High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among ten Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes. Sex bias in most sex-biased genes evolved recently and was species-specific. We compared rates of evolutionary change in expression for genes that were sex-biased in one species but unbiased in others and found that sex-biased genes evolved faster in expression than un-biased genes. This greater rate of expression evolution of sex-biased genes, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of sex-biased genes predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.

Transitions to asexuality and evolution of gene expression in Artemia brine shrimp

While sexual reproduction is widespread among many taxa, asexual lineages have repeatedly evolved from sexual ancestors. Despite extensive research on the evolution of sex, it is still unclear whether this switch represents a major transition requiring major molecular reorganization, and how convergent the changes involved are. In this study, we investigated the phylogenetic relationship and patterns of gene expression of sexual and asexual lineages of Eurasian Artemia brine shrimp, to assess how gene expression patterns are affected by the transition to asexuality. We find only a few genes that are consistently associated with the evolution of asexuality, suggesting that this shift may not require an extensive overhauling of the meiotic machinery. While genes with sex-biased expression have high rates of expression divergence within Eurasian Artemia , neither female- nor male-biased genes appear to show unusual evolutionary patterns after sexuality is lost, contrary to theoretical expectations.

Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

X and Y chromosomes in mammals are different in size and gene content due to an evolutionary process of differentiation and degeneration of the Y chromosome. Nevertheless, these chromosomes usually share a small region of homology, the pseudoautosomal region (PAR), which allows them to perform a partial synapsis and undergo reciprocal recombination during meiosis, which ensures their segregation. However, in some mammalian species the PAR has been lost, which challenges the pairing and segregation of sex chromosomes in meiosis. The African pygmy mouse Mus mattheyi shows completely differentiated sex chromosomes, representing an uncommon evolutionary situation among mouse species. We have performed a detailed analysis of the location of proteins involved in synaptonemal complex assembly (SYCP3), recombination (RPA, RAD51 and MLH1) and sex chromosome inactivation (γH2AX) in this species. We found that neither synapsis nor chiasmata are found between sex chromosomes and their pairing is notably delayed compared to autosomes. Interestingly, the Y chromosome only incorporates RPA and RAD51 in a reduced fraction of spermatocytes, indicating a particular DNA repair dynamic on this chromosome. The analysis of segregation revealed that sex chromosomes are associated until metaphase-I just by a chromatin contact. Unexpectedly, both sex chromosomes remain labelled with γH2AX during first meiotic division. This chromatin contact is probably enough to maintain sex chromosome association up to anaphase-I and, therefore, could be relevant to ensure their reductional segregation. The results presented suggest that the regulation of both DNA repair and epigenetic modifications in the sex chromosomes can have a great impact on the divergence of sex chromosomes and their proper transmission, widening our understanding on the relationship between meiosis and the evolution of sex chromosomes in mammals.

Evolutionary dynamics of sex-biased gene expression in a young XY system: Insights from the brown 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.

Preface

This preface introduces the two parts of a theme issue on vertebrate sex chromosome evolution (title below). We invited and edited 22 articles concerning the following main topics (Part 1): sex determination without sex chromosomes and/or governed by epigenetics; origin of sex-determining genes; reasons for differentiation of sex chromosomes and differences in their rates of differentiation as well as (Part 2): co-option of the same linkage groups into sex chromosomes; is differentiation of sex chromosomes a unidirectional pathway?; consequences of differentiated sex chromosomes; differences in differentiation of sex chromosomes under male versus female heterogamety; evolution of sex chromosomes under hybridization and polyploidy. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.