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The evolution of hybrid infertility: Perpetual coevolution between gender-specific and sexually antagonistic genes

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Genetics of Mate Choice: From Sexual Selection to Sexual Isolation

Part of the book series: Contemporary Issues in Genetics and Evolution ((CIGE,volume 9))

Abstract

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a ‘gender-load’ in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.

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References

  • Alvesalo, L., 1997. Sex chromosomes and human growth-a dental approach. Hum. Genet. 101: 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Arnqvist, G. & L. Rowe, 1995. Sexual conflict and arms races between the sexes-a morphological adaptation for control of mating in a female insect. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 261: 123–127.

    Article  Google Scholar 

  • Bull, J.J., 1983. Evolution of Sex Determination Systems. Benjamin Cummings, Menlo Park, California.

    Google Scholar 

  • Chapman, T., F. Lindsay, F. Liddle, J.M. Kalb, M.F. Wolfner & L. Partridge, 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241–244.

    Article  PubMed  CAS  Google Scholar 

  • Chen, P.S., 1996. The accessory gland proteins in male Drosophila: structural, reproductive, and evolutionary aspects. Experientia 52:503–510.

    Article  PubMed  CAS  Google Scholar 

  • Chippindale, A.K., J.R. Gibson & W.R. Rice, 2001. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl. Acad. Sci. USA 98: 1671–1675.

    Article  PubMed  CAS  Google Scholar 

  • Chippindale, A.K. & W.R. Rice, 2001. Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 5677–5682.

    Article  PubMed  CAS  Google Scholar 

  • Civetta, A. & R.S. Singh, 1995. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J. Mol. Evol. 41: 1085–1095.

    Article  PubMed  CAS  Google Scholar 

  • Clark, A.G., 1987. Variation in Y-chromosome segregation in natural-populations of Drosophila melanogaster. Genetics 115: 143–151.

    PubMed  CAS  Google Scholar 

  • Clark, A.G. & E.M.S. Lyckegaard, 1990. 2 neutrality tests of Y-linked rDNA variation in Drosophila melanogaster. Evolution 44:2106–2112.

    Article  Google Scholar 

  • Eberhard, W.G., 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, Princeton.

    Google Scholar 

  • Endler, J.A., 1980. Natural selection on color patterns in Poecilia reticulata. Evolution 34: 76–91.

    Article  Google Scholar 

  • Forsman, A., 1995. Opposing fitness consequences of color pattern in male and female snakes. J. Evol. Biol. 8: 53–70.

    Article  Google Scholar 

  • Haig, D., 1993. Genetic conflicts in human pregnancy. Quart. Rev. Biol. 68:495–531.

    Article  PubMed  CAS  Google Scholar 

  • Haig, D. & C. Graham, 1991. Genomic imprinting and the strange case of the insulin-like growth factor-ii receptor. Cell 64: 1045–1046.

    Article  PubMed  CAS  Google Scholar 

  • Hurst, L.D., 1992. Intragenomic conflict as an evolutionary force. Proc. R. Soc. Lond. B 247: 189–194.

    Article  Google Scholar 

  • Howard, D.J., M. Reece, P.G. Gregory, J. Chu & M.L. Caim, 1998. The evolution of barriers to fertilization between closely related organisms, pp. 279–290 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, Oxford.

    Google Scholar 

  • Jiang, M., J. Ryu, M. Kiraly, K. Duke, V. Reinke & S.K. Kim, 2001. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98: 218–223.

    Article  PubMed  CAS  Google Scholar 

  • Jin, W., R.M. Riley, R.D. Wolfinger, K.P. White, G. Passador-Gurgel & G. Gibson, 2001. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet. 29: 389–395.

    Article  PubMed  CAS  Google Scholar 

  • Kohorn, L.U., 1994. Shoot morphology and reproduction in jojoba: advantages of sexual reproduction. Ecology 75: 2384–2394.

    Article  Google Scholar 

  • Lindsley, D.L. & E.H. Grell, 1968. Genetic Variations of Drosophila melanogaster. Carnegie Institute of Washington, Washington D.C.

    Google Scholar 

  • Maynard Smith, J., 1978. The Evolution of Sex. Cambridge University Press, New York.

    Google Scholar 

  • Meagher, T.R., 1992. The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae). 1. Genetic variation. Evolution 46: 445–457.

    Article  Google Scholar 

  • Orgad, S.G., Rosenfeld, R.J. Greenspan & D. Segal, 2000. Court-less, the Drosophila UBC7 homolog, is involved in male courtship behavior and spermatogenesis. Genetics 155: 1267–1280.

    PubMed  CAS  Google Scholar 

  • Ostrer, H., 2001. Genome and hormones: gender differences in physiology-invited review: sex-based differences in gene expression. J. Appl. Physiol. 91: 2384–2388.

    PubMed  CAS  Google Scholar 

  • Palumbi, S.R., 1998. Speciation and the evolution of gamete recognition loci, pp. 271–278 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, Oxford.

    Google Scholar 

  • Parker, G.A., 1979. Sexual selection and sexual conflict, pp. 123–166 in Sexual Selection and Reproductive Competition in Insects, edited by M.S. Blum & N.A. Blum. Academic Press, New York.

    Google Scholar 

  • Parker, G.A. & L. Partridge, 1998. Sexual conflict and speciation. Phil. Trans. R. Soc. Lond. Ser.-B Biol. Sci. 353: 261–274.

    Article  CAS  Google Scholar 

  • Partridge, L., K. Fowler, S. Trevitt & W. Sharp, 1986. An examination of the effects of males on the survival and egg-production rates of female Drosophila-melanogaster. J. Insect Physiol. 32: 925–929.

    Article  Google Scholar 

  • Pitnick, S. & G.T. Miller, 2000. Correlated response in reproductive and life history traits to selection on testis length in Drosophila hydei. Heredity 84: 416–426.

    Article  PubMed  Google Scholar 

  • Rice, W.R., 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735–742.

    Article  Google Scholar 

  • Rice, W.R., 1986. On the instability of polygenic sex determination: the effect of sex-specific selection. Evolution 40: 633–639.

    Article  Google Scholar 

  • Rice, W.R., 1987. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41: 911–914.

    Article  Google Scholar 

  • Rice, W.R., 1992. Sexually antagonistic genes: experimental evidence. Science 256: 1436–1439.

    Article  PubMed  CAS  Google Scholar 

  • Rice, W.R., 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 361: 232–234.

    Article  Google Scholar 

  • Rice, W.R., 1998a. Intergenomic conflict, interlocus antagonistic coevolution, and the evolution of reproductive isolation, pp. 261–270 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, Oxford.

    Google Scholar 

  • Rice, W.R., 1998b. Male fitness increases when females eliminated from gene pool: implications for the Y chromosome. Proc. Natl. Acad. Sci. USA 95: 6217–6221.

    Article  PubMed  CAS  Google Scholar 

  • Rice, W.R. & B. Holland, 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41: 1–10.

    Article  Google Scholar 

  • Rice, W.R. & A.K. Chippindale, 2001. Intersexual ontogenetic conflict. J. Evol. Biol. 14: 685–693.

    Article  Google Scholar 

  • Rinchik, E.M., D.A. Carpenter & M.A. Handel, 1995. Pleiotropy in microdeletion syndromes-neurologic and spermatogenic abnormalities in mice homozygous for the P(6H) deletion are likely due to dysfunction of a single-gene. Proc. Natl. Acad. Sci. USA 92: 6394–6398.

    Article  PubMed  CAS  Google Scholar 

  • Roldan, E.R.S. & M. Gomendio, 1999. The Y chromosome as a battleground for sexual selection. Trends Ecol. Evol. 14: 58–62.

    Article  PubMed  Google Scholar 

  • Sasaki, A. & G. de Jong, 1999. Density dependence and unpredictable selection in a heterogeneous environment: compromise and polymorphism in the ESS reaction norm Evolution 53: 1329–1342.

    Article  Google Scholar 

  • Schoener, T.W., J.B. Slade & C.H. Stinson, 1982. Diet and sexual dimorphism in the very catholic lizard genus, Leiocephalus of the Bahamas. Oecologia 53: 160–169.

    Article  Google Scholar 

  • Sherman, P.W., 1977. Nepotism and evolution of alarm calls. Science 197: 1246–1253.

    Article  PubMed  CAS  Google Scholar 

  • Singh, R.S. & R.J. Kulathinal, 2000. Sex gene pool evolution and speciation: a new paradigm Genes. Genet. Syst. 75: 119–130.

    Article  CAS  Google Scholar 

  • Slatkin, M. & J. Maynard Smith, 1979. Models of coevolution. Quart. Rev. Biol. 54: 233–263.

    Article  Google Scholar 

  • Stenseth, N.C. & J. Maynard Smith, 1984. Coevolution in ecosystems-red queen evolution or stasis. Evolution 38: 870–880.

    Article  Google Scholar 

  • Swanson, W.J., A.G. Clark, H.M. Waldrip-Dail, M.F. Wolfner & C.F. Aquadro, 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl. Acad. Sci. USA 98: 7375–7379.

    Article  PubMed  CAS  Google Scholar 

  • Toro, M.A. & B. Charlesworth, 1982. An attempt to detect genetic-variation in sex-ratio in Drosophila melanogaster. Heredity 49: 199–209.

    Article  Google Scholar 

  • Trivers, R.L., 1974. Parent-offspring conflict. Am. Zool. 14: 249–264.

    Google Scholar 

  • True, J.R., B.S. Weir & C.V.C. Laurie, 1996. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142: 819–837.

    PubMed  CAS  Google Scholar 

  • Vacquier, V.D., 1998. Evolution of gamete recognition proteins. Science 28: 1995–1998.

    Article  Google Scholar 

  • Van Valen, L., 1973. A new evolutionary law. Evol. Theory 1: 1–30.

    Google Scholar 

  • West-Eberhard, M., 1983. Sexual selection, social competition and speciation. Quart. Rev. Biol. 58: 155–183.

    Article  Google Scholar 

  • Wolfner, M.F., 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products Insect. Biochem. Mol. 27: 179–192.

    CAS  Google Scholar 

  • Wu, C.-I. & A.W. Davis, 1993. Evolution of postmating reproductive isolation-the composite nature of Haldane rule and its genetic bases. Am. Nat. 142: 187–212.

    Article  PubMed  CAS  Google Scholar 

  • Wu, C.-I. & M.F. Palopoli, 1994. Genetics of postmating reproductive isolation in animals. Ann. Rev. Genet. 28: 283–308.

    Article  PubMed  CAS  Google Scholar 

  • Wyckoff, G.J., W. Wang & C.-I. Wu, 2000. Rapid evolution of male reproductive genes in the descent of man. Nature 403: 304–309.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, 931060, USA

    William R. Rice

  2. Department of Biology, Queen’s University, Kingston, ON, K7L 3N6, Canada

    Adam K. Chippindale

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  1. William R. Rice
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  2. Adam K. Chippindale
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W. J. Etges M. A. F. Noor

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© 2002 Springer Science+Business Media Dordrecht

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Rice, W.R., Chippindale, A.K. (2002). The evolution of hybrid infertility: Perpetual coevolution between gender-specific and sexually antagonistic genes. In: Etges, W.J., Noor, M.A.F. (eds) Genetics of Mate Choice: From Sexual Selection to Sexual Isolation. Contemporary Issues in Genetics and Evolution, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0265-3_3

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  • DOI: https://doi.org/10.1007/978-94-010-0265-3_3

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3958-1

  • Online ISBN: 978-94-010-0265-3

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