Abstract
Gene loss and gain during genome evolution are thought to play important roles in adaptive phenotypic diversification. Among mammals, bats possess the smallest genomes and have evolved the unique abilities of powered flight and laryngeal echolocation. To investigate whether gene family evolution has contributed to the genome downsizing and phenotypic diversification in this group, we performed comparative evolutionary analyses of complete proteome data for eight bat species, including echolocating and non-echolocating forms, together with the proteomes of 12 other laurasiatherian mammals. Our analyses revealed extensive gene loss in the most recent ancestor of bats, and also of carnivores (both >1,000 genes), although this gene contraction did not appear to correlate with the reduction in genome size in bats. Comparisons of highly dynamic families suggested that expansion and contraction affected genes with similar functions (immunity, response to stimulus) in all laurasiatherian lineages. However, the magnitude and direction of these changes varied greatly among groups. In particular, our results showed contraction of the Olfactory Receptor (OR) gene repertoire in the last common ancestor of all bats, as well as that of the echolocating species studied. In contrast, non-echolocating fruit bats showed evidence of expansion in ORs, supporting a “trade-off” between sensory modalities.
Highlights
Gene gain and loss are expected to be a major source of genomic variation, and a principal driver of phenotypic diversity[1, 2]
To identify homologous genes and elucidate evolutionary patterns of gene gain and loss in bats, we compared the complete proteomes from 20 laurasiatherian mammals using the Orthologous MAtrix (OMA) algorithm implemented in the OMA standalone software package[17]
We did not find any significantly enriched G-protein coupled receptor activity (GO) terms for expanded genes in the most recent common ancestor (MRCA) of bats after correction for multiple testing (Supplementary Table S6), our analyses indicated that genes encoding proteins with olfactory receptor activity (GO:0004984), including those involved in the sensory perception of smell (GO:0050911), were significantly enriched among contracted Hierarchical Orthologous Groups (HOGs) in bat genomes (Fig. 2, Supplementary Table S7)
Summary
Gene gain and loss are expected to be a major source of genomic variation, and a principal driver of phenotypic diversity[1, 2]. It was previously shown that genome size reduction in bats can be partially attributed to shortened introns and intergenic regions, a trend that is seen in birds[9] In both groups, it has been suggested that genome contraction might be an adaptation for powered flight and its associated high metabolic rates[10]. Despite the large amount of genomic data generated for bats over the past four years[11,12,13], a comprehensive picture of gene gain and loss at a genome scale for the group is still lacking This is mainly because all studies so far have focussed on one or two representative species at a time, or, when encompassing more taxa, have been restricted to specific gene families[14,15,16].
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