the newly invading ancestor. Backward invasions by the derived species can succeed only when the derived females develop a strict mating discrimination against the ancestral males. We then expect strong character displacement in the derived species. Thus, peripheral isolation and repeated invasions lead to the relaxed female mating preferences in the derived species and backward invasions lead to stronger female mating preferences in the derived species. This agrees withDrosophila data from Hawaii and the continents. Experimental data of theDrosophila arizonaemojavensis species cluster also support the hypothesis.
Similar content being viewed by others
References
Anderson, R. F. V. (1977) Ethological isolation and competition of allospecies in a secondary contact.American Naturalist 111: 939–949.
Barker, J. S. F. and W. T. Starmer (eds.) (1982)Ecological genetics and evolution: the cactus-yeast-Drosophila model system. Academic Press, New York.
Barton, N. H. and G. M. Hewitt (1989) Adaptation, speciation and hybrid zones.Nature 341: 497–503.
Bateman, A. J. (1948) Intra-sexual selection inDrosophila.Heredity 2: 349–368.
Bateson, P. (ed.) (1983)Mate choice. Cambridge Univ. Press, Cambridge, UK.
Brazner, J., V. Aberdeen and W. T. Starmer (1984) Host-plant shifts and adult survival in the cactus breedingDrosophila mojavensis.Ecological Entomology 9: 375–381.
Brown, W. L. and E. O. Wilson (1956) Character displacement.Systematic Zoology 5: 49–64.
Butlin, R. K. (1987a) Speciation by reinforcement.Trends in Ecology and Evolution 2: 8–13.
Butlin, R. K. (1987b) Species, speciation, and reinforcement.American Naturalist 130: 461–464.
Butlin, R. (1989) Reinforcement of premating isolation, pp. 158–179. In D. Otte and J. A. Endler (eds.)Speciation and its consequences. Sinauer, Sunderland, MA.
Carson, H. L. (1986) Sexual selection and speciation. pp. 391–409. In S. Karlin and E. Nevo (eds.)Evolutionary processes and theory. Academic Press, San Diego.
Carson, H. L. (1990) Evolutionary process as studied in population genetics: clues from phylogeny.Oxford Surveys in Evolutionary Biology 7: 129–156.
Colwell, R. K. (1985) Community biology and sexual selection: Lessons from hummingbird flower mites, pp. 406–424. In T. Case and J. M. Diamond (eds.)Ecological communities. Harper & Row, New York.
Colwell, R. K. (1986) Population structure and sexual selection for host fidelity in the speciation of hummingbird flower mites. pp. 475–493. In S. Karlin and E. Nevo (eds.)Evolutionary processes and theory. Academic Press, San Diego.
Coyne, J. A. and H.A. Orr (1989) Patterns of speciation inDrosophila.Evolution 43: 362–381.
Dobzhansky, T. (1940) Speciation as a stage of genetic divergence.American Naturalist 74: 312–321.
Dobzhansky, T. (1951)Genetics and the origin of species, 3rd edn. Columbia University Press, New York.
Eberhard, W. G. (1985)Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA.
Fellows, D. P. and W. B. Heed (1972) Factors affecting host plant selection in desert-adapted cactiphilicDrosophila.Ecology 53: 850–858.
Fisher, R. A. (1930)The genetical theory of natural selection. Oxford University Press (Reprint: 1958, Dover, New York).
Gastil, R. G., R. P. Phillips and E. C. Allison (1975) Reconnaissance geology of the state of Baja California.The Geological Society of America, Inc. Memoir 140: 139–143.
Giddings, L. V., K. Y. Kaneshiro and W. W. Anderson (eds.) (1989)Genetics, speciation and the founder principle. Oxford University Press, New York.
Grant, P. R. (1986)Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton.
Grimaldi, D. A. (1987) Phylogenetics and taxonomy ofZygothrica (Diptera: Drosophilidae).Bulletin of the American Museum of Natural History 186: 103–268.
Harrison, R. G. (1990) Hybrid zones: windows on evolutionary process.Oxford Surveys in Evolutionary Biology 7: 69–128.
Harvey, P. H. and S. J. Arnold (1982) Female mate choice and runaway sexual selection.Nature 297: 533–534.
Heed, W. B. (1978) Ecology and genetics of Sonoran desertDrosophila. pp. 109–126. In P. F. Brussard (ed.)Ecological genetics: the interface Springer-Verlag, New York.
Hoy, R. R., A. Hoikkala and K. Kaneshiro (1988) Hawaiian courtship songs: evolutionary innovation in communication signals ofDrosophila.Science 240: 217–219.
Hutchinson, G. E. (1978)An introduction to population ecology. Yale University Press, New Haven.
Imanishi, K. (1949)The logic of biological society. Mainichishinbun (Reprint: 1971, Shisakusha, Tokyo), (in Japanese)
Kaneshiro, K. Y. (1976) Ethological isolation and phylogeny in the plantibia subgroup of HawaiianDrosophila.Evolution 30: 740–745.
Kaneshiro, K. Y. (1983) Sexual selection and direction of evolution in the biosystematics of Hawaiian Drosophilidae.Annual Review of Entomology 28: 161–178.
Kaneshiro, K. Y. (1987a) Speciation via sexual selection versus adaptive evolution in HawaiianDrosophila.Insect Science and Application 8: 447–452.
Kaneshiro, K. Y. (1987b) The dynamics of sexual selection and its pleiotropic effects.Behavior Genetics 17: 559–569.
Kaneshiro, K. Y. (1988) Speciation in the HawaiiwanDrosophila.BioScience 38: 258–263.
Kaneshiro, K. Y. (1989) The dynamics of sexual selection and founder effects in species formation, pp. 279–296. In L. V. Giddings, K. Y. Kaneshiro and W. W. Anderson (eds.)Genetics, speciation, and the founder principle. Oxford University Press, New York.
Kaneshiro, K. Y. and C. R. B. Boake (1987) Sexual selection and speciation: issues raised by HawaiianDrosophila.Trends in Ecology and Evolution 2: 207–212.
Kani, T. (1944)Ecology of stream living insects. Kenkyusha, Tokyo. (in Japanese)
Koepfer, H. R. (1987a) Selection for sexual isolation between geographic forms ofDrosophila mojavensis. I. Interactions between the selected forms.Evolution 41: 37–48.
Koepfer, H. R. (1987b) Selection for sexual isolation between geographic forms ofDrosophila mojavensis. II. Effects of selection of mating preference and propensity.Evolution 41: 1409–1413.
Kubota, K. (1991) Natural hybridization betweenLeptocarabus (L.)procerulus andL. (L.)kumagaii (Coleoptera, Carabidae).Japanese Journal of Entomology 59: 323–329.
Kuno, E. (1992) Competitive exclusion through reproductive interference.Researches on Population Ecology 34: 275–284.
Lack, D. (1961)Darwin’s finches, 2nd edn. Cambridge University Press, Cambridge, UK.
Lack, D. (1971)Ecological isolation in birds. Blackwell, Oxford, UK.
Lambert, D. M. (1984) Species-mate recognition systems, phylogenies and asymmetrical evolution.Journal of theoretical Biology 109: 147–156.
Lorenz, K. Z. (1981)The foundations of ethology. Simon and Schuster, New York.
MacArthur, R. H. and E. O. Wilson (1967)The theory of island biogeography. Princeton University Press, Princeton.
Mallet, J. and N. H. Barton (1989) Strong natural selection in a warning-color hybrid zone.Evolution 43: 421–431.
Malogolowkin-Cohen, C., A. S. Simmons and H. Levene (1965) A study of sexual isolation between certain strains ofDrosophila paulistorum.Evolution 29: 368–369.
Mangan, R. L. (1978) Comparative interactions among host plant specificDrosophila species. Ph. D. Thesis, University of Arizona, Tuscon.
Markow, T. A. (1981) Mating preferences are not predictive of the direction of evolution in experimental populations ofDrosophila.Science 213: 1405–1407.
Mayr, E. (1963)Animal species and evolution. Harvard University Press, Cambridge, MA.
Mettler, L. E. (1963)Drosophila mojavensis baja, a new form in themulleri complex.Drosophila Information Service 38: 57–58.
Montague, J. R. and K. Y. Kaneshiro (1982) Flower-breeding species of Hawaiian Drosophilids in an early stage of sympatry.Pacific Insects 24: 209–213.
Ohta, A. T. (1978) Ethological isolation and phylogeny in the Grimshawi species complex of HawaiianDrosophila.Evolution 32: 485–492.
Otte, D. and J. A. Endler (eds.) (1989)Speciation and its consequences. Sinauer, Sunderland, MA.
Paterson, H. E. H. (1978) More evidence against speciation by reinforcement.South African Journal of Science 74: 369–371.
Paterson, H.E. H. (1993)Evolution and the recognition concept of species: collected writings. Johns Hopkins University Press, Baltimore.
Ribeiro, J. M. C. and A. Spielman (1986) The satyr effect: a model predicting parapatry and species extinction.American Naturalist 128: 513–528.
Ringo, J. M. (1977) Why 300 species of HawaiianDrosophila? The sexual selection hypothesis.Evolution 31: 694–696.
Ritchie, M. G., R. K. Butlin and G. M. Hewitt (1989) Assortative mating across a hybrid zone inChorthippusparallelus (Orthoptera: Acrididae).Journal of Evolutionary Biology 2: 339–352.
Robinson, B. W. and D. S. Wilson (1994) Character release and displacement in fishes: a neglected literature.American Naturalist 144: 596–627.
Robinson, B. W., D. S. Wilson, A. S. Margosian and P. T. Lotito (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish.Evolutionary Ecology 7: 451–464.
Ruiz, A., W. B. Heed and M. Wasserman (1990) Evolution of themojavensis cluster of cactophilicDrosophila with descriptions of two new species.Journal of Heredity 81: 30–42.
Schluter, D. (1988) Character displacement and the adaptive divergence of finches on islands and continents.American Naturalist 131: 799–824.
Slatkin, M. (1980) Ecological character displacement.Ecology 61: 163–177.
Slobodkin, L.B. (1961)Growth and regulation of animal populations. Holt, Rinehart and Winston, New York.
Spencer, H. G., B. H. McArdle and D.M. Lambert (1986) A theoretical investigation of speciation by reinforcement.American Naturalist 128: 241–262.
Starmer, W. T. (1981) A comparison ofDrosophila habitats according to the physiological attributes of the associated yeast communities.Evolution 35: 38–52.
Starmer, W. T. and J. C. Fogleman (1986) Coadaptation ofDrosophila and yeasts in their natural habitat.Journal of Chemical Ecology 12: 1037–1055.
Templeton, A. R. (1979) Once again, why 300 species of HawaiianDrosophilal Evolution 33: 513–517.
Templeton, A. R. (1981) Mechanisms of speciation-a population genetic approach.Annual Review of Ecology and Systematics 12: 23–48.
Thornhill, R. and J. Alcock (1983)The evolution of insect mating systems. Harvard University Press, Cambridge, MA.
Tilman, D. (1982)Resource competition and community structure. Princeton University Press, Princeton.
Tinbergen, N. (1951)The study of instinct. Oxford University Press, Cambridge, UK.
Wasserman, M. (1982) Evolution of therepleta group, pp. 61–139. In M. Ashburner, H. L. Carson, and J. N. Thompson, Jr. (eds.)The genetics and biology of Drosophila, Vol. 3b. Academic Press, New York.
Wasserman, M. and H. R. Koepfer (1977) Character displacement for sexual isolation betweenDrosophila mojavensis andDrosophila arizonensis.Evolution 31: 812–823.
Wasserman, M. and H. R. Koepfer (1980) Does asymmetrical mating preference show the direction of evolution?Evolution 34: 1116–1124.
Watanabe, T. K. and M. Kawanishi (1979) Mating preference and the direction of evolution inDrosophila.Science 205: 906–907.
Wilson, D. S. (1989) The diversification of single gene pools by densityand frequency-dependent selection, pp. 366–385. In D. Otte and J. A. Endler (eds.)Speciation and its consequences. Sinauer, Sunderland, MA.
Yoshimura, J. (1992) By-product runaway evolution by adaptive mate choice: a behavioural aspect of sexual selection.Evolutionary Ecology 6: 261–269.
Yoshimura, J. and C. W. Clark (1994) Population dynamics of sexual and resource competition.Theoretical Population Biology 45: 121–131.
Zahavi, A. (1975) Mate selection — a selection for a handicap.Journal of theoretical Biology 53: 205–214.
Zouros, E. and C. J. d’Entremont (1980) Sexual isolation among populations ofDrosophila mojavensis: response to pressure from a related species.Evolution 34: 421–430.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yoshimura, J., Starmer, W.T. Speciation and evolutionary dynamics of asymmetric mating preference. Res Popul Ecol 39, 191–200 (1997). https://doi.org/10.1007/BF02765265
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02765265