Abstract
BackgroundThe primate Y chromosome is distinguished by a lack of inter-chromosomal recombination along most of its length, extensive gene loss, and a prevalence of repetitive elements. A group of genes on the male-specific portion of the Y chromosome known as the “ampliconic genes” are present in multiple copies that are sometimes part of palindromes, and that undergo a form of intra-chromosomal recombination called gene conversion, wherein the nucleotides of one copy are homogenized by those of another. With the aim of further understanding gene family evolution of these genes, we collected nucleotide sequence and gene copy number information for several species of papionin monkey. We then tested for evidence of gene conversion, and developed a novel statistical framework to evaluate alternative models of gene family evolution using our data combined with other information from a human, a chimpanzee, and a rhesus macaque.ResultsOur results (i) recovered evidence for several novel examples of gene conversion in papionin monkeys and indicate that (ii) ampliconic gene families evolve faster than autosomal gene families and than single-copy genes on the Y chromosome and that (iii) Y-linked singleton and autosomal gene families evolved faster in humans and chimps than they do in the other Old World Monkey lineages we studied.ConclusionsRapid evolution of ampliconic genes cannot be attributed solely to residence on the Y chromosome, nor to variation between primate lineages in the rate of gene family evolution. Instead other factors, such as natural selection and gene conversion, appear to play a role in driving temporal and genomic evolutionary heterogeneity in primate gene families.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2187-8) contains supplementary material, which is available to authorized users.
Highlights
The primate Y chromosome is distinguished by a lack of inter-chromosomal recombination along most of its length, extensive gene loss, and a prevalence of repetitive elements
Phylogenetic analysis of the primate male-specific region of the Y chromosome (msrY) Focusing on Old World Primate msrYs, we estimated phylogenetic relationships among msrY sequences from a human, chimp, and rhesus macaque, as well as new sequence data that we collected from several species of papionin monkey
We inferred the paternal relationships among samples from concatenated singleton genes from the msrY, as well as the phylogenetic relationships within individual ampliconic gene (AG) families including pseudogene sequences obtained from completely sequenced msrY from a human, a chimp, and a rhesus macaque (Additional files 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18 and 19)
Summary
The primate Y chromosome is distinguished by a lack of inter-chromosomal recombination along most of its length, extensive gene loss, and a prevalence of repetitive elements. A group of genes on the male-specific portion of the Y chromosome known as the “ampliconic genes” are present in multiple copies that are sometimes part of palindromes, and that undergo a form of intra-chromosomal recombination called gene conversion, wherein the nucleotides of one copy are homogenized by those of another. The evolutionary histories of gene families are trimmed by gene loss and intertwined by non-reciprocal recombination (gene conversion), raising the question of whether and how genomic context influences their evolution. One genomic context of interest is the male-specific region of the Y chromosome (msrY) of placental and marsupial (therian) mammals. The origin of this region coincides with the ascendancy of the SRY gene as the trigger for the male. Examples of gene loss of otherwise conserved Y-linked genes exist, but these are often coupled with translocation to the autosomes or X chromosome [12]
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