Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila

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.

Figure 1.—

Male SRR genes have fewer detectable orthologs in comparison to female SRR or non-SRR genes. Percentages of D. melanogaster male, SFP, female, FRTP, unbiased, and nonsex and non-SRR genes with detectable orthologs over phylogenetic distance. The total number of D. melanogaster genes in each class is given in parentheses. The representation of the phylogenetic relationship among Drosophila species is according to FlyBase.

Figure 2.—

Higher evolutionary rates of male-specific genes in the melanogaster group. (A) d_S, d_N, and ω estimates of genes expressed in head, ovary, testis, expressed in seminal fluid and female reproductive tract, and involved in spermatogenesis and oogenesis. Error bars represent 95% confidence intervals. T, testis specific; O, ovary specific; TH, testis and head; TO, testis and ovary; H, head specific; OH, ovary and head; TOH, testis, ovary, and head; Sp, spermatogenesis; Oo, oogenesis. (B) Proportion of gene categories among the top 10% of the most rapidly evolving genes. Proportions of genes in each category among the top 10% genes were compared to the initial proportions in the whole data set using a χ² test and a Bonferroni correction. ns, nonsignificant. *P < 0.05, ***P < 0.001. (C) Average d_S and d_N for testis-, ovary-, and head-specific genes across lineages. Testis-specific genes show significantly higher d_N in all lineages (Tukey HSD test, P < 0.001).

Figure 2.—

Higher evolutionary rates of male-specific genes in the melanogaster group. (A) d_S, d_N, and ω estimates of genes expressed in head, ovary, testis, expressed in seminal fluid and female reproductive tract, and involved in spermatogenesis and oogenesis. Error bars represent 95% confidence intervals. T, testis specific; O, ovary specific; TH, testis and head; TO, testis and ovary; H, head specific; OH, ovary and head; TOH, testis, ovary, and head; Sp, spermatogenesis; Oo, oogenesis. (B) Proportion of gene categories among the top 10% of the most rapidly evolving genes. Proportions of genes in each category among the top 10% genes were compared to the initial proportions in the whole data set using a χ² test and a Bonferroni correction. ns, nonsignificant. *P < 0.05, ***P < 0.001. (C) Average d_S and d_N for testis-, ovary-, and head-specific genes across lineages. Testis-specific genes show significantly higher d_N in all lineages (Tukey HSD test, P < 0.001).

Figure 2.—

Higher evolutionary rates of male-specific genes in the melanogaster group. (A) d_S, d_N, and ω estimates of genes expressed in head, ovary, testis, expressed in seminal fluid and female reproductive tract, and involved in spermatogenesis and oogenesis. Error bars represent 95% confidence intervals. T, testis specific; O, ovary specific; TH, testis and head; TO, testis and ovary; H, head specific; OH, ovary and head; TOH, testis, ovary, and head; Sp, spermatogenesis; Oo, oogenesis. (B) Proportion of gene categories among the top 10% of the most rapidly evolving genes. Proportions of genes in each category among the top 10% genes were compared to the initial proportions in the whole data set using a χ² test and a Bonferroni correction. ns, nonsignificant. *P < 0.05, ***P < 0.001. (C) Average d_S and d_N for testis-, ovary-, and head-specific genes across lineages. Testis-specific genes show significantly higher d_N in all lineages (Tukey HSD test, P < 0.001).

Figure 3.—

Lineage-specific evolutionary acceleration of testis-specific, SFP, and spermatogenesis genes. Branch lengths proportional to the number of genes with ω-values significantly higher on the foreground than background branch for genes (A) expressed specifically in head, testis, and ovary, (B) encoding SFPs, (C) encoding FRTPs, and (D) involved in spermatogenesis and oogenesis. Internal branch lengths indicate results for branch tests using the internal branch, as well as all daughter branches. Data are not available for the sim-sec branch.

Figure 4.—

Faster evolution of genes involved in spermatogenesis over genes involved in oogenesis. Average d_N for spermatogenesis (solid) and oogenesis genes (shaded) in different lineages. Genes involved in spermatogenesis show greater average d_N and ω than oogenesis genes in the melanogaster group. This is particularly striking in the more distant members of the melanogaster subgroup.