Rare recombination in Salix nivalis and the maintenance of homomorphic sex chromosomes in willows

Premise

Most dioecious angiosperms have homomorphic sex chromosomes, and non-recombining sex-linked regions (SLRs) likely comprise a small portion of the sex chromosome. The fountain of youth hypothesis posits that rare recombination within heterogametic SLRs may act to maintain homomorphy. Alternatively, turnovers of the sex-determining genes could also contribute to sex chromosome homomorphy.

Methods

We used reduced representation sequencing and mapping to the Salix purpurea reference genome to determine the size of the sex-linked region in three dwarf willows (Salix phlebophylla, S. reticulata, and S. nivalis). To test the fountain of youth hypotheses, we performed allelic state and linkage disequilibrium (LD) analyses.

Results

For all three species, sex-linked single nucleotide polymorphisms (SNPs) were identified on chromosome 15. Mean heterozygosity was higher in females, confirming that all three species were female heterogametic (ZW). A recombinant haplotype between the Z and W chromosomes was identified in S. nivalis, contributing to higher-than-expected mean heterozygosity in SLR and slow LD decay in males.

Conclusions

We propose that the uncommon ZW haplotype resulting from a recombination event identified here initiates the homogenization of Z and W chromosomes, leading to the maintenance of their homomorphy. Based on comparisons across all three SLRs, we further speculate that ongoing rare recombination events have influenced the shared patterns of sex-linked SNPs across S. phlebophylla, S. reticulata, and S. nivalis and is a process that influences sex chromosome evolution throughout the Salicaceae and flowering plants with homomorphic sex chromosomes.