Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution

Abstract

Although more than thirty mammalian genomes have been sequenced to draft quality, very few of these include the Y chromosome. This has limited our understanding of the evolutionary dynamics of gene persistence and loss, our ability to identify conserved regulatory elements, as well our knowledge of the extent to which different types of selection act to maintain genes within this unique genomic environment. Here, we present the first MSY (male-specific region of the Y chromosome) sequences from two carnivores, the domestic dog and cat. By combining these with other available MSY data, our multiordinal comparison allows for the first accounting of levels of selection constraining the evolution of eutherian Y chromosomes. Despite gene gain and loss across the phylogeny, we show the eutherian ancestor retained a core set of 17 MSY genes, most being constrained by negative selection for nearly 100 million years. The X-degenerate and ampliconic gene classes are partitioned into distinct chromosomal domains in most mammals, but were radically restructured on the human lineage. We identified multiple conserved noncoding elements that potentially regulate eutherian MSY genes. The acquisition of novel ampliconic gene families was accompanied by signatures of positive selection and has differentially impacted the degeneration and expansion of MSY gene repertoires in different species.[Supplemental material is available for this article.]Y chromosomes have arisen independently in divergent evolutionary lineages across the eukaryotic tree of life

A time- and cost-effective strategy to sequence mammalian Y Chromosomes: an application to the de novo assembly of gorilla Y

“…The sequence of the mammalian male-specific sex chromosomethe Y-is crucial for understanding male infertility disorders , population genetics of male-specific dispersal (Mendez et al 2011;Karmin et al 2015), and male mutation bias (Kuroki et al 2006;Hughes et al 2010Hughes et al , 2012aWilson Sayres et al 2011;Li et al 2013). Despite its importance, the sequence of the Y Chromosome has so far been determined only for a handful of mammals-human, chimpanzee, rhesus macaque, mouse, and pig Hughes et al 2010Hughes et al , 2012aSoh et al 2014;Skinner et al 2016), as well as partially sequenced for bull, dog, cat, marmoset, opossum, and rat (Chang et al 2013;Li et al 2013;Bellott et al 2014).…”

“…Despite its importance, the sequence of the Y Chromosome has so far been determined only for a handful of mammals-human, chimpanzee, rhesus macaque, mouse, and pig Hughes et al 2010Hughes et al , 2012aSoh et al 2014;Skinner et al 2016), as well as partially sequenced for bull, dog, cat, marmoset, opossum, and rat (Chang et al 2013;Li et al 2013;Bellott et al 2014).…”

The pig X and Y Chromosomes: structure, sequence, and evolution

“…These few assemblies, and several partial sequence assemblies, have permitted the elucidation of chromosome topology and gene order in human , chimpanzee (Hughes et al 2010), rhesus macaque (Hughes et al 2012), wallaby (Murtagh et al 2012), mouse (Soh et al 2014), marmoset, rat, and opossum (Bellott et al 2014), cattle (Elsik et al 2009), horse (Paria et al 2011), and cat and dog (Li et al 2013a). These works show divergence in gene content, order, structure, and sequence between Y Chromosomes from different mammalian species.…”

Estimating Tempo and Mode of Y Chromosome Turnover: Explaining Y Chromosome Loss With the Fragile Y Hypothesis

“…As noted in the introduction, frequent turnover in the sex-determining chromosome and or intermittent recombination can promote retention of homomorphic sex chromosomes, but these mechanisms do not apply in species with highly degenerate Xy+ sex chromosomes. Other hypotheses for retention that could apply to the situation in Polyphaga involve purifying selection either due to "essential" male genes or haploinsufficiency (Li et al 2013). Although little is known about the genes present on the Y chromosomes of Coleoptera, it seems unlikely that genes required for male viability are widespread on the Y chromosome, since XO species occur in 24 of 59 Coleoptera families studied, and our estimates indicate that the Y chromosome has been independently lost 69 and 65 times in Polyphaga and Adephaga, respectively (Figure 4).…”