Sexual Dimorphism and the Evolution of Sex-Biased Gene Expression in the Brown Alga Ectocarpus

Abstract

Males and females often have marked phenotypic differences, and the expression of these dissimilarities invariably involves sex differences in gene expression. Sex-biased gene expression has been well characterized in animal species, where a high proportion of the genome may be differentially regulated in males and females during development. Male-biased genes tend to evolve more rapidly than female-biased genes, implying differences in the strength of the selective forces acting on the two sexes. Analyses of sex-biased gene expression have focused on organisms that exhibit separate sexes during the diploid phase of the life cycle (diploid sexual systems), but the genetic nature of the sexual system is expected to influence the evolutionary trajectories of sex-biased genes. We analyze here the patterns of sex-biased gene expression in Ectocarpus, a brown alga with haploid sex determination (dioicy) and a low level of phenotypic sexual dimorphism. In Ectocarpus, female-biased genes were found to be evolving as rapidly as male-biased genes. Moreover, genes expressed at fertility showed faster rates of evolution than genes expressed in immature gametophytes. Both male- and female-biased genes had a greater proportion of sites experiencing positive selection, suggesting that their accelerated evolution is at least partly driven by adaptive evolution. Gene duplication appears to have played a significant role in the generation of sex-biased genes in Ectocarpus, expanding previous models that propose this mechanism for the resolution of sexual antagonism in diploid systems. The patterns of sex-biased gene expression in Ectocarpus are consistent both with predicted characteristics of UV (haploid) sexual systems and with the distinctive aspects of this organism's reproductive biology.

Multiple gene movements into and out of haploid sex chromosomes

“…Evolutionary rates can be affected by gene expression pattern, in particular breadth of expression [31, 32]. We therefore also compared the dN/dS ratios of sex-linked genes with those of sex-biased genes, because the latter exhibit narrow (sex-specific) expression patterns similar to those observed for SDR genes [33]. Evolutionary rates for SDR genes were comparable to those for sex-biased autosomal genes (Wilcoxon test, p  = 0.19501) but dS values were significantly lower for SDR genes (Wilcoxon test, p  = 0.00017) (Fig.…”

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

“…Although this is somewhat different than work in Drosophila and mammals, where only male-biased genes show elevated rates of evolution (Ellegren and Parsch 2007; Zhang et al 2007; Parsch and Ellegren 2013), it does add to the diversity of patterns observed in other taxa. For example, female-biased genes show more rapid rates of evolution in Neurospora crassa (Whittle and Johannesson 2013), and both male- and female-biased genes show elevated rates of evolution in brown alga (Lipinska et al 2015). …”

“…It is often assumed that the majority of sexually dimorphic traits arise from differences in expression for genes present in both sexes (Connallon and Knowles 2005; Rinn and Snyder 2005). In line with this, studies in a wide array of organisms have attempted to determine the differences in gene expression between males and females (Parsch and Ellegren 2013), including Drosophila (Assis et al 2012; Perry et al 2014), birds (Pointer et al 2013), nematodes (Albritton et al 2014), and brown alga (Lipinska et al 2015). These works have revealed that a significant fraction of genes in the genome exhibit differential expression between males and females (Rinn and Snyder 2005; Mank, Hultin-Rosenberg, Webster, et al 2008; Reinius et al 2008; Jiang and Machado 2009), which suggests that the expression of sexual dimorphism is related to marked genetic reprogramming (Lipinska et al 2015).…”

“…In Drosophila and mammals, male-biased genes show elevated rates of evolution (Khaitovich et al 2005; Assis et al 2012), however fungi show elevated rates of evolution for female-biased genes (Whittle and Johannesson 2013). Both male- and female-biased genes in brown alga show elevated rates of evolution (Lipinska et al 2015). Finally, in birds, genes that are female-biased in late development show higher rates of evolution than male-biased adult-expressed genes, although both categories show higher rates of evolution than unbiased genes (Mank et al 2010).…”

The Ectocarpus IMMEDIATE UPRIGHT gene encodes a member of a novel family of cysteine-rich proteins with an unusual distribution across the eukaryotes

“…To compare the EsV-1-7 proteins with known fast-evolving proteins, a similar analysis was then carried out with a set of 905 Ectocarpus sp. sex-biased genes that have one-to-one orthologues in S. japonica (Lipinska et al, 2015). The statistical significance of differences between datasets was evaluated with a Wilcoxon test and bootstrap resampling with replacement (10,000 replicates).…”