Evolutionary dynamics of sex‐biased gene expression in a young XY system: insights from the brown alga genus Fucus

Abstract

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.

Positive selection and relaxed purifying selection contribute to rapid evolution of male-biased genes in a dioecious flowering plant

“…S8C). So, we obtained ten rapidly evolving tissue-biased genes which were also male-biased in male flower buds, suggesting that elevated evolutionary rates may partly be linked to low pleiotropy, consistent with male-biased genes in Fucus (Hatchett et al, 2023). Finally, gene duplication has long been thought to promote functional divergences and phenotypic novelties by relaxing the constraints of purifying selection on the duplicated gene copy early in its history (Lynch and Conery, 2000; Lynch and Katju, 2004; Lahti et al, 2009).…”

Repeated co-option of HMG-box genes for sex determination in brown algae and animals

“…Initially, we constructed an MSA containing the HMG-sex sequence from Ectocarpus sp. 7 and manually corrected HMGsex sequences from various brown algal species, including Fucus distichus, Fucus spiralis, Dictyota dichotoma, and Undaria pinnatifida (63,(81)(82)(83). The alignment was computed using MAFFT (84).…”

“…We extracted brown algal HMG-box domaincontaining proteins from publicly available genomic resources (63,(81)(82)(83). We searched for putative orthologs of HMG-sex using OrthoFinder (88).…”

“…We manually corrected the gene models of the HMG-sex orthologs using GenomeView (89) to verify that they were complete to assess its structural conservation in different species. We retrieved complete HMG-sex protein sequences for Ectocarpus, Ectocarpus subulatus, Undaria pinnatifida, Fucus distichus, Fucus spiralis, Dictyota dichotoma, and Schizocladia ischiensis (63,(81)(82)(83).…”

Identification of reproductive sex‐biased gene expression in Asparagopsis taxiformis (lineage 6) gametophytes

“…Sex‐biased genes often evolve rapidly, and their differential expression regulates the sexual dimorphism as males and females (Parsch & Ellegren, 2013). In the example of the seaweed Fucus vesiculosus , female‐biased enzyme‐encoding genes associated with carbohydrate modification have been identified and are potentially relevant to cell wall or matrix modification (Hatchett et al., 2023; Martins et al., 2013). Although there is limited knowledge about how sex‐biased or sex‐associated genes are recruited, are regulated, or have evolved over time for seaweeds, these phenomena have been well documented in several animal and plant systems (Scharmann et al., 2021).…”