Simon Jacobsen Ellerstrand

Sex chromosome evolution is characterized by Y/W degeneration and its consequences for selection on X/Z-linked recessive mutations in the heterogametic sex, yet how functional constraints modulate the evolutionary dynamics of Z–W gametologs remains poorly resolved. We addressed this question in larks (Alaudidae), a lineage carrying enlarged neo-sex chromosomes with multiple evolutionary strata formed through repeated translocations and successive recombination-suppression events. Using whole-genome sequences of males and females of two Alauda species, we analysed 1,759 Z–W gametologs. We found that W-gene degeneration was governed primarily by evolutionary time and intrinsic gene features: long genes were lost earliest, although this tendency was mitigated by gene essentiality, as indicated by high haploinsufficiency scores. Z-linked genes lacking a functional W counterpart exhibited higher nonsynonymous divergence than Z genes retaining a functional W, consistent with selection-driven faster-Z evolution. The strongest signature of purifying selection, comparable to that of pseudoautosomal genes, was observed in haploinsufficient Z-linked genes, which were also more likely to retain W gametologs. Although W genes generally diverged faster, their selection signatures covaried with those of Z and with haploinsufficiency, suggesting partially shared Z–W evolutionary dynamics. Notably, a small subset of W genes showed intensified or positive selection, including several genes associated with putative female-specific functions. Together, our results demonstrate that gene essentiality slows functional divergence on both Z and W, modulates faster-Z dynamics and enables key W genes to remain functional—and potentially advantageous for females—for millions of generations after recombination cessation.

Sex chromosomes are central to many ecological and evolutionary processes. Evidence has accumulated that sex chromosome systems vary extensively in age, turnover and transitions, motivating renewed efforts to study the diversity of sex chromosome systems across the tree of life. However, successful genomic detection of sex chromosomes depends on several factors, including the size and divergence time, background genetic diversity, and the number of sequenced females and males. In addition, technical challenges associated with sequencing and analysing the sex-limited Y/W chromosome remain. Here, we present PhaseWY, an automated Snakemake pipeline that uses whole-genome sequencing data from multiple female and male individuals to identify sex-chromosomal regions and extract the corresponding Y/W sequences. PhaseWY (i) detects sex differences in alignment depth, (ii) applies read-based and statistical haplotype phasing, (iii) identifies sex-linked regions using haplotype clustering, and (iv) subsets autosomal, X/Z- and Y/W-linked variants for downstream analyses. We applied PhaseWY to simulated data to benchmark factors influencing sex-linkage detection and successful extraction of Y/W-linked variants. To demonstrate its practical utility, we further applied PhaseWY to the neo-sex chromosome system in Alauda larks (Alaudidae) and performed a range of downstream analyses demonstrating the scope of applications of the PhaseWY output. We conclude that PhaseWY provides an easy-to-use and reproducible tool for population-genomic analyses in non-model organisms, with particular importance for advancing our understanding of sex-chromosome evolution.

Avian genomes are typically stable, yet instances of chromosome fissions, fusions and translocations are known across various lineages. For example, multiple sex chromosome translocations have been described in the superfamily Sylvioidea. In this study, we examine the sex chromosomes in two Sylvioidea families, Nicatoridae and Cisticolidae, using whole-genome data. We found sex-linkage of chromosomes Z and 4A, consistent with findings in other Sylvioidea species. We also identify sex-linkage of parts of chromosome 4, marking a novel discovery for Nicatoridae and a previously documented feature in Cisticolidae. These families are non-sister taxa, and the size of the translocated region of chromosome 4 differs between them, supporting independent translocation events. We uncover variation in recombination suppression and evolutionary strata on chromosome 4 between families, as well as between two genera within Cisticolidae. This study reveals both recurrent and independent trajectories in sex chromosome evolution, deepening our understanding of complex genomes.

Sex chromosomes often contain recombining pseudoautosomal regions (PARs). Uncovering the dynamics of PAR is crucial for understanding sex chromosome evolution. We analyse PAR dynamics in Sylvioidea songbird neo-sex chromosomes formed by multiple sex chromosome–autosome fusions. We show that the otherwise highly conserved ancestral songbird PAR has stopped recombining independently multiple times when novel PARs formed in the new sex-linked regions. Such PAR transitions were associated with PAR-end fusions, but resulted from subsequent recombination suppression events rather than the fusions themself. We provide support for the hypothesis that episodes of recombination suppression are preceded by sex-associated sequence divergence close to the PAR boundary, and suggest that PAR-end fusions have released the ancestral PAR from constraints in evolving recombination suppression and allowed PAR transitions along the neo-sex chromosomes. This study reveals exceptional PAR diversity among birds and provides novel insights into the process of recombination suppression.

The early evolution of sex chromosomes has remained obscure for more than a century. The Vandiemenella viatica species group of morabine grasshoppers is highly suited for studying the early stages of sex chromosome divergence and degeneration of the Y chromosome. This stems from the fact that neo‐XY sex chromosomes have independently evolved multiple times by X‐autosome fusions with different autosomes. Here, we generated new chromosome‐level assemblies for two chromosomal races representing karyotypes with and without neo‐sex chromosomes (P24XY and P24X0), and sequence data of a third chromosomal race with a different neo‐XY chromosome system (P25XY). Interestingly, these two neo‐XY chromosomal races are formed by different X‐autosome fusions (involving chr1 and chrB, respectively), and we found that both neo‐Y chromosomes have partly ceased to recombine with their neo‐X counterpart. We show that the neo‐XY chromosomes have diverged through accumulation of SNPs and structural mutations, and that many neo‐Y‐linked genes have degenerated since recombination ceased. However, the non‐recombining regions of neo‐Y chromosomes host non‐degenerated genes crucial for sex determination, such as sex‐lethal and transformer, alongside genes associated with spermatogenesis, fertility, and reproduction, illustrating their integrative role as a masculinizing supergene. Contrary to expectations, the neo‐Y chromosomes showed (slightly) lower density of transposable elements (TEs) compared to other genomic regions. The study reveals the unique dynamics of young sex chromosomes, with evolution of recombination suppression and pronounced decay of (some) neo‐sex chromosome genes, and provides a compelling case illustrating how chromosomal fusions and post‐fusion mutational processes contribute to the evolution of supergenes.

The Eurasian spruce bark beetle, Ips typographus, is a major pest, capable of killing spruce forests during large population outbreaks. Recorded dispersal distances of individual beetles are typically within hundreds of meters or a few kilometers. However, the connectivity between populations at larger distances and longer time spans and how this is affected by the habitat is less studied, despite its importance for understanding at which distances local outbreaks may spread. Previous population genetic studies in I. typographus typically used low resolution markers. Here, we use genome‐wide data to assess population structure and connectivity of I. typographus in Sweden. We used 152 individuals from 19 population samples, distributed over 830 km from Strömsund (63° 46′ 8″ N) in the north to Nyteboda (56° 8′ 50″ N) in the south, to capture processes at a large regional scale, and a transect sampling design adjacent to a recent outbreak to capture processes at a smaller scale (76 km). Using restriction site‐associated DNA sequencing (RADseq) markers capturing 1409–1997 SNPs throughout the genome, we document a weak genetic structure over the large scale, potentially indicative of high connectivity with extensive gene flow. No differentiation was detected at the smaller scale. We find indications of isolation‐by‐distance both for relative (F_ST) and absolute divergence (Dxy). The two northernmost populations are most differentiated from the remaining populations, and diverge in parallel to the southern populations for a set of outlier loci. In conclusion, the population structure of I. typographus in Sweden is weak, suggesting a high capacity to disperse and establish outbreak populations in new territories.