The population genetic behavior of mutations in sperm genes is theoretically investigated. We modeled the processes at two levels. One is the standard population genetic process, in which the population allele frequencies change generation by generation, depending on the difference in selective advantages. The other is the sperm competition during each genetic transmission from one generation to the next generation. For the sperm competition process, we formulate the situation where a huge number of sperm with alleles A and B, produced by a single heterozygous male, compete to fertilize a single egg. This "minimal model" demonstrates that a very slight difference in sperm performance amounts to quite a large difference between the alleles' winning probabilities. By incorporating this effect of paternity-sharing sperm competition into the standard population genetic process, we show that fierce sperm competition can enhance the fixation probability of a mutation with a very small phenotypic effect at the singlesperm level, suggesting a contribution of sperm competition to rapid amino acid substitutions in haploid-expressed sperm genes. Considering recent genome-wide demonstrations that a substantial fraction of the mammalian sperm genes are haploid expressed, our model could provide a potential explanation of rapid evolution of sperm genes with a wide variety of functions (as long as they are expressed in the haploid phase). Another advantage of our model is that it is applicable to a wide range of species, irrespective of whether the species is externally fertilizing, polygamous, or monogamous. The theoretical result was applied to mammalian data to estimate the selection intensity on nonsynonymous mutations in sperm genes.
FOR sexual organisms, reproduction is an essential process that allows an individual's genomic information to survive beyond its lifetime. Years ago, it was thought that the functional constraints on genes involved in reproduction should be as strong as those on functionally important genes such as histones, etc. (e.g., Miyata and Yasunaga 1980;Li 1997); hence it was predicted that such genes should evolve much more slowly than average. Therefore, it was a surprise when the first molecular evolutionary analyses on reproduction-related genes (or proteins) revealed their faster than normal evolutionary rates (see, e.g., Swanson et al. 2001; Swanson and Vacquier 2002a,b). Since then, analyses of additional reproductive genes in additional species continue to support the initial observation that reproductive genes evolve more rapidly than the genomic average (e.g., Cutter and Ward 2005;Clark et al. 2006Clark et al. , 2009Ramm et al. 2008;Turner and Hoekstra 2008;Findlay and Swanson 2010; Wong 2011). A common and particularly typical pattern for reproductive genes is a higher ratio, often denoted as d N /d S (= v), of the number of nonsynonymous nucleotide substitutions per nonsynonymous site (d N ) to the number of synonymous nucleotide substitutions per synonymous site (d S ). This pa...