The Y Chromosome is a Reliable Marker for Deep-Time Phylogenetic Inference

The Y chromosome has been omitted from almost all phylogenomic analyses to date due to its complex structure, which makes accurate assembly and alignment across species challenging. Yet the Y chromosome is, in theory, an optimal phylogenetic marker. Y-chromosomal genes have a smaller effective population size than autosomal genes, reducing the likelihood of incomplete lineage sorting. Likewise, heterogametic hybrid offspring of different species are generally sterile, creating a barrier to Y-chromosomal gene flow. To overcome difficulties in using the Y chromosome, we developed a novel approach to identify orthologous Y-linked sequences in placental mammals, enabling us to generate a 63-species Y-chromosome alignment. We aligned ∼80 kilobases of predominantly non-coding sequence from conserved genes that are broadly expressed regulators of protein synthesis and spermatogenesis - the X-degenerate genes. Our phylogenetic reconstructions demonstrate that noncoding X-degenerate gene sequences recapitulate the same phylogeny derived from genome-wide noncoding, neutrally evolved sequences across the biparentally inherited autosomes and the X chromosome. We find strong support for the superordinal clades Euarchonta, Scrotifera, Fereuungulata, and Zooamata - groupings that have been historically considered controversial. Our results demonstrate that not only can the Y chromosome be aligned across species divergences spanning more than 100 million years, but it also performs robustly in a comparative phylogenetic context. We also present evidence that interchromosomal gene conversion between the non-recombining ZFX and ZFY genes has independently occurred in multiple lineages. ZFY has a proposed function as a meiotic executioner, and interchromosomal gene conversion may serve as a compensatory mechanism to prevent genetic decay of this essential gene.