Key Points
-
Many genes that are involved in different aspects of sexual reproduction evolve at rapid rates. For example, when rodent and human gene sequences are compared, many reproductive genes are found among the 10% most divergent genes.
-
In some cases, the rapid evolution of reproductive proteins is promoted by adaptive evolution, which indicates that a functional benefit underlies their rapid divergence.
-
The selective pressures that drive the evolution of reproductive proteins could include: sperm competition, cryptic female choice and sexual conflict.
-
The coevolution of corresponding (interacting) female and male pairs of reproductive proteins could be a factor in the establishment of barriers to fertilization, which leads to reproductive isolation between populations and, perhaps, the establishment of new species.
Abstract
Many genes that mediate sexual reproduction, such as those involved in gamete recognition, diverge rapidly, often as a result of adaptive evolution. This widespread phenomenon might have important consequences, such as the establishment of barriers to fertilization that might lead to speciation. Sequence comparisons and functional studies are beginning to show the extent to which the rapid divergence of reproductive proteins is involved in the speciation process.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Singh, R. S. & Kulathinal, R. J. Sex gene pool evolution and speciation: a new paradigm. Genes Genet. Syst. 75, 119–130 (2000).
Vacquier, V. D. Evolution of gamete recognition proteins. Science 281, 1995–1998 (1998).
Civetta, A. & Singh, R. S. 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 (1995).An important paper showing that, on average, Drosophila reproductive proteins are about twice as diverse as non-reproductive proteins.
Yang, Z. & Bielawski, J. P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–503 (2000). An excellent review on the use of the d N/d S ratio to detect adaptive evolution (positive Darwinian selection).
Makalowski, W. & Boguski, M. S. Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc. Natl Acad. Sci. USA 95, 9407–9412 (1998).The authors compare many genes between rodents and humans, and provide a good database for the comparison of rapidly, and non-rapidly, evolving genes.
Li, W.-H. Molecular Evolution (Sinauer Associates, Sunderland, Massachusetts, 1997).
Lee, Y. H., Ota, T. & Vacquier, V. D. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol. Biol. Evol. 12, 231–238 (1995).
Hughes, A. L. & Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170 (1988).
Yang, Z., Nielsen, R., Goldman, N. & Pedersen, A. M. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431–449 (2000).
Swanson, W. J., Yang, Z., Wolfner, M. F. & Aquadro, C. F. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98, 2509–2514 (2001).This is the first demonstration of female reproductive proteins being subject to positive Darwinian selection.
Swanson, W. J., Clark, A. G., Waldrip-Dail, H. M., Wolfner, M. F. & Aquadro, C. F. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl Acad. Sci. USA 98, 7375–7379 (2001).
Luporini, P., Vallesi, A., Miceli, C. & Bradshaw, R. A. Chemical signaling in ciliates. J. Eukaryot. Microbiol. 42, 208–212 (1995).
Ferris, P. J., Pavlovic, C., Fabry, S. & Goodenough, U. W. Rapid evolution of sex-related genes in Chlamydomonas. Proc. Natl Acad. Sci. USA 94, 8634–8639 (1997).
Ferris, P. J., Woessner, J. P. & Goodenough, U. W. A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol. Biol. Cell 7, 1235–1248 (1996).
Armbrust, E. V. & Galindo, H. M. Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira. Appl. Environ. Microbiol. 67, 3501–3513 (2001).
Brown, A. J. & Casselton, L. A. Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet. 17, 393–400 (2001).
Casselton, L. A. & Olesnicky, N. S. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62, 55–70 (1998).
Schopfer, C. R., Nasrallah, M. E. & Nasrallah, J. B. The male determinant of self-incompatibility in Brassica. Science 286, 1697–1700 (1999).
Schopfer, C. R. & Nasrallah, J. B. Self-incompatibility. Prospects for a novel putative peptide-signaling molecule. Plant Physiol. 124, 935–940 (2000).
Kachroo, A., Schopfer, C. R., Nasrallah, M. E. & Nasrallah, J. B. Allele-specific receptor–ligand interactions in Brassica self-incompatibility. Science 293, 1824–1826 (2001).An elegant biochemical demonstration of receptor–ligand interaction that shows the specificity of reproductive proteins.
Nasrallah, J. B. Cell–cell signaling in the self-incompatibility response. Curr. Opin. Plant Biol. 3, 368–373 (2000).
Richman, A. D. & Kohn, J. R. Evolutionary genetics of self-incompatibility in the Solanaceae. Plant Mol. Biol. 42, 169–179 (2000).
Mayfield, J. A., Fiebig, A., Johnstone, S. E. & Preuss, D. Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292, 2482–2485 (2001).
Hellberg, M. E. & Vacquier, V. D. Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol. Biol. Evol. 16, 839–848 (1999).
Metz, E. C., Robles-Sikisaka, R. & Vacquier, V. D. Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc. Natl Acad. Sci. USA 95, 10676–10681 (1998).
Yang, Z., Swanson, W. J. & Vacquier, V. D. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol. Biol. Evol. 17, 1446–1455 (2000).
Swanson, W. J. & Vacquier, V. D. Liposome fusion induced by a M(r) 18,000 protein localized to the acrosomal region of acrosome-reacted abalone spermatozoa. Biochemistry 34, 14202–14208 (1995).
Swanson, W. J. & Vacquier, V. D. Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proc. Natl Acad. Sci. USA 92, 4957–4961 (1995).
Hellberg, M. E., Moy, G. W. & Vacquier, V. D. Positive selection and propeptide repeats promote rapid interspecific divergence of a gastropod sperm protein. Mol. Biol. Evol. 17, 458–466 (2000).
Swanson, W. J. & Vacquier, V. D. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281, 710–712 (1998).A model of species-specific fertilization based on molecular evolutionary analysis of interacting male and female reproductive proteins in plants.
Swanson, W. J., Aquadro, C. F. & Vacquier, V. D. 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 (2001).
Vacquier, V. D., Swanson, W. J. & Hellberg, M. E. What have we learned about sea urchin sperm bindin. Dev. Growth Differ. 37, 1–10 (1995).
Palumbi, S. R. & Metz, E. C. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol. 8, 227–239 (1991).
Metz, E. C. & Palumbi, S. R. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397–406 (1996).
Biermann, C. H. The molecular evolution of sperm bindin in six species of sea urchins (Echinodia: Strongylocentrotidae). Mol. Biol. Evol. 15, 1761–1771 (1998).
Wolfner, M. F. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem. Mol. Biol. 27, 179–192 (1997).A review of Drosophila accessory-gland proteins, which have been included in several evolutionary studies of reproductive proteins.
Partridge, L. & Hurst, L. D. Sex and conflict. Science 281, 2003–2008 (1998).
Xue, L. & Noll, M. Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proc. Natl Acad. Sci. USA 97, 3272–3275 (2000).
Chen, P. S. et al. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54, 291–298 (1988).
Herndon, L. A. & Wolfner, M. F. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc. Natl Acad. Sci. USA 92, 10114–10118 (1995).
Heifetz, Y., Lung, O., Frongillo, Jr E. A. & Wolfner, M. F. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr. Biol. 10, 99–102 (2000).
Kalb, J. M., DiBenedetto, A. J. & Wolfner, M. F. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc. Natl Acad. Sci. USA 90, 8093–8097 (1993).
Bertram, M. J., Neubaum, D. M. & Wolfner, M. F. Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem. Mol. Biol. 26, 971–980 (1996).
Neubaum, D. M. & Wolfner, M. F. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153, 845–857 (1999).
Tram, U. & Wolfner, M. F. Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics 153, 837–844 (1999).
Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F. & Partridge, L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241–244 (1995).
Harshman, L. G. & Prout, T. Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48, 758–766 (1994).
Clark, A. G., Aguade, M., Prout, T., Harshman, L. G. & Langley, C. H. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139, 189–201 (1995).
Tsaur, S. C. & Wu, C. I. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol. Biol. Evol. 14, 544–549 (1997).
Tsaur, S. C., Ting, C. T. & Wu, C. I. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila. II. Divergence versus polymorphism. Mol. Biol. Evol. 15, 1040–1046 (1998).
Begun, D. J., Whitley, P., Todd, B. L., Waldrip-Dail, H. M. & Clark, A. G. Molecular population genetics of male accessory gland proteins in Drosophila. Genetics 156, 1879–1888 (2000).
Aguade, M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics 152, 543–551 (1999).
Fuyama, Y. Species-specificity of paragonial substances as an isolating mechanism in Drosophila. Experientia 39, 190–192 (1983).
Wyckoff, G. J., Wang, W. & Wu, C. I. Rapid evolution of male reproductive genes in the descent of man. Nature 403, 304–309 (2000).This paper shows that rapidly evolving reproductive proteins occur in organisms with complex mating courtships.
Wassarman, P. M. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96, 175–183 (1999).
Yurewicz, E. C., Sacco, A. G., Gupta, S. K., Xu, N. & Gage, D. A. Hetero-oligomerization-dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J. Biol. Chem. 273, 7488–7494 (1998).
Chen, J., Litscher, E. S. & Wassarman, P. M. Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. Proc. Natl Acad. Sci. USA 95, 6193–6197 (1998).
Eidne, K. A., Henery, C. C. & Aitken, R. J. Selection of peptides targeting the human sperm surface using random peptide phage display identify ligands homologous to ZP3. Biol. Reprod. 63, 1396–1402 (2000).
Gao, Z. & Garbers, D. L. Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains. J. Biol. Chem. 273, 3415–3421 (1998).
Juneja, R., Agulnik, S. I. & Silver, L. M. Sequence divergence within the sperm-specific polypeptide TCTE1 is correlated with species-specific differences in sperm binding to zona-intact eggs. J. Androl. 19, 183–188 (1998).
Higgie, M., Chenoweth, S. & Blows, M. W. Natural selection and the reinforcement of mate recognition. Science 290, 519–521 (2000).
Hill, K. L. & L'Hernault, S. W. Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev. Biol. 232, 105–114 (2001).
O'Rand, M. G. Sperm–egg recognition and barriers to interspecies fertilization. Gamete Res. 19, 315–328 (1988).
Swanson, W. J. & Vacquier, V. D. The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc. Natl Acad. Sci. USA 94, 6724–6729 (1997).
Kresge, N., Vacquier, V. D. & Stout, C. D. Abalone lysin: the dissolving and evolving sperm protein. Bioessays 23, 95–103 (2001).
Elder, Jr J. F. & Turner, B. J. Concerted evolution of repetitive DNA sequences in eukaryotes. Q. Rev. Biol. 70, 297–320 (1995).
McAllister, B. F. & Werren, J. H. Evolution of tandemly repeated sequences: what happens at the end of an array? J. Mol. Evol. 48, 469–481 (1999).
Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).
Rieseberg, L. H., Van, F. C. & Desrochers, A. M. Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375, 313–316 (1995).
Knowlton, N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420, 73–90 (2000).
Palumbi, S. R. Marine speciation on a small planet. Trends Ecol. Evol. 7, 114–118 (1992).
Hellberg, M. E., Balch, D. P. & Roy, K. Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292, 1707–1710 (2001).
Van Doorn, G. S. Ecological versus sexual selection models of sympatric speciation. Selection (in the press).
Higashi, M., Takimoto, G. & Yamamura, N. Sympatric speciation by sexual selection. Nature 402, 523–526 (1999).
Palumbi, S. R. All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl Acad Sci. USA 96, 12632–12637 (1999).This paper shows the functional consequences of diversity of reproductive proteins, and that fertilization efficiency is dependent on the genotype of the reproductive protein loci.
Biermann, C. H. & Marks, J. A. Geographic divergence of gamete recognition systems in two species in the sea urchin genus Strongylocentrotus. Zygote 8, S86–S87 (2000).
Rahman, M. A. & Uehara, T. Experimental hybridisation between two tropical species of sea urchins (genus Echinometra) in Okinawa. Zygote 8, S90 (2000).
Dieckmann, U. & Doebeli, M. On the origin of species by sympatric speciation. Nature 400, 354–357 (1999).
Kondrashov, A. S. & Shpak, M. On the origin of species by means of assortative mating. Proc. R. Soc. Lond. B 265, 2273–2278 (1998).
Kondrashov, A. S. & Kondrashov, F. A. Interactions among quantitative traits in the course of sympatric speciation. Nature 400, 351–354 (1999).
Gavrilets, S. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403, 886–889 (2000).A mathematical model that shows how the rapid evolution of genes, such as in those that encode reproductive proteins, can lead to speciation.
Wu, C. I. A stochastic simulation study on speciation by sexual selection. Evolution 39, 66–82 (1985).
Clark, A. G., Begun, D. J. & Prout, T. Female × male interactions in Drosophila sperm competition. Science 283, 217–220 (1999).
Howard, D. J. Conspecific sperm and pollen precedence and speciation. A. Rev. Ecol. Syst. 30, 109–132 (1999).
Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, New Jersey, 1996).
Rice, W. R. & Holland, B. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41, 1–10 (1997).
Gould-Somero, M. & Jaffe, L. A. in Cell Fusion and Transformation(eds Beers, R. F. & Bassett, E. G.) 27–38 (Raven, New York, 1984).
Stephano, J. L. in Abalones of the World (eds Shepherd,S. A., Tegner, M. J. & Guzman del Proo, S. A.) 518–526 (Blackwell Science, Cambridge, Massachussetts,1992).
Jaffe, L. A., Sharp, A. P. & Wolf, D. P. Absence of an electrical polyspermy block in the mouse. Dev. Biol. 96, 317–323 (1983).
Gavrilets, S., Arnqvist, G. & Friberg, U. The evolution of female mate choice by sexual conflict. Proc. R. Soc. Lond. B 268, 531–539 (2001).
Barton, N. The rapid origin of reproductive isolation. Science 290, 462–463 (2000).
Eady, P. E. Postcopulatory, prezygotic reproductive isolation. J. Zool. 253, 47–52 (2001).
Blows, M. W. Evolution of the genetic covariance between male and female components of mate recognition: an experimental test. Proc. R. Soc. Lond. B 266, 2169–2174 (1999).
Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234 (1996).A description of a laboratory experiment showing that sexual conflict might drive the rapid evolution of reproductive proteins.
Arnqvist, G., Edvardsson, M., Friberg, U. & Nilsson, T. Sexual conflict promotes speciation in insects. Proc. Natl Acad. Sci. USA 97, 10460–10464 (2000).
Metz, E. C., Gomez-Gutierrez, G. & Vacquier, V. D. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol. Biol. Evol. 15, 185–195 (1998).
Acknowledgements
V.D.V. is supported by the National Institutes of Health and W.J.S. by the National Science Foundation. C. F. Aquadro, M. F. Wolfner, J. D. Calkins, J. P. Vacquier, M. E. Hellberg and two anonymous reviewers are thanked for their critical reading of the manuscript.
This article will appear as part of a web focus on the evolution of sex, which will coincide with our forthcoming special issue on this topic.
Author information
Authors and Affiliations
Corresponding author
Related links
Related links
DATABASES
FURTHER INFORMATION
Glossary
- ADAPTIVE EVOLUTION
-
A genetic change that results in increased fitness.
- ORTHOLOGOUS GENES
-
Homologous genes in different species that derive from a common ancestral gene without gene duplication or horizontal transmission.
- PURIFYING SELECTION
-
Selection against a deleterious allele.
- MAXIMUM LIKELIHOOD
-
The maximum-likelihood method takes a model of sequence evolution (essentially a set of parameters that describe the pattern of substitutions) and searches for the combination of parameter values that gives the greatest probability of obtaining the observed sequences.
- CILIATE
-
A single-celled protist with a micronucleus (germ-line nucleus), a macronucleus (somatic nucleus), and cilia for swimming and capturing food.
- CONJUGATION
-
The joining of two cells for the transfer of genetic material.
- DIATOM
-
A unicellular alga that is important in global photosynthesis and carbon cycling.
- INBREEDING DEPRESSION
-
Loss of vigour owing to homozygosity of an increasing number of genes; it occurs as a consequence of mating between closely related individuals.
- SPOROPHYTE
-
In plants that undergo alternation of generations, a multicellular diploid form that results from a union of haploid gametes and that meiotically produces haploid spores, which will in turn grow into the gametophyte generation.
- SIGNAL SEQUENCE
-
A short sequence on a newly translated polypeptide that serves as a signal for its transfer to the correct subcellular location.
- GAMETOPHYTE
-
In a reproductive cycle of a plant, a generation that has a haploid set of chromosomes and produces gametes.
- ACROSOME
-
A secretory organelle in the sperm head.
- SYMPATRIC
-
Having overlapping geographical distributions.
- GENE CONVERSION
-
The non-reciprocal transfer of information between homologous genes as a consequence of heteroduplex formation followed by repair mismatches.
- GASTROPOD
-
A class in the phylum Mollusca that is characterized by a muscular foot, on which the body rests, and a single shell. Examples include snails, limpets, sea hares and abalone.
- POLYMORPHISM
-
Occurrence, at a single genetic locus, of two or more alleles that differ in nucleotide sequence.
- ASSORTATIVE MATING
-
Non-random mating; it occurs when individuals select their mates on the basis of one or more physical or chemical characteristics.
- SEXUAL SELECTION
-
Selection for characteristics that enhance mating success.
- QUANTITATIVE TRAIT
-
A measurable trait that depends on the cumulative action of many genes (or quantitative trait loci).
- ALLOPATRIC
-
Having non-overlapping geographical distributions.
Rights and permissions
About this article
Cite this article
Swanson, W., Vacquier, V. The rapid evolution of reproductive proteins. Nat Rev Genet 3, 137–144 (2002). https://doi.org/10.1038/nrg733
Issue Date:
DOI: https://doi.org/10.1038/nrg733
This article is cited by
-
Evolutionary genetics of pulmonary anatomical adaptations in deep-diving cetaceans
BMC Genomics (2024)
-
Hybridization barriers between the congeneric antarctic notothenioid fish Notothenia coriiceps and Notothenia rossii
Polar Biology (2024)
-
Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella
BMC Ecology and Evolution (2022)
-
Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria
Genome Biology (2022)
-
Sperm membrane proteins DCST1 and DCST2 are required for sperm-egg interaction in mice and fish
Communications Biology (2022)