Summary Sex‐biased gene expression is considered to be an underlying cause of sexually dimorphic traits. Although the nature and degree of sex‐biased expression have been well documented in several animal and plant systems, far less is known about the evolution of sex‐biased genes in more distant eukaryotic groups. Here, we investigate sex‐biased gene expression in two brown algal dioecious species, Fucus serratus and Fucus vesiculosus, where male heterogamety (XX/XY) has recently emerged. We find that in contrast to evolutionary distant plant and animal lineages, male‐biased genes do not experience high turnover rates, but instead reveal remarkable conservation of bias and expression levels between the two species, suggesting their importance in sexual differentiation. Genes with consistent male bias were enriched in functions related to gamete production, along with sperm competition and include three flagellar proteins under positive selection. We present one of the first reports, outside of the animal kingdom, showing that male‐biased genes display accelerated rates of coding sequence evolution compared with female‐biased or unbiased genes. Our results imply that evolutionary forces affect male and female sex‐biased genes differently on structural and regulatory levels, resulting in unique properties of differentially expressed transcripts during reproductive development in Fucus algae.

The sex-dependent regulation of gene expression is considered to be the underlying cause of often extensive, sexually dimorphic traits between males and females. Although the nature and degree of sex-biased gene expression has been well-documented in several animal and plant systems, far less is known about the commonality, conservation, recruitment mechanisms and evolution of sex-biased genes in more distant eukaryotic groups. Brown algae are of particular interest for empirical studies on the evolution of sex-biased gene expression, as they have been evolving independently from animals and plants for over one billion years. Here we focus on two brown algal dioecious species, Fucus serratus and Fucus vesiculosus, where male heterogamety (XX/XY) has recently emerged. Using RNA-seq, we study sex-biased gene expression and discuss different evolutionary forces responsible for the evolution of sex-biased genes. We find that both species evolved masculinized transcriptomes, with sex-biased genes allocated mainly to male reproductive tissue, but virtually absent in vegetative tissues. Conserved male-biased genes were enriched in functions related to gamete production, along with sperm competition and include two flagellar proteins under positive selection. In contrast to female-biased genes, which show high turnover rates, male-biased genes reveal remarkable conservation of bias and expression levels between the two species. As observed in other XY systems, male-biased genes also display accelerated rates of coding sequence evolution compared to female-biased or unbiased genes. Our results imply that evolutionary forces affect male and female sex-biased genes differently on structural and regulatory levels. Similarly to evolutionary distant plant and animal lineages, sex-biased gene expression in Fucus evolved during the transition to dioecy to resolve intra-locus sexual conflict arising from anisogamy.

The genus Fucus dominates the intertidal and shallow subtidal rocky reefs of the North Atlantic and also is commonly found in the intertidal of the North Pacific. It likely diversified 12.2-2.7 mya into two genetically distinct lineages: Lineage 1 with one species in the North Pacific and two in the North Atlantic; and Lineage 2 found only in the North Atlantic (one species recently introduced into the North Pacific). With 10 accepted species, Fucus spp. (and the Fucales) are unique among algae in having a diplontic life cycle, whereby the only haploid stage is the single-celled gamete. Further, Fucus spp. produce eight eggs in each oogonium; have hermaphroditic and dioecious species in each lineage; display sperm:egg ratios differing by more than one order of magnitude; have synchronized and predictable release of gametes; are capable of self- and/or cross- fertilization and asexual (fragmentation via adventitious branching) reproduction; readily hybridize in culture, as well as the field; and form ecads (free-living individuals with morphological variability linked to habitat) by hybridization or polyploidy. Consequently, the genus is an excellent model for a variety of studies in reproductive biology, employing laboratory and field manipulations as well as detailed genetic studies using the molecular ‘omics’. We review here the relevant literature in order to fully understand and appreciate the unique opportunities that Fucus spp. provide as model organisms for future studies of reproduction.

Gene regulation plays an important role in an organism's development and morphological evolution. However, the importance of regulatory divergence in speciation remains unclear. Hybrids between mammalian species often differ in size from their parents due to dramatic parent-of-origin growth effects (Vrana 2007; Brekke and Good 2014;Wolf et al. 2014). The parent-of-origin effects on growth usually manifest in the placenta and embryo development stage, when the embryo is highly sensitive to gene dosage/expression (Haig 1996). It is however, unclear whether this observed pattern of abnormal hybrid growth has a common regulatory basis across mammalian species.According to a long-standing hypothesis for abnormal hybrid growth, a loss of imprinting (LOI) results in the disruption to gene expression in hybrid placentas, leading to an imbalance between paternal and maternal growth factors (Vrana 2007). The predictions of LOI are clear; however, empirical support for this model has been mixed. Additionally, most data supporting the LOI in hybrids have come from a limited number of candidate genes, and the generality of this model remains unclear (Wolf et al. 2014).Hybrids of the closely related dwarf hamster species Phodopus sungorus and Phodopus campbelli show extreme parent-oforigin growth effects. The hybrid formed from a P. sungorus female crossed with a P. campbelli male (SxC) show large placental and embryonic overgrowth and also a range of birth defects that can result in late-term pregnancy failure or maternal death. In the reciprocal hybrids (cxs), this does not occur. By comparing genome-wide patterns of placental expressions between both species and hybrids, researchers can determine if abnormal hybrid growth is associated with disrupted expression and also test the central predictions of the LOI model (Vrana 2007;Wolf et al. 2014). In this study, Brekke and colleagues analyzed placental transcriptomes to evaluate expression levels in the hybrids. They found that many genes (approximately ten percent) are misexpressed in the hybrids relative to the parent species, and that the large hybrid (SxC) has more misexpressed genes than the normal hybrid (cxs). This latter observation suggests that abnormal expression is associated with abnormal growth and is not just a general dysregulation from hybrids of these species.The LOI model predicts a connection between LOI and expression level. For this system, the researchers predicted biallelic expression of paternally expressed genes that promote growth in SxC hybrids. Instead, they found that while there was much biallelic expression in the SxC hybrids, candidateimprinted genes were strongly biased toward maternal expression. Additionally, the researchers found that the expression level of biallelic-expressed genes in SxC was severely reduced overall.These results show that the expression levels and predicted functional roles of both maternally and paternally expressed genes were consistent with the phenotypic patterns of hybrid placental overgrowth, but the results co...

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