Ecology and the Evolution of Sex Chromosomes

This article reviews and discusses ecological factors that affect sex chromosome evolution. Sex chromosomes are common features of animal genomes, and are often the location where master sex determination genes are found. Many important aspects of sex chromosome evolution are thought to be driven by sex-specific selection pressures, such as sexual antagonism and sexual selection. Sex-specific selection affects both the formation of sex chromosomes from autosomes and differences in the evolutionary trajectories between sex chromosomes and autosomes. Most population genetic models are agnostic as to whether the sex-specific selection pressures arise from intrinsic features of organismal biology or extrinsic factors that depend on environment. Here, I review the evidence that extrinsic, or ecological, factors are important determinants of sex-specific selection pressures that shape sex chromosome evolution.

Dynamic Patterns of Sex Chromosome Evolution in Neognath Birds: Many Independent Barriers to Recombination at the ATP5F1A Locus

Avian sex chromosomes evolved after the divergence birds and crocodilians from their common ancestor, so they are much younger than the better-studied chromosomes of mammals. It has long been recognized that there may have been several stages to the evolution of avian sex chromosomes. For example, the CHD1 undergoes recombination in paleognaths but not neognaths. Genome assemblies have suggested there may be variation in the timing of barriers to recombination among Neognathae, but there remains little understanding of the extent of this variability. Here, we look at partial sequences of ATP5F1A, which is on the avian Z and W chromosomes. It is known that recombination of this gene has independently ceased in Galliformes, Anseriformes, and at least five neoavian orders, but whether there are other independent cessations of recombination among Neoaves is not understood. We used a combination of data extracted from published chromosomal-level genomes with data collected using PCR and cloning to identify Z and W copies in 22 orders. Our results suggest there may be at least 19 independent cessations of recombination within Neognathae, and 3 clades that may still be undergoing recombination (or have only recently ceased recombination). Analyses of ATP5F1A protein sequences revealed an increased amino acid substitution rate for W chromosome gametologs, suggesting relaxed purifying selection on the W chromosome. Supporting this hypothesis, we found that the increased substitution rate was particularly pronounced for buried residues, which are expected to be more strongly constrained by purifying selection. This highlights the dynamic nature of avian sex chromosomes, and that this level of variation among clades means they should be a good system to understand sex chromosome evolution.

Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

DNA methylation is involved in sexual differentiation and sex chromosome evolution in the dioecious plant garden asparagus

DNA methylation is a crucial regulatory mechanism in many biological processes. However, limited studies have dissected the contribution of DNA methylation to sexual differentiation in dioecious plants. In this study, we investigated the variances in methylation and transcriptional patterns of male and female flowers of garden asparagus. Compared with male flowers, female flowers at the same stages showed higher levels of DNA methylation. Both male and female flowers gained DNA methylation globally from the premeiotic to meiotic stages. Detailed analysis revealed that the increased DNA methylation was largely due to increased CHH methylation. Correlation analysis of differentially expressed genes and differentially methylated regions suggested that DNA methylation might not have contributed to the expression variation of the sex-determining genes SOFF and TDF1 but probably played important roles in sexual differentiation and flower development of garden asparagus. The upregulated genes AoMS1, AoLAP3, AoAMS, and AoLAP5 with varied methylated CHH regions might have been involved in sexual differentiation and flower development of garden asparagus. Plant hormone signaling genes and transcription factor genes also participated in sexual differentiation and flower development with potential epigenetic regulation. In addition, the CG and CHG methylation levels in the Y chromosome were notably higher than those in the X chromosome, implying that DNA methylation might have been involved in Y chromosome evolution. These data provide insights into the epigenetic modification of sexual differentiation and flower development and improve our understanding of sex chromosome evolution in garden asparagus.

Lizards as Model Organisms of Sex Chromosome Evolution: What We Really Know from A Systematic Distribution of Available Data?

Lizards represent unique model organisms in the study of sex determination and sex chromosome evolution. Among tetrapods, they are characterized by an unparalleled diversity of sex determination systems, including temperature-dependent sex determination (TSD) and genetic sex determination (GSD) under either male or female heterogamety. Sex chromosome systems are also extremely variable in lizards. They include simple (XY and ZW) and multiple (X1X2Y and Z1Z2W) sex chromosome systems and encompass all the different hypothesized stages of diversification of heterogametic chromosomes, from homomorphic to heteromorphic and completely heterochromatic sex chromosomes. The co-occurrence of TSD, GSD and different sex chromosome systems also characterizes different lizard taxa, which represent ideal models to study the emergence and the evolutionary drivers of sex reversal and sex chromosome turnover. In this review, we present a synthesis of general genome and karyotype features of non-snakes squamates and discuss the main theories and evidences on the evolution and diversification of their different sex determination and sex chromosome systems. We here provide a systematic assessment of the available data on lizard sex chromosome systems and an overview of the main cytogenetic and molecular methods used for their identification, using a qualitative and quantitative approach.

Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?

Sex chromosomes are a great example of a convergent evolution at the genomic level, having evolved dozens of times just within amniotes. An intriguing question is whether this repeated evolution was random, or whether some ancestral syntenic blocks have significantly higher chance to be co-opted for the role of sex chromosomes owing to their gene content related to gonad development. Here, we summarize current knowledge on the evolutionary history of sex determination and sex chromosomes in amniotes and evaluate the hypothesis of non-random emergence of sex chromosomes. The current data on the origin of sex chromosomes in amniotes suggest that their evolution is indeed non-random. However, this non-random pattern is not very strong, and many syntenic blocks representing putatively independently evolved sex chromosomes are unique. Still, repeatedly co-opted chromosomes are an excellent model system, as independent co-option of the same genomic region for the role of sex chromosome offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and gene identity. Future studies should use these systems more to explore the convergent/divergent evolution of sex chromosomes. 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 II)’.

Sex chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog

Sex chromosomes generally evolve from a homomorphic to heteromorphic state. Once a heteromorphic system is established, the sex chromosome system may remain stable for an extended period. Here, we show the opposite case of sex chromosome evolution from a heteromorphic to a homomorphic system in the Japanese frog Glandirana rugosa. One geographic group, Neo-ZW, has ZZ-ZW type heteromorphic sex chromosomes. We found that its western edge populations, which are geographically close to another West-Japan group with homomorphic sex chromosomes of XX-XY type, showed homozygous genotypes of sex-linked genes in both sexes. Karyologically, no heteromorphic sex chromosomes were identified. Sex-reversal experiments revealed that the males were heterogametic in sex determination. In addition, we identified another similar population around at the southwestern edge of the Neo-ZW group in the Kii Peninsula: the frogs had homomorphic sex chromosomes under male heterogamety, while shared mitochondrial haplotypes with the XY group, which is located in the east and bears heteromorphic sex chromosomes. In conclusion, our study revealed that the heteromorphic sex chromosome systems independently reversed back to or turned over to a homomorphic system around each of the western and southwestern edges of the Neo-ZW group through hybridization with the West-Japan group bearing homomorphic sex chromosomes. 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 II)’.

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. 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 II)’.