Ancient U/V sex chromosomes reveal slow expansion of recombination suppression in Polytrichaceae mosses.

Abstract

Sex chromosomes evolving in haploid versus diploid life cycles provide complementary systems for testing theories of sex chromosome evolution, yet haploid sex chromosomes remain poorly studied. In dioicous bryophytes, females and males carry non-recombining U and V chromosomes, respectively, providing a unique opportunity to examine the consequences of long-term recombination suppression independently of diploid heterogamety. Here, we characterize the U/V sex chromosomes of Polytrichaceae using chromosome-scale genomes from ten species. We identify homologous U/V chromosomes across the family and show that their non-recombining sex-determining regions (SDRs) originated early in Polytrichaceae evolution, approximately 124 million years ago. Despitetheir ancient origin, however, the SDRs have undergone limited expansion and are consistently flanked by large pseudoautosomal regions (PARs). The SDRs nevertheless show strong genomic signatures of recombination suppression, including reduced gene density, transposable-element accumulation, reduced diversity, high synonymous divergence, and altered codon usage. Yet they retain hundreds of genes and show limited evidence of functional degeneration. Their gene content is dynamic, with frequent lineage-specific gains and losses, while a conserved core of 60 orthogroups has persisted across all ten species for more than 100 million years. Comparisons across sex chromosome systems suggest that haploid U/V chromosomes retain more genes than similarly old diploid X/Y or Z/W chromosomes, consistent with a role for haploid selection in limiting degeneration. However, haploid selection alone cannot explain the limited SDR expansion observed in Polytrichaceae, suggesting that other factors also shape SDR evolution. Together, these results reveal an ancient U/V system in which recombination suppression has strong genomic consequences but has not driven extensive SDR expansion or functional degeneration. By decoupling recombination suppression from diploid heterogamety, U/V chromosomes provide a powerful framework for distinguishing the consequences of recombination arrest from those of ploidy in sex chromosome evolution.