Rapid divergence and diversification of mammalian duplicate gene functions

Abstract

BackgroundGene duplication provides raw material for the evolution of functional innovation. We recently developed a phylogenetic method that classifies evolutionary processes driving the retention of duplicate genes by quantifying divergence between their spatial gene expression profiles and that of their single-copy orthologous gene in a closely related sister species.ResultsHere, we apply our classification method to pairs of duplicate genes in eight mammalian genomes, using data from 11 tissues to construct spatial gene expression profiles. We find that young mammalian duplicates are often functionally conserved, and that expression divergence rapidly increases over evolutionary time. Moreover, expression divergence results in increased tissue specificity, with an overrepresentation of expression in male kidney, underrepresentation of expression in female liver, and strong underrepresentation of expression in testis. Thus, duplicate genes acquire a diversity of new tissue-specific functions outside of the testis, possibly contributing to the origin of a multitude of complex phenotypes during mammalian evolution.ConclusionsOur findings reveal that mammalian duplicate genes are initially functionally conserved, and then undergo rapid functional divergence over evolutionary time, acquiring diverse tissue-specific biological roles. These observations are in stark contrast to the much faster expression divergence and acquisition of broad housekeeping roles we previously observed in Drosophila duplicate genes. Due to the smaller effective population sizes of mammals relative to Drosophila, these analyses implicate natural selection in the functional evolution of duplicate genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0426-x) contains supplementary material, which is available to authorized users.

Evolutionary Fates and Dynamic Functionalization of Young Duplicate Genes in Arabidopsis Genomes

“…Alternatively, the rare cases of subfunctionalization of plant duplicate genes may be due to the stringent criteria of our methodology for identification, which cause some subfunctionalization cases to be classified into conservation and specialization categories. One possible solution might be to conduct the same analysis using expression data from more tissues (Assis and Bachtrog, 2015).…”

Gene duplication and the evolution of phenotypic diversity in insect societies

“…We investigated the evolutionary processes maintaining duplicate genes in A. mellifera (Assis and Bachtrog , ). We found that there were 63 cases of conservation, 28 cases of neofunctionalization (15 of D1 copy, the duplicate with higher sequence similarity to the single copy ortholog, 13 of D2 copy, the duplicate with lower sequence similarity to the single copy ortholog), nine cases of specialization, and no cases of subfunctionalization.…”

“…Interestingly, we identified no cases of subfunctionalization. It is notable that prior studies of this type also found that conservation was one of the most common mechanisms maintaining gene duplicates in mammals and plants (Assis and Bachtrog ; Wang et al. ).…”

Out of the testis, into the ovary: biased outcomes of gene duplication and deletion in Drosophila

“…; Farré and Albà ; Assis and Bachtrog ; Assis ; Assis and Bachtrog ; Jiang and Assis ) divergence that often generates novel (Chen et al. ; Assis and Bachtrog ; Assis ; Assis and Bachtrog ; Jiang and Assis , ) and essential (Holland et al. ; Taylor and Raes ; Liao and Zhang ; Chen et al.…”

“…; Chen et al. ; Farré and Albà ; Assis and Bachtrog ; Assis ; Assis and Bachtrog ; Jiang and Assis ) often diverge soon after duplication, suggesting that any initial redundancy between duplicates is rapidly abolished. Moreover, if duplicate gene functions are in fact redundant, then deleterious effects of the deletion of one copy should be compensated by the presence of another copy.…”