Most genes linked to male reproductive function have been known to evolve rapidly among species and to show signatures of positive selection. Different male species-specific reproductive strategies have been proposed to underlie positive selection, such as sperm competitive advantage and control over females postmating physiology. However, an underexplored aspect potentially affecting male reproductive gene evolution in mammals is the effect of gene duplications. Here we analyze the molecular evolution of members of the izumo gene family in mammals, a family of four genes mostly expressed in the sperm with known and potential roles in sperm-egg fusion. We confirm a previously reported bout of selection for izumo1 and establish that the bout of selection is restricted to the diversification of species of the superorder Laurasiatheria. None of the izumo genes showed evidence of positive selection in Glires (Rodentia and Lagomorpha), and in the case of the non-testes-specific izumo4, rapid evolution was driven by relaxed selection. We detected evidence of positive selection for izumo3 among Primates. Interestingly, positively selected sites include several serine residues suggesting modifications in protein function and/or localization among Primates. Our results suggest that positive selection is driven by aspects related to species-specific adaptations to fertilization rather than sexual selection. 1. Introduction Molecular evolutionary analysis of protein coding genes show that most genes evolve under purifying selection with few exceptions of rapid change between species driven by positive selection [1, 2]. One class of rapidly evolving genes are those linked to reproduction, and in many cases positive selection has been found to drive their evolution towards species-specific adaptations. Broad-sense sexual selection [3] can lead to rapid evolution of primary sexual traits and genes that function largely to improve reproductive success, thus sexual selection has been suggested as an explanation for the rapid adaptive diversification of reproductive proteins. In mammals, many male reproductive genes have shown evidence of rapid evolution driven by positive selection [4–6]. It has been more difficult, however, to link positive selection to sexual selection, and numerous hypotheses have been proposed to explain this difficulty [7, 8]. One possible explanation is that most genes in mammals are members of gene families that have experienced several rounds of gene duplication. After duplication, genes can follow different paths in terms of their evolutionary
References
[1]
W. H. Li, Molecular Evolution, Sinauer Associates, Sunderland, Mass, USA, 1997.
[2]
E. V. Koonin and Y. I. Wolf, “Constraints and plasticity in genome and molecular-phenome evolution,” Nature Reviews Genetics, vol. 11, no. 7, pp. 487–498, 2010.
[3]
A. Civetta and R. S. Singh, “Broad-sense sexual selection, sex gene pool evolution, and speciation,” Genome, vol. 42, no. 6, pp. 1033–1041, 1999.
[4]
W. J. Swanson and V. D. Vacquier, “The rapid evolution of reproductive proteins,” Nature Reviews Genetics, vol. 3, no. 2, pp. 137–144, 2002.
[5]
W. J. Swanson, R. Nielsen, and Q. Yang, “Pervasive adaptive evolution in mammalian fertilization proteins,” Molecular Biology and Evolution, vol. 20, no. 1, pp. 18–20, 2003.
[6]
L. M. Turner and H. E. Hoekstra, “Causes and consequences of the evolution of reproductive proteins,” International Journal of Developmental Biology, vol. 52, no. 5-6, pp. 769–780, 2008.
[7]
A. Wong, “The molecular evolution of animal reproductive tract proteins: what have we learned from mating-system comparisons?” International Journal of Evolutionary Biology, vol. 2011, Article ID 908735, 9 pages, 2011.
[8]
A. Civetta, “Fast evolution of reproductive genes: when is selection sexual?” in Rapidly Evolving Genes and Genetic Systems, R. S. Singh, J. Xu, and R. J. Kulathinal, Eds., pp. 165–175, Oxford University Press, Oxford, UK, 2012.
[9]
M. Lynch and J. S. Conery, “The evolutionary fate and consequences of duplicate genes,” Science, vol. 290, no. 5494, pp. 1151–1155, 2000.
[10]
S. Dorus, E. R. Wasbrough, J. Busby, E. C. Wilkin, and T. L. Karr, “Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes,” Molecular Biology and Evolution, vol. 27, no. 6, pp. 1235–1246, 2010.
[11]
S. A. Ramm, P. L. Oliver, C. P. Ponting, P. Stockley, and R. D. Emes, “Sexual selection and the adaptive evolution of mammalian ejaculate proteins,” Molecular Biology and Evolution, vol. 25, no. 1, pp. 207–219, 2008.
[12]
T. D. O'Connor and N. I. Mundy, “Genotype-phenotype associations: substitution models to detect evolutionary associations between phenotypic variables and genotypic evolutionary rate,” Bioinformatics, vol. 25, no. 12, pp. i94–i100, 2009.
[13]
S. B. Kingan, M. Tatar, and D. M. Rand, “Reduced polymorphism in the chimpanzee semen coagulating protein, semenogelin I,” Journal of Molecular Evolution, vol. 57, no. 2, pp. 159–169, 2003.
[14]
S. J. Carnahan and M. I. Jensen-Seaman, “Hominoid seminal protein evolution and ancestral mating behavior,” American Journal of Primatology, vol. 70, no. 10, pp. 939–948, 2008.
[15]
B. Glassey and A. Civetta, “Positive selection at reproductive ADAM genes with potential intercellular binding activity,” Molecular Biology and Evolution, vol. 21, no. 5, pp. 851–859, 2004.
[16]
S. Finn and A. Civetta, “Sexual selection and the molecular evolution of ADAM proteins,” Journal of Molecular Evolution, vol. 71, no. 3, pp. 231–240, 2010.
[17]
N. Inoue, M. Ikawa, A. Isotani, and M. Okabe, “The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs,” Nature, vol. 434, no. 7030, pp. 234–238, 2005.
[18]
D. A. Ellerman, J. Pei, S. Gupta, W. J. Snell, D. Myles, and P. Primakoff, “Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm,” Molecular Reproduction and Development, vol. 76, no. 12, pp. 1188–1199, 2009.
[19]
J. D. Thompson, D. G. Higgins, and T. J. Gibson, “CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice,” Nucleic Acids Research, vol. 22, no. 22, pp. 4673–4680, 1994.
[20]
F. Abascal, R. Zardoya, and D. Posada, “ProtTest: selection of best-fit models of protein evolution,” Bioinformatics, vol. 21, no. 9, pp. 2104–2105, 2005.
[21]
K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011.
[22]
J. Felsenstein, “Confidence limits on phylogenies: an approach using the bootstrap,” Evolution, vol. 39, no. 4, pp. 783–791, 1985.
[23]
Z. Yang, “PAML: a program package for phylogenetic analysis by maximum likelihood,” Computer Applications in the Biosciences, vol. 13, no. 5, pp. 555–556, 1997.
[24]
Z. Yang, “PAML 4: phylogenetic analysis by maximum likelihood,” Molecular Biology and Evolution, vol. 24, no. 8, pp. 1586–1591, 2007.
[25]
W. S. W. Wong, Z. Yang, N. Goldman, and R. Nielsen, “Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites,” Genetics, vol. 168, no. 2, pp. 1041–1051, 2004.
[26]
Z. Yang, W. S. W. Wong, and R. Nielsen, “Bayes empirical Bayes inference of amino acid sites under positive selection,” Molecular Biology and Evolution, vol. 22, no. 4, pp. 1107–1118, 2005.
[27]
D. T. Jones, W. R. Taylor, and J. M. Thornton, “The rapid generation of mutation data matrices from protein sequences,” Computer Applications in the Biosciences, vol. 8, no. 3, pp. 275–282, 1992.
[28]
S. Kumar and S. B. Hedges, “Timetree2: species divergence times on the iPhone,” Bioinformatics, vol. 27, no. 14, pp. 2023–2024, 2011.
[29]
N. Inoue, T. Kasahara, M. Ikawa, and M. Okabe, “Identification and disruption of sperm-specific angiotensin converting enzyme-3 (ACE3) in mouse,” PLoS ONE, vol. 5, no. 4, Article ID e10301, 2010.
[30]
M. Lynch and A. Force, “The probability of duplicate gene preservation by subfunctionalization,” Genetics, vol. 154, no. 1, pp. 459–473, 2000.
