Unraveling the effect of genomic structural changes in the rhesus macaque - implications for the adaptive role of inversions

Abstract

BackgroundBy reshuffling genomes, structural genomic reorganizations provide genetic variation on which natural selection can work. Understanding the mechanisms underlying this process has been a long-standing question in evolutionary biology. In this context, our purpose in this study is to characterize the genomic regions involved in structural rearrangements between human and macaque genomes and determine their influence on meiotic recombination as a way to explore the adaptive role of genome shuffling in mammalian evolution.ResultsWe first constructed a highly refined map of the structural rearrangements and evolutionary breakpoint regions in the human and rhesus macaque genomes based on orthologous genes and whole-genome sequence alignments. Using two different algorithms, we refined the genomic position of known rearrangements previously reported by cytogenetic approaches and described new putative micro-rearrangements (inversions and indels) in both genomes. A detailed analysis of the rhesus macaque genome showed that evolutionary breakpoints are in gene-rich regions, being enriched in GO terms related to immune system. We also identified defense-response genes within a chromosome inversion fixed in the macaque lineage, underlying the relevance of structural genomic changes in evolutionary and/or adaptation processes. Moreover, by combining in silico and experimental approaches, we studied the recombination pattern of specific chromosomes that have suffered rearrangements between human and macaque lineages.ConclusionsOur data suggest that adaptive alleles – in this case, genes involved in the immune response – might have been favored by genome rearrangements in the macaque lineage.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-530) contains supplementary material, which is available to authorized users.

An Integrative Breakage Model of genome architecture, reshuffling and evolution

“…Certain changes in gene expression could reflect a selective advantage, but empirical data are weak. On the one hand, it has been reported that EBRs co-localize with genes related to the immune system [18,30,53], suggesting the connection between EBRs and the development of new adaptive characters may be specific to mammalian lineages. On the other hand, studies in Drosophila have shown both changes in gene expression levels resulting from GR [54] and a high number of gene alterations at breakpoints in D. mojavensis [55], all with putative adaptive consequences.…”

Mammalian Meiotic Recombination: A Toolbox for Genome Evolution

“…In the case of inversions, direct evidence has been provided by cytogenetic studies in mammals [Ashley et al, 1981;Greenbaum and Reed, 1984;Ullastres et al, 2014] and Drosophila [Navarro et al, 1997]. Boro-din et al [2008] detected a reduction in CO frequency in translocated chromosomes of the common shrew, whereas others reported a reduction in both chiasmata number and COs in house mice due to Robertsonian translocations [Castiglia and Capanna, 2002;Dumas and BrittonDavidian, 2002;Capilla et al, 2014].…”

Recombination Suppression is Unlikely to Contribute to Speciation in SympatricHeliconiusButterflies

“…Drosophila melanogaster [7,8], D. pseudoobscura [9,10] and Anopheles mosquitoes [11,12]) fish (e.g. sticklebacks [13] and cod [14,15]), birds [16], and mammals [17,18], as well as in plants (e.g.…”