Nonadaptive molecular evolution of seminal fluid proteins in Drosophila

Abstract

Seminal fluid proteins (SFPs) are a group of reproductive proteins that are among the most evolutionarily divergent known. As SFPs can impact male and female fitness, these proteins have been proposed to evolve under postcopulatory sexual selection (PCSS). However, the fast change of the SFPs can also result from nonadaptive evolution, and the extent to which selective constraints prevent SFPs rapid evolution remains unknown. Using intra- and interspecific sequence information, along with genomics and functional data, we examine the molecular evolution of approximately 300 SFPs in Drosophila. We found that 50-57% of the SFP genes, depending on the population examined, are evolving under relaxed selection. Only 7-12% showed evidence of positive selection, with no evidence supporting other forms of PCSS, and 35-37% of the SFP genes were selectively constrained. Further, despite associations of positive selection with gene location on the X chromosome and protease activity, the analysis of additional genomic and functional features revealed their lack of influence on SFPs evolving under positive selection. Our results highlight a lack of sufficient evidence to claim that most SFPs are driven to evolve rapidly by PCSS while identifying genomic and functional attributes that influence different modes of SFPs evolution.

Keywords: Functional attributes; nonadaptive evolution; postcopulatory sexual selection; relaxed selection; selective constraints; seminal fluid proteins.

Figure 1

Mode of evolution of SFP genes. Genes were divided into two groups based on their K _a/K _s ratios relative to the genome average. The eMKT, as well as comparisons of polymorphism (π _a/π _s) and divergence (K _a/K _s), and the frequency distribution of derived alleles (DAF) were used to group genes under three major groups (bold). Significance (sig.) indicates FDR corrected P < 0.05.

Figure 2

Summary statistics for polymorphism and divergence, and modes of evolution, compared between the ancestral (ZI) and derived (RAL) D. melanogaster populations. (A) Average polymorphism (π _a/π _s) and divergence (K _a/K _s) for the genome and SFPs after correcting for covariance between the two estimates. Error bars are 95% confidence intervals. (B) The derived allele frequency spectrum of mean counts of nonsynonymous (Daf0f) and synonymous (Daf4f) polymorphisms in SFP genes with K _a/K _s higher than the genome average and nonsignificant α. (C) The ratio of nonadaptive (ω _na) and adaptive (ω _a) nonsynonymous to synonymous substitutions, respectively. Error bars represent standard error of the mean. Dark‐colored bar: Raleigh population, light‐colored bar: Zambia population. (D) SFP genes modes of evolution in ZI and RAL. Modes of evolution groups are positive selection (orange), relaxed selection (green), and selectively constrained (blue). Numbers are counts per group with colored lines showing movement of genes across group classifications.