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Sexual Selection and Mate Choice: Insights from Neutralist Perspectives

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Darwin’s concept of sexual selection has been an area of intense research interest for the past half-century. Research has mainly focused on intersexual selection (selection arising from mate choice), and has particularly focused on the hypothesis that mates are chosen on the basis of “genetic quality” which is “honestly” signaled by sexually dimorphic traits. I discuss these models in the light of evidence that most genetic variation in real populations is either selectively neutral or slightly deleterious. Since several well-known models have focused on the immune system as a source of heritable variation in fitness, I examine evidence from studies of the vertebrate major histocompatibility complex and its interaction with pathogens. Finally, I discuss alternative hypotheses for the evolution of secondary sexual characteristics that are consistent with the prevalence of purifying selection rather than positive selection in most populations. One such model, the random walk model, relies only on the well-attested processes of mutation, purifying selection, and genetic drift, thereby providing an attractive alternative to models that assume ubiquitous positive selection.

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References

  • Agrawal, A. F. (2001). Sexual selection and the maintenance of sexual reproduction. Nature, 411, 692–695.

    Article  CAS  PubMed  Google Scholar 

  • Andersson, M. (1994). Sexual selection. Princeton: Princeton University Press.

    Google Scholar 

  • Arnqvist, G. (1998). Comparative evidence for the evolution of genitalia by sexual selection. Nature, 393, 784–786.

    Article  CAS  Google Scholar 

  • Arnqvist, G., & Thornhill, R. (1998). Evolution of animal genitalia: Patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in water strider (Heteroptera: Gerridae: Insecta). Genetical Research, 71, 193–212.

    Article  Google Scholar 

  • Baker, T. C. (2002). Mechanism for saltational shifts in pheromone communication systems. Proceedings of the National Academy of Sciences of the United States of America, 99, 13368–13370.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Borgia, G. (1979). Sexual selection and the evolution of mating systems. In M. S. Blum & N. A. Blum (Eds.), Sexual selection and reproductive systems in insects (pp. 19–80). New York: Academic Press.

    Google Scholar 

  • Carrington, M., Nelson, G. W., Martin, M. P., Kissner, T., Vlahov, D., Goedert, J. J., et al. (1999). HLA and HIV-1: Heterozygote advantage and B*35-Cw*04 disadvantage. Science, 283, 1748–1752.

    Article  CAS  PubMed  Google Scholar 

  • Chenoweth, S. F., & McGuigan, K. (2010). The genetic basis of sexually selected variation. Annual Review of Ecology Evolution and Systematics, 41, 81–101.

    Article  Google Scholar 

  • Collins, S. (2004). Vocal fighting and flirting; the functions of birdsong. In P. Marler & H. Slabbekoorn (Eds.), Nature’s music: The science of birdsong (pp. 225–233). SanDiego: Elsevier Academic Press.

    Google Scholar 

  • Darwin, C. (1871). The descent of man, and selection in relation to sex. London: John Murray.

    Book  Google Scholar 

  • Eberhard, W. G. (1985). Sexual selection and animal genitalia. Cambridge (MA): Harvard University Press.

    Book  Google Scholar 

  • Eshel, I., & Hamilton, W. D. (1984). Parent-offspring correlation in fitness under fluctuating selection. Proceedings of the Royal Society of London Series B: Biological Sciences, 222, 1–14.

    Article  Google Scholar 

  • Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Frankham, R. (1995). Effective population size/adult population size ratios in wildlife: A review. Genetical Research, 66, 95–107.

    Article  Google Scholar 

  • Friedrich, T. T., Dodds, E. J., Yant, L. J., Vojnov, L., Rudersdorf, R., Cullen, C., et al. (2004). Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nature Medicine, 10, 275–281.

    Article  CAS  PubMed  Google Scholar 

  • Fu, W., O’Connor, T. D., Jun, G., Kang, H. M., Abecasis, G., Leal, S. M., et al. (2012). Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants. Nature, 493, 216–220.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fuller, R. C., Houle, D., & Travis, J. (2005). Sensory bias as an explanation for the evolution of mate preferences. The American Naturalist, 166, 437–446.

    Article  PubMed  Google Scholar 

  • Grafen, A. (1990). Biological signals as handicaps. Journal of Theoretical Biology, 144, 517–546.

    Article  CAS  PubMed  Google Scholar 

  • Guyon, J. (1992). Darwin et l’après-Darwin: Une histoire de l’hypothèse de selection naturelle. Paris: Editions Kimé.

    Google Scholar 

  • Haag-Liautard, C., Dorris, M., Maside, X., Macaskill, S., Halligan, D. L., Charlesworth, B., & Keightley, P. D. (2007). Direct estimates of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature, 445, 82–85.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos, 35, 282–290.

    Article  Google Scholar 

  • Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science, 218, 384–387.

    Article  CAS  PubMed  Google Scholar 

  • Hedrick, P. W. (2002). Pathogen resistance and genetic variation at MHC loci. Evolution, 56, 1902–1908.

    Article  PubMed  Google Scholar 

  • Höglund, J., & Alatalo, R. V. (1995). Leks. Princeton: Princeton University Press.

    Book  Google Scholar 

  • Hosken, D. J., & Stockley, P. (2004). Sexual selection and genital evolution. Trends in Ecology and Evolution, 19, 87–93.

    Article  PubMed  Google Scholar 

  • Houle, D., & Kondrashov, A. S. (2002). Coevolution of costly mate choice and condition-dependent display of good genes. Proceedings of the Royal Society of London Series B: Biological Sciences, 269, 97–104.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes, A. L. (1981). Differential male mating success in the white spotted sawyer Monochamus scutellatus (Coleoptera: Cerambycidae). Annals of the Entomological Society of America, 74, 180–184.

    Article  Google Scholar 

  • Hughes, A. L. (1985). Male size, mating success, and mating strategy in the mosquitofish Gambusia affinis (Poeciliidae). Behavioral Ecology and Sociobiology, 17, 271–278.

    Article  Google Scholar 

  • Hughes, A. L. (1999). Adaptive evolution of genes and genomes. New York: Oxford University.

    Google Scholar 

  • Hughes, A. L. (2001). Evolutionary change of predicted cytotoxic T cell epitopes of dengue virus. Infection, Genetics and Evolution, 1, 123–130.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L. (2005). Evidence for abundant slightly deleterious polymorphisms in bacterial populations. Genetics, 169, 553–558.

    Article  Google Scholar 

  • Hughes, A. L. (2007). Looking for Darwin in all the wrong places: The misguided quest for positive selection at the nucleotide sequence level. Heredity, 99, 364–373.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L. (2008). Near neutrality: Leading edge of the neutral theory of molecular evolution. Annals of the New York Academy of Sciences, 1133, 162–179.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes, A. L. (2010a). Reduced microsatellite heterozygosity in island endemics supports the role of long-term effective population size in avian microsatellite diversity. Genetica, 138, 1271–1276.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes, A. L. (2010b). Runaway evolution of the male-specific exon of the doublesex gene in Diptera. Gene, 472, 1–6.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes, A. L. (2012). Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity, 108, 347–353.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes, A. L. (2013). Female reproductive effort and sexual selection on male waterfowl. Evolutionary Biology, 40, 92–100.

    Article  Google Scholar 

  • Hughes, A. L., & Hughes, M. A. (2007). Coding sequence polymorphism in avian mitochondrial genomes reflects population histories. Molecular Ecology, 16, 1369–1376.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L., Hughes, M. K., Howell, C. Y., & Nei, M. (1994). Natural selection at the class II major histocompatibility complex loci of mammals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 346, 359–367.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L., & Nei, M. (1988). Pattern of nucleotide substitution at MHC class I loci reveals overdominant selection. Nature, 335, 167–170.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L., Packer, B., Welsch, R., Bergen, A. W., Chanock, S. J., & Yeager, M. (2003). Widespread purifying selection at polymorphic sites in human protein-coding loci. Proceedings of the National Academy of Sciences of the United States of America, 100, 15754–15757.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes, A. L., & Yeager, M. (1998). Natural selection at major histocompatibility complex loci of vertebrates. Annual Review of Genetics, 32, 415–435.

    Article  CAS  PubMed  Google Scholar 

  • Irausquin, S. J., & Hughes, A. L. (2008). Distinctive pattern of sequence polymorphism in the NS3 protein of hepatitis C virus type 1b reflects conflicting evolutionary pressures. Journal of General Virology, 89, 1921–1929.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Irausquin, S. J., & Hughes, A. L. (2011). Conflicting selection pressures on T-cell epitopes in HIV-1 subtype B. Infection, Genetics and Evolution, 11, 483–488.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iwasa, Y., Pomiankowski, A., & Nee, S. (1991). The evolution of costly mate preferences. II. The “handicap” principle. Evolution, 45, 1431–1442.

    Article  Google Scholar 

  • Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge (UK): Cambridge University Press.

    Book  Google Scholar 

  • Kirkpatrick, M. (1996). Good genes and direct selection in the evolution of mating preferences. Evolution, 50, 2125–2140.

    Article  Google Scholar 

  • Kirkpatrick, M., & Ryan, M. J. (1991). The evolution of mating preferences and the paradox of the lek. Nature, 350, 33–38.

    Article  Google Scholar 

  • Klein, J., & Hořejší, V. (1997). Immunology (2nd ed.). Oxford: Blackwell.

    Google Scholar 

  • Kondrashov, A. (1988). Deleterious mutations and the evolution of sexual reproduction. Nature, 336, 435–440.

    Article  CAS  PubMed  Google Scholar 

  • Kuijper, B., Pen, I., & Weissing, F. J. (2012). A guide to sexual selection theory. Annual Review of Ecology Evolution and Systematics, 43, 287–311.

    Article  Google Scholar 

  • Kull, K. (2013). Adaptive evolution without natural selection. Biological Journal of the Linnean Society, 112, 287–294.

    Article  Google Scholar 

  • Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences of the United States of America, 78, 3721–3725.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lehmann, L., Keller, L. F., & Kokko, H. (2007). Mate choice evolution, dominance effects, and the maintenance of genetic variation. Journal of Theoretical Biology, 244, 282–295.

    Article  CAS  PubMed  Google Scholar 

  • Lehtonen, J., & Kokko, H. (2011). Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 211–221.

    Article  Google Scholar 

  • Lynch, M., & Conery, J. S. (2003). The origins of genome complexity Science, 302, 1401–1404.

    CAS  PubMed  Google Scholar 

  • Mayr, E. (1963). Populations, species, and evolution. Cambridge (MA): Belknap Press.

    Book  Google Scholar 

  • Mays, H. L., & Hill, G. E. (2004). Choosing mates: Good genes versus genes that are a good fit. Trends in Ecology & Evolution, 19, 554–559.

    Article  Google Scholar 

  • McGuigan, K., Petfield, D., & Blows, M. W. (2011). Reducing mutation load through sexual selection on males. Evolution, 65, 2816–2829.

    Article  PubMed  Google Scholar 

  • Milinski, M. (2006). The major histocompatibility complex, sexual selection, and mate choice. Annual Review of Ecology Evolution and Systematics, 37, 159–186.

    Article  Google Scholar 

  • Moore, C. B., John, M., James, I. R., Christiansen, F. T., Witt, C. S., & Mallal, S. A. (2002). Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science, 296, 1439–1443.

    Article  CAS  PubMed  Google Scholar 

  • Morton, E. S. (1975). Sources of ecological selection on avian sounds. American Naturalist, 109, 17–34.

    Article  Google Scholar 

  • Neff, B. D., & Pitcher, T. P. (2005). Genetic quality and sexual selection: An integrated framework for good genes and compatible genes. Molecular Ecology, 14, 19–38.

    Article  CAS  PubMed  Google Scholar 

  • Nei, M. (2005). Selectionism and neutralism in molecular evolution. Molecular Biology and Evolution, 22, 2318–2342.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nei, M. (2007). The new mutation theory of phenotypic evolution. Proceedings of the National Academy of Sciences of the United States of America, 104, 12235–12242.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nei, M. (2013). Mutation-driven evolution. New York: Oxford University Press.

    Google Scholar 

  • Nichols, R. A., & Butlin, R. K. (1989). Does runaway sexual selection work in finite populations? Journal of Evolutionary Biology, 2, 299–313.

    Article  Google Scholar 

  • O’Brien, S. J., & Nelson, G. W. (2004). Human genes that limit AIDS. Nature Genetics, 36, 565–574.

    Article  PubMed  Google Scholar 

  • O’Connor, S. L., Lhost, J. J., Becker, E. A., Detmer, A. M., Johnson, R. C., Macnair, C. E., et al. (2010). MHC heterozygote advantage in simian immunodeficiency cirus-infected Mauritian cynomolgus macaques. Science Translational Medicine, 2, 2ra18.

    Google Scholar 

  • Ohta, T. (1973). Slightly deleterious mutant substitutions in evolution. Nature, 246, 96–98.

    Article  CAS  PubMed  Google Scholar 

  • Palstra, F. P., & Ruzzante, D. E. (2008). Genetic estimates of contemporary effective population size: What can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology, 17, 3428–3447.

    Article  PubMed  Google Scholar 

  • Partridge, L. (1980). Mate choice increases a component of offspring fitness in fruit flies. Nature, 283, 290–291.

    Article  Google Scholar 

  • Penn, D. J., Damjanovich, K., & Potts, W. K. (2002). MHC heterozygosity confers a selective advantage against multiple-strain infections. Proceedings of the National Academy of Sciences of the United States of America, 99, 11260–11264.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Penn, D., & Potts, W. A. (1998). Chemical signals and parasite-mediated sexual selection. Trends in Ecology & Evolution, 13, 391–396.

    Article  CAS  Google Scholar 

  • Price, T. (2006). Phenotypic plasticity, sexual selection and the evolution of colour patterns. Journal of Experimental Biology, 209, 2368–2374.

    Article  CAS  PubMed  Google Scholar 

  • Prum, R. O. (2010). The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: Implications for meaning, honesty, and design in intersexual signals. Evolution, 64, 3085–3100.

    Article  PubMed  Google Scholar 

  • Reynolds, J. D., & Gross, M. R. (1992). Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proceedings of the Royal Society of London Series B: Biological Sciences, 250, 57–62.

    Article  Google Scholar 

  • Roelofs, W. L., Liu, W., Hao, G., Jiao, H., Rooney, A. P., & Linn, C. E., Jr. (2002). Evolution of moth sex pheromones via ancestral genes. Proceedings of the National Academy of Sciences of the United States of America, 99, 13621–13636.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roelofs, W. L., & Rooney, A. J. (2003). Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America, 100, 9179–9184.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan, M. J. (1990). Sexual selection, sensory systems and sensory exploitation. Oxford Surveys Evolutionary Biology, 7, 157–195.

    Google Scholar 

  • Ryan, M. J., & Cummings, M. E. (2013). Perceptual biases and mate choice. Annual Review of Ecology Evolution and Systematics, 44, 437–459.

    Article  Google Scholar 

  • Sánchez, L., & Guerrero, I. (2001). The development of the Drosophila genital disc. BioEssays, 23, 698–707.

    Article  PubMed  Google Scholar 

  • Shapiro, A. M., & Porter, A. H. (1989). The lock-and-key hypothesis: Evolutionary and biosystematic interpretation of insect genitalia. Annual Review of Entomology, 34, 231–245.

    Article  Google Scholar 

  • Siller, S. (2001). Sexual selection and the maintenance of sex. Nature, 411, 689–692.

    Article  CAS  PubMed  Google Scholar 

  • Simmons, L. W. (1986). Female choice contributes to offspring fitness in the field cricket, Gryllus bimaculatus (De Geer). Behavioral Ecology and Sociobiology, 21, 313–321.

    Article  Google Scholar 

  • Spurgin, L. G., & Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society of London Series B: Biological Sciences, 277, 979–988.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahata, N., & Nei, M. (1990). Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124, 967–978.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tomkins, J. L., Penrise, M. A., Greeft, J., & leBas, N. R. (2010). Additive genetic breeding values correlate with the load of partially deleterious mutations. Science, 328, 892–894.

    Article  CAS  PubMed  Google Scholar 

  • Trivers, R. L. (1972). Parental effort and sexual selection. In B. G. Campbell (Ed.), Sexual selection and the descent of man (pp. 136–179). Chicago: Aldine.

    Google Scholar 

  • Van Oosterhout, C. (2009). A new theory of MHC evolution: Beyond selection on the immune genes. Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 657–665.

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1, 1–30.

    Google Scholar 

  • Vincent, S., Perkins, L. A., & Perrimon, N. (2001). Doublesex surprises. Cell, 106, 399–402.

    Article  CAS  PubMed  Google Scholar 

  • Wallace, A. R. (1889). Darwinism. London: Macmillan.

    Google Scholar 

  • Weatherhead, P. J., & Robertson, R. T. (1979). Offspring quality and the polygyny threshold: “The sexy son hypothesis”. American Naturalist, 113, 201–208.

    Article  Google Scholar 

  • Wegner, K. M., Kalbe, M., Schaschl, H., & Reusch, T. B. (2004). Parasites and individual major histocompatibility complex diversity: An optimal choice? Micobes and Infection, 6, 1110–1116.

    Article  CAS  Google Scholar 

  • Whitlock, M. C. (2000). Fixation of new alleles and the extinction of small populations; Drift load, beneficial alleles, and sexual selection. Evolution, 54, 1855–1861.

    Article  CAS  PubMed  Google Scholar 

  • Whitlock, M. C., & Agrawal, A. F. (2009). Purging the genome with sexual selection: Reducing mutation load through selection on males. Evolution, 63, 569–582.

    Article  CAS  PubMed  Google Scholar 

  • Williams, G. C. (1966). Adaptation and natural selection. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Zahavi, A. (1975). Mate selection: Selection for a handicap. Journal of Theoretical Biology, 53, 205–214.

    Article  CAS  PubMed  Google Scholar 

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Hughes, A.L. Sexual Selection and Mate Choice: Insights from Neutralist Perspectives. Evol Biol 42, 366–378 (2015). https://doi.org/10.1007/s11692-015-9315-x

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