Academic journal article Genetics

Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila

Academic journal article Genetics

Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila

Article excerpt

ABSTRACT

A large portion of the annotated genes in Drosophila melanogaster show sex-biased expression, indicating that sex and reproduction-related genes (SRR genes) represent an appreciable component of the genome. Previous studies, in which subsets of genes were compared among few Drosophila species, have found that SRR genes exhibit unusual evolutionary patterns. Here, we have used the newly released genome sequences from 12 Drosophila species, coupled to a larger set of SRR genes, to comprehensively test the generality of these patterns. Among 2505 SRR genes examined, including ESTs with biased expression in reproductive tissues and genes characterized as involved in gametogenesis, we find that a relatively high proportion of SRR genes have experienced accelerated divergence throughout the genus Drosophila. Several testis-specific genes, male seminal fluid proteins (SFPs), and spermatogenesis genes show lineage-specific bursts of accelerated evolution and positive selection. SFP genes also show evidence of lineage-specific gene loss and/or gain. These results bring us closer to understanding the details of the evolutionary dynamics of SRR genes with respect to species divergence.

THE spectacular sexual dimorphisms observed in many species of insects, birds, and mammals were originally explained by Charles Darwin to be the result of competition for mates (i.e., sexual selection), which drives the evolution of sex-specific traits (Darwin 1871). Evolutionary biologists have since studied sexual dimorphisms, primarily at the phenotypic level, across a wide variety of species (Eberhard 1985; Andersson 1994; Möller 1994; Houde 1997; Markow 2002). With the advent of molecular techniques in the 1980s and their application in examining gene evolutionamong species, a pattern of rapid divergence of genes with sex-specific expression began to emerge (Coulthart and Singh 1988; Thomas and Singh 1992; Civetta and Singh 1995). We have since learned that sexual selection can influencenotonly theevolutionofmorphological sexual dimorphism but also the patterns and rates of molecular evolution and speciation (Civetta and Singh 1998a; Singh and Kulathinal 2000; Swanson et al. 2001; Swanson andVacquier 2002;Coyne andOrr 2004). In Drosophila, sexual dimorphism occurs atmorphological (e.g., body size, genitalia, abdomen pigmentation, sex combs in males but not females), behavioral (e.g., courtship and postmating behaviors), and molecular levels (e.g., yolk proteins and seminal fluid proteins) (see Markow 2002 for review). Interest in the evolution of sexual dimorphism at the molecular level and its consequences has received renewed attention with the recent reports that over half of the genes in Drosophila melano-gaster and D. simulans exhibit sexually dimorphic expression (Ranz et al. 2003; Parisi et al. 2004). Within these sex-biasedgenes, those withmale-biased expressiontend to show greater difference in expression levels than do female-biased genes or non-sex-biased genes in both within- and between-species comparisons (Meiklejohn et al. 2003; Parisi et al. 2003, 2004; Ranz et al. 2003). In addition, rates of sequence evolution of sex and reproduction-related (SRR) and non-SRR genes differ quite dramatically: male and female SRR genes evolve faster than non-SRR genes (Begun et al. 2000; Swanson et al. 2001; Zhang et al. 2004; Jagadeeshan and Singh 2005;Mueller et al.2005;Proschel et al.2006;L awniczak and Begun 2007; see Swanson and Vacquier 2002 for review).

Despite the importance of these conclusions, their generality remains questionable, as previous studies examined sequence divergence within a limited set of genes in a small number of species. Such studies reported that genes expressed in the testis and genes encoding seminal fluid proteins include many that evolve rapidly (Begun et al. 2000, 2006; Swanson et al. 2001; Holloway and Begun 2004; Kern et al. 2004; Z hang et al. 2004; Begun and Lindfors 2005; Mueller et al. …

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