Abstract
Understanding the processes underlying the origin of new species is a fundamental problem in evolutionary research. Whilst it has long been recognised that closely related taxa often differ markedly in reproductive characteristics, only relatively recently has sexual selection been evoked as a key promoter of speciation through its ability to generate reproductive isolation (RI). Sexual selection potentially can influence the probability that individuals from the same or different populations will reproduce successfully since it shapes precisely those traits involved in mating and reproduction. If reproductive characters diverge along different trajectories, then sexual selection can impact on the evolution of reproductive barriers operating both before and after mating. In this perspective, we consider some new advances in our understanding of the coevolution of male and female sexual signals and receptors and suggest how these developments may provide heretofore neglected insights into the mechanisms by which isolating barriers may emerge. Specifically, we explore how selfish genetic elements (SGEs) can mediate pre- and post-copulatory mate choice, thereby influencing gene flow and ultimately population divergence; we examine evidence from studies of intracellular sperm–egg interactions and propose that intracellular gametic incompatibilities may arise after sperm entry into the egg, and thus contribute to RI; we review findings from genomic studies demonstrating rapid, adaptive evolution of reproductive genes in both sexes and discuss whether such changes are causal in determining RI or simply associated with it; and finally, we consider genetic, developmental and functional mechanisms that might constrain reproductive trait diversification, thereby limiting the scope for reproductive barriers to arise via sexual selection. We hope to stimulate work that will further the understanding of the role sexual selection plays in generating RI and ultimately speciation.
Similar content being viewed by others
References
Alipaz JA, Wu CI, Karr TL (2001) Gametic incompatibilities between races of D. melanogaster. Proc Roy Soc Lond B 268:789–795
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Arnold S (1992) Constraints on phenotypic evolution. Am Nat 140:S85–S107
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Bacigalupe L, Crudgington HS, Hunter F, Moore AJ, Snook RR (2007) Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura. J Evol Biol. doi: 10.1111/j.1420–9101.2007.01389.x
Begun DJ, Whitley P, Todd BL, Waldrip-Dail HM, Clark AG (2000) Molecular population genetics of male accessory gland proteins in Drosophila. Genetics 156:1879–1888
Begun DJ, Lindfors HA, Thompson ME, Holloway AK (2006) Recently evolved genes identified from Drosophila yakuba and D. erecta accessory gland expressed sequence tags. Genetics 172:1675–1681
Beukeboom LW (1994) Phenotypic fitness effects on the selfish B-chromosome, paternal sex-ratio (PSR) in the parasitic wasp Nasonia vitripennis. Evol Ecol 8:1–24
Bordenstein SR, O’Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409:707–710
Braswell WE, Andrès JA, Maroja LS, Harrison RG, Howard DJ, Swanson WJ (2006) Identification and comparative analysis of accessory gland proteins in Orthoptera. Genome 49:1069–1080
Brent AF, MacQueen A, Hazelrigg T (2000) The Drosophila wispy gene is required for RNA localization and other microtubule-based events of meiosis and early embryogenesis. Genetics 154:1649–1662
Burt A, Trivers R (2006) Genes in conflict. Harvard University Press, London
Casselton LA, Olesnicky NS (1998) Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62:55–70
Champion de Crespigny FE, Wedell N (2006) Wolbachia infection reduces sperm competitive ability in an insect. Proc R Soc Lond B 273:1455–1458
Champion de Crespigny FE, Wedell N (2007) Mate preferences in Drosophila infected with Wolbachia? Behav Ecol Sociobiol 61:1229–1235
Champion de Crespigny FE, Butlin RK, Wedell N (2005) Can cytoplasmic incompatibility inducing Wolbachia promote the evolution of mate preferences? J Evol Biol 18:967–977
Civetta A, Singh RS (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
Clark NL, Swanson WJ (2005) Pervasive adaptive evolution in primate seminal proteins. Plos Genet 1:335–342
Clark AG, Aguade M, Prout T, Harshman LG, Langley CH (1995) Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139:189–201
Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, New York
Cutter AD, Ward S (2005) Sexual and temporal dynamics of molecular evolution in C. elegans. Mol Biol Evol 22:178–188
Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London
Davies SJ, Chapman T (2006) Identification of genes expressed in the accessory glands of male Mediterranean Fruit Flies (Ceratitis capitata). Ins Biochem Mol Biol 36:846–856
Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT (2004) Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36:1326–1329
Ducrocq V, Humblot P (1995) Genetic characteristics and evolution of semen production of young Normande bulls. Livest Prod Sci 41:1–10
Duret L, Mouchiroud D (2000) Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol Biol Evol 17:68–74
Feibig A, Kimport R, Preuss D (2004) Comparisons of pollen coat genes across Brassicaceae species reveals rapid evolution by repeat expansion and diversification. Proc Natl Acad Sci USA 101:3286–3291
Fiumera AC, Dumont BL, Clark AG (2005) Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics 169:243–257
Frank SA (2000) Sperm competition and female avoidance of polyspermy mediated by sperm–egg biochemistry. Evol Ecol Res 2:613–625
Fry CL, Wilkinson GS (2004) Sperm survival in female stalk-eyed flies depends on seminal fluid and meiotic drive. Evolution 58:1622–1626
Fuyama Y (1983) Species-specificity of paragonial substances as an isolating mechanism in Drosophila. Experientia 39:190–192
Gage MJG, Freckleton RP (2002) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc Roy Soc Lond B 270:625–632
Gage MJG, Parker GA, Nylin S, Wiklund C (2002) Sexual selection and speciation in mammals, butterflies and spiders. Proc Roy Soc Lond B 269:2309–2316
Galindo BE, Vacquier VD, Vacquier WJ (2003) Positive selection in the egg receptor for abalone sperm lysine. Proc Natl Acad Sci USA 100:4639–4643
Garant D, Dodson JD, Bernatchez L (2005) Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar). Behav Ecol Sociobiol 57:240–244
García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution 61:816–824
Gavrilets S (2000) Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886–889
Good JM, Nachman MW (2005) Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol Biol Evol 22:1044–1052
Gray D, Plusa B, Piotrowska K (2004) First cleavage of the mouse embryo responds to change in egg shape at fertilization. Curr Biol 14:397–405
Haig D, Bergstrom CT (1995) Multiple mating, sperm competition and meiotic drive. J Evol Biol 8:265–282
Hoffmann AA, Turelli M (1988) Unidirectional incompatibility in Drosophila simulans: Inheritance, geographic variation and fitness effects. Genetics 119: 435–444
Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–948
Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Ann Rev Ecol Syst 30:109–132
Hurst GDD, Schilthuizen M (1998) Selfish genetic elements and speciation. Heredity 80:2–8
Hurst GDD, Hammarton TC, Obrycki JJ, Majerus TMO, Walker LE, Bertrand D, Majerus MEN (1996) Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera:Coccinellidae). Heredity 77:177–185
Jaenike J, Dyer KA, Cornish C, Minhas MS (2006) Asymmetrical reinforcement and Wolbachia infection in Drosophila. Plos Biol 4:1852–1862
Jagadeeshan S, Singh RS (2005) Rapidly evolving genes of Drosophila: differing levels of selective pressure in testis, ovary, and head tissues between sibling species. Mol Biol Evol 22:1793–1801
Jamieson BGM (1987) The ultrastructure and phylogeny of insect spermatozoa. Cambridge University Press, Cambridge
Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9:393–405
Jiggins FM, Randerson JP, Hurst GDD, Majerus MEN (2002) How can sex ratio distorters reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution 56:2290–2295
Johns PM, Wolfenbarger LL, Wilkinson GS (2005) Genetic linkage between a sexually selected trait and X chromsome meiotic drive. Proc Roy Soc Lond B 272:2097–2103
Karr TL (1991) Intracellular sperm/egg interactions in Drosophila: a three dimensional structural analysis of a paternal product in the developing egg. Mech Dev 34:101–112
Karr TL (1996) Paternal investment and intracellular sperm–egg interactions during and following fertilization in Drosophila. Curr Top Dev Biol 34:89–115
Karr TL, Pitnick S (1996) The ins and outs of fertilization. Nature 379:405–406
Kern A, Jones C, Begun D (2004) Molecular population genetics of male accessory gland proteins in the Drosophila simulans complex. Genetics 167:725–735
Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiotisi SN (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60:87–96
Krawetz SA (2005) Paternal contributions: new insights and future challenges. Nat Rev Genet 6:633–642
LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc Roy Soc Lond B 265:1997–2002
Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725
Lande R, Wilkinson GS (1999) Models of sex-ratio meiotic drive and sexual selection in stalk-eyed flies. Genet Res 74:245–253
Lassy CW, Karr TL (1996) Cytological analysis of fertilization and early embryonic development in the incompatible crosses of Drosophila simulans. Mech Dev 57: 47–58
Lenington S (1983) Social preferences for partners carrying ‘good genes’ in wild house mice. Anim Behav 31:325–333
Lenington S (1991) The t-complex: a story of genes, behavior, and populations. Adv Study Behav 20:51–86
Levitan DR, Ferrell DL (2006) Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312:267–269
Loppin B, Karr TL (2005) Molecular genetics of insect fertilization. In: Gilbert L, Iatrou K, Gill S (eds) Comprehensive insect physiology, biochemistry, pharmacology and molecular biology. Elsevier, pp 213–235
Lyon JD, Vacquier VD (1999) Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelling envelope. Dev Biol 214:151–159
Makalowski W, Boguski MS (1998) Evolutionary parameters of the transmitted mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci USA 95:9407–9412
Martin OY, Hosken DJ (2003) The evolution of reproductive isolation through sexual conflict. Nature 423:979–982
Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 10:554–559
Meiklejohn CD, Parsch J, Ranz JM, Hartl DL (2003) Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci USA 100:9894–9899
Metta M, Gudavalli R, Gibert JM, Schlötterer C (2006) No accelerated rate of protein evolution in male-biased Drosophila pseudoobscura genes. Genetics 174:411–420
Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233
Moomjy M, Columbero LT, Beeck LL, Rosenwaks Z, Palermo GD (1999) Sperm integrity is critical for normal mitotic division and early embryonic development. Mol Hum Reprod 5:836–844
Moore AJ, Moore PJ (1999) Balancing sexual selection through opposing mate choice and male competition. Proc Roy Soc Lond B 266:711–716
Moore PJ, Harris WE, Montrose VT, Levin D, Moore AJ (2004) Genetic constraints on post-copulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58:1773–1780
Morrow EH, Pitcher TE, Arnqvist G (2003) No evidence that sexual selection is an ‘engine of speciation’ in birds. Ecol Lett 6:228–234
Mueller JL, Ripoll DR, Aquadro CF, Wolfner MF (2004) Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. Proc Natl Acad Sci USA 101:13542–13547
Mueller JL, Ram KR, McGraw LA, Qazi MCB, Siggia ED, Clark AG, Aquadro CF, Wolfner MF (2005) Cross-species comparison of Drosophila male accessory gland protein genes. Genetics 171:131–143
Nakamura S, Terada Y, Horiuchi T, Emuta C, Murakami T, Yaegashi N, Okamura K (2001) Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a piezo-driven pipette: a novel assay for human sperm centrosomal function. Biol Reprod 65:1359–1363
Navara CS, First NL, Schatten G (1996) Phenotypic variations among paternal chromosomes expressed within the zygote as disparate microtubule lengths and sperm aster organization: correlations between centrosome activity and developmental success. Proc Natl Acad Sci USA 93:5384–5388
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:9–38
Nichols RA, Butlin RK (1989) Does selection work in finite populations? J Evol Biol 2:299–313
Nurminsky DI, Nurminskaya MV, De Aguiar D, Hartl DL (1998) Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396:572–575
Ohsako T, Hirai K, Yamamoto MT (2003) The Drosophila misfire gene has an essential role in sperm activation during fertilization. Genes Genet Syst 78:253–266
O’Neill SL, Hoffmann AA, Werren JH (1997) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford
Orr HA (2005) The genetic basis of reproductive isolation: insights from Drosophila. Proc Natl Acad Sci USA 102:6522–6526
Orr HA, Masly JP, Phadnis N (2006) Speciation in Drosophila: from phenotypes to molecules. J Hered 98:102–110
Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637
Panhuis TM, Swanson WJ (2006) Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila. Genetics 173:2039–2047
Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371
Panhuis TM, Clark NL, Swanson WJ (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans Roy Soc B 361:261–268
Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 3–54
Parker GA, Partridge L (1998) Sexual conflict and speciation. Philos Trans Roy Soc Lond B 353:261–274
Parsch J, Meiklejohn C, Hauschteck-Jungen E, Hartl D (2001) Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup. Mol Biol Evol 18:801–811
Pattarini JM, Starmer WT, Bjork A, Pitnick S (2006) Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60:2064–2080
Pedersen RA (2001) Sperm and mammalian polarity. Nature 409:473–474
Piotrowska K, Zernicka-Goetz M (2001) Role for sperm in spatial patterning of the early mouse embryo. Nature 409:517–521
Pitnick S, Karr TL (1998) Paternal products and by-products in Drosophila development. Proc Roy Soc Lond B 265:821–826
Pitnick S, Miller GT, Schneider K, Markow TA (2003) Ejaculate-female coevolution in Drosophila mojavensis. Proc Roy Soc Lond B 270:1507–1512
Podlaha O, Zhang J (2003) Positive selection on protein length in the evolution of a primate sperm ion channel. Proc Natl Acad Sci USA 100:12241–12246
Pomiankowski A, Hurst LD (1999) Driving sexual preference. Trends Ecol Evol 14:425–426
Price TAR, Wedell N (2007) Selfish genetic elements and sexual selection: their impact on male fertility. Genetica (in press)
Proschel M, Zhang Z, Parsch J (2006) Widespread adaptive evolution of Drosophila genes with sex biased expression. Genetics 174:893–900
Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. Unviersity of Chicago Press, Chicago
Randerson JP, Jiggins FM, Hurst LD (2000) Male killing can select for male mate choice: a novel solution to the paradox of the lek. Proc Roy Soc Lond B 267:867–874
Rawe Y, Terada Y, Nakamura S, Chillik CF, Olmedo SB, Hemes HE (2002) A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Hum Reprod 17:2344–2349
Reinhold K, Engqvist L, Misof B, Kurtz J (1999) Meiotic drive and evolution of female choice. Proc Roy Soc Lond B 266:1341–1345
Richards S, Liu Y, Bettencourt BB et al (49 authors) (2005) Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res 15:1–18
Rice WR (1998) Intergenomic conflict, interlocus antagonistic coevolution and the evolution of reproductive isolation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 261–270
Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102
Sainudiin R, Wong WS, Yogeeswaran K, Nasrallah JB, Yang Z, Neilsen R (2005) Detecting site-specific physiochemical selection pressures: applications to the class I HLA of the human major histocompatibility complex and the SRK of the plant sporophytic self-incompatibility system. J Mol Evol 60:315–326
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton Press, Princeton
Sinervo MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34:339–364
Snook RR (1997) Is the production of multiple sperm types adaptive? Evolution 51:797–808
Snook RR (2005) Sperm competition: not playing by the numbers. Trends Ecol Evol 20:46–53
Snook RR, Karr TL (1998) Only long sperm are fertilization-competent in six sperm-heteromorphic Drosophila species. Curr Biol 8:291–294
Snook RR, Cleland SY, Wolfner MF, Karr TL (2000) Offsetting effects of Wolbachia infection and heat shock on sperm production in Drososphila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155:167–178
Stouthamer R, Breeuwer JAJ, Luck RF, Werren JH (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66–68
Sullivan J, Jaenike J (2006) Male-killing Wolbachia and male mate choice: a test with Drosophila innubila. Evol Ecol Res 8:91–102
Sutovsky P, Schatten G (2000) Paternal contributions to the mammalian zygote: fertilization after sperm–egg fusion. Int Rev Cytol 195:1–65
Swanson WJ, Vacquier VD (1995) Extraordinary divergence and positive Darwinian selection in a fisagenic protein coating the acrosomal process of abalone spermatozoa. Proc Natl Acad Sci USA 92:4957–4961
Swanson WJ, Vacquier VD (1998) Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281:710–712
Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144
Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF (2001a) Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA 98:7375–7379
Swanson WJ, Aquadro CF, Vacquier VD (2001b) Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg’s receptor for lysin (VERL) and positive Darwinian selection of sperm lysin. Mol Biol Evol 18:376–383
Swanson WJ, Yang Z, Wolfner MF, Aquadro CF (2001c) Positive Darwinian selection drives the evolution of several reproductive proteins in mammals. Proc Natl Acad Sci USA 98:2509–2514
Swanson WJ, Nielsen R, Yang QF (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20:18–20
Swanson WJ, Wong A, Wolfner MF, Aquadro CF (2004) Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168:1457–1465
Takebayashi N, Brewer PB, Newbigin E, Uyenoyama MK (2003) Patterns of variation within self-incompatibility loci. Mol Biol Evol 20:1779–1794
Telschow A, Hammerstein P, Werren JH (2005) The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59:1607–1619
Tregenza T, Wedell N (2000) Genetic incompatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027
Vala F, Egas M, Breeuwer JAJ, Sabelis MW (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. J Evol Biol 17:692–700
Wade MJ, Chang NW (1995) Increased male fertility in Tribolium confusum beetles after infection with the intracellular parasite Wolbachia. Nature 373:72–74
Wagstaff BJ, Begun DJ (2005a) Comparative genomics of accessory gland protein genes in Drosophila melanogaster and D. pseudoobscura. Mol Biol Evol 22:818–832
Wagstaff BJ, Begun DJ (2005b) Molecular population genetics of accessory gland protein genes and testis-expressed genes in Drosophila mojavensis and D. arizonae. Genetics 171:1083–1101
Wakimoto BT, Lindsley DL, Herrera C (2004) Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167:207–216
West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Quart Rev Biol 58:155–183
Wigby S, Chapman T (2006) No evidence that experimental manipulation of sexual conflict drives premating reproductive isolation in Drosophila melanogaster. J Evol Biol 19:1033–1039
Wilkinson GS, Fry CL (2001) Meiotic drive alters sperm competitive ability in stalk-eyed flies. Proc Roy Soc Lond B 268:2559–2564
Wilkinson GS, Sanchez MI (2001) Sperm development, age and sex chromosome meiotic drive in the stalk-eyed fly, Cyrtodiopsis whitei. Heredity 87:17–24
Wilkinson GS, Johns PM, Kelleher ES, Muscedere ML, Lorsong A (2006) Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni. J Evol Biol 19:1851–1860
Wilkinson GS, Presgraves DC, Crymes L (1998) Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391:276–279
Williams J, Lenington S (1993) Environmental and genetic factors affecting preferences of female house mice (Mus domesticus) for males that differ in t-complex genotype. Behav Genet 23:51–58
Wong A, Albright SN, Wolfner MF (2006) Evidence for structural constraint on ovulin, a rapidly evolving Drosophila melanogaster seminal protein. Proc Natl Acad Sci USA 103:18644–18649
Yang Z, Swanson WJ, Vacquier VD (2000) Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol Biol Evol 17:1446–1455
Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc Roy Soc Lond B 263:1711–1717
Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc Roy Soc Lond B 264:69–75
Zeh JA, Zeh DW (2003) Towards a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950
Zigler KS, McCartney MA, Levitan DR, Lessios HA (2005) Sea urchin bindin divergence predicts gamete compatibility. Evolution 59:2399–2404
Acknowledgements
RRS would like to thank the organizers of the Lund speciation symposium, Roger Härdling, Åsa Lankinen, Erik Svensson and Jörgen Ripa, for the invitation to participate and their patience during the production of this manuscript. RRS also thanks Tim Karr for his critical role in the development of understanding intracellular gametic interactions. RRS was funded by NSF and NERC. TC was funded by the Royal Society. NW wishes to thank Roger Butlin and Tom Tregenza for insightful comments and NERC for funding.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Snook, R.R., Chapman, T., Moore, P.J. et al. Interactions between the sexes: new perspectives on sexual selection and reproductive isolation. Evol Ecol 23, 71–91 (2009). https://doi.org/10.1007/s10682-007-9215-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-007-9215-3