The evolutionary maintenance of ancient recombining sex chromosomes in the ostrich.

Sex chromosomes have evolved repeatedly across the tree of life and often exhibit extreme size dimorphism due to genetic degeneration of the sex-limited chromosome (e.g. the W chromosome of some birds and Y chromosome of mammals). However, in some lineages, ancient sex-limited chromosomes have escaped degeneration. Here, we study the evolutionary maintenance of sex chromosomes in the ostrich (Struthio camelus), where the W remains 65% the size of the Z chromosome, despite being more than 100 million years old. Using genome-wide resequencing data, we show that the population scaled recombination rate of the pseudoautosomal region (PAR) is higher than similar sized autosomes and is correlated with pedigree-based recombination rate in the heterogametic females, but not homogametic males. Genetic variation within the sex-linked region (SLR) (π = 0.001) was significantly lower than in the PAR, consistent with recombination cessation. Conversely, genetic variation across the PAR (π = 0.0016) was similar to that of autosomes and dependent on local recombination rates, GC content and to a lesser extent, gene density. In particular, the region close to the SLR was as genetically diverse as autosomes, likely due to high recombination rates around the PAR boundary restricting genetic linkage with the SLR to only ~50Kb. The potential for alleles with antagonistic fitness effects in males and females to drive chromosome degeneration is therefore limited. While some regions of the PAR had divergent male-female allele frequencies, suggestive of sexually antagonistic alleles, coalescent simulations showed this was broadly consistent with neutral genetic processes. Our results indicate that the degeneration of the large and ancient sex chromosomes of the ostrich may have been slowed by high recombination in the female PAR, reducing the scope for the accumulation of sexually antagonistic variation to generate selection for recombination cessation.

Digest: Neo-sex chromosome underlying the Faster-Z effect in a species of Lepidoptera.

Do Z chromosomes evolve at a faster rate than autosomes in Lepidoptera? Mongue et al. show that Z-linked genes in two Lepidopteran species evolve faster than autosomal genes. However, the neo-sex chromosome differs from the ancestral chromosome and shows adaptive evolution for genes with a biased expression in the heterogametic sex. These findings indicate that studying molecular evolutionary patterns in sex-linked sequences at different evolutionary stages is essential to understand the dynamics of sex chromosome evolution.

Why Do Some Sex Chromosomes Degenerate More Slowly Than Others? The Odd Case of Ratite Sex Chromosomes.

The hallmark of sex chromosome evolution is the progressive suppression of recombination which leads to subsequent degeneration of the non-recombining chromosome. In birds, species belonging to the two major clades, Palaeognathae (including tinamous and flightless ratites) and Neognathae (all remaining birds), show distinctive patterns of sex chromosome degeneration. Birds are female heterogametic, in which females have a Z and a W chromosome. In Neognathae, the highly-degenerated W chromosome seems to have followed the expected trajectory of sex chromosome evolution. In contrast, among Palaeognathae, sex chromosomes of ratite birds are largely recombining. The underlying reason for maintenance of recombination between sex chromosomes in ratites is not clear. Degeneration of the W chromosome might have halted or slowed down due to a multitude of reasons ranging from selective processes, such as a less pronounced effect of sexually antagonistic selection, to neutral processes, such as a slower rate of molecular evolution in ratites. The production of genome assemblies and gene expression data for species of Palaeognathae has made it possible, during recent years, to have a closer look at their sex chromosome evolution. Here, we critically evaluate the understanding of the maintenance of recombination in ratites in light of the current data. We conclude by highlighting certain aspects of sex chromosome evolution in ratites that require further research and can potentially increase power for the inference of the unique history of sex chromosome evolution in this lineage of birds.

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics.

Sexually antagonistic (SA) genetic variation-in which alleles favored in one sex are disfavored in the other-is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research-including F ST and F IS statistics, genome-wide association studies, pedigree analyses, reciprocal transplant studies, and evolve-and-resequence experiments-to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex F ST and F IS, including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS, along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.

A Genetic Map of Ostrich Z Chromosome and the Role of Inversions in Avian Sex Chromosome Evolution.

Recombination arrest is a necessary step for the evolution of distinct sex chromosomes. Structural changes, such as inversions, may represent the mechanistic basis for recombination suppression and comparisons of the structural organization of chromosomes as given by chromosome-level assemblies offer the possibility to infer inversions across species at some detail. In birds, deduction of the process of sex chromosome evolution has been hampered by the lack of a validated chromosome-level assembly from a representative of one of the two basal clades of modern birds, Paleognathae. We therefore developed a high-density genetic linkage map of the ostrich Z chromosome and used this to correct an existing assembly, including correction of a large chimeric superscaffold and the order and orientation of other superscaffolds. We identified the pseudoautosomal region as a 52 Mb segment (≈60% of the Z chromosome) where recombination occurred in both sexes. By comparing the order and location of genes on the ostrich Z chromosome with that of six bird species from the other major clade of birds (Neognathae), and of reptilian outgroup species, 25 Z-linked inversions were inferred in the avian lineages. We defined Z chromosome organization in an early avian ancestor and identified inversions spanning the candidate sex-determining DMRT1 gene in this ancestor, which could potentially have triggered the onset of avian sex chromosome evolution. We conclude that avian sex chromosome evolution has been characterized by a complex process of probably both Z-linked and W-linked inversions (and/or other processes). This study illustrates the need for validated chromosome-level assemblies for inference of genome evolution.

Old but not (so) degenerated--slow evolution of largely homomorphic sex chromosomes in ratites.

Degeneration of the nonrecombining chromosome is a common feature of sex chromosome evolution, readily evident by the presence of a pair of largely heteromorphic chromosomes, like in eutherian mammals and birds. However, in ratites (order Palaeognathae, including, e.g., ostrich), the Z and W chromosomes are similar in size and largely undifferentiated, despite avian sex chromosome evolution was initiated > 130 Ma. To better understand what may limit sex chromosome evolution, we performed ostrich transcriptome sequencing and studied genes from the nonrecombining region of the W chromosome. Fourteen gametologous gene pairs present on the W chromosome and Z chromosome were identified, with synonymous sequence divergence of 0.027-0.177. The location of these genes on the Z chromosome was consistent with a sequential increase in divergence, starting 110-157 and ending 24-30 Ma. On the basis of the occurrence of Z-linked genes hemizygous in females, we estimate that about one-third of the Z chromosome does not recombine with the W chromosome in female meiosis. Pairwise d(N)/d(S) between gametologs decreased with age, suggesting strong evolutionary constraint in old gametologs. Lineage-specific d(N)/d(S) was consistently higher in W-linked genes, in accordance with the lower efficacy of selection expected in nonrecombining chromosomes. A higher ratio of GC > AT:AT > GC substitutions in W-linked genes supports a role for GC-biased gene conversion in differentially driving base composition on the two sex chromosomes. A male-to-female (M:F) expression ratio of close to one for recombining genes and close to two for Z-linked genes lacking a W copy show that dosage compensation is essentially absent. Some gametologous genes have retained active expression of the W copy in females (giving a M:F ratio of 1 for the gametologous gene pair), whereas for others W expression has become severely reduced resulting in a M:F ratio of close to 2. These observations resemble the patterns of sex chromosome evolution seen in other avian and mammalian lineages, suggesting similar underlying evolutionary processes, although the rate of sex chromosome differentiation has been atypically low. Lack of dosage compensation may be a factor hindering sex chromosome evolution in this lineage.