Gene Family Evolution across 12 Drosophila Genomes

Matthew W Hahn,Sang-Gook Han,Mira V Han,Gil Mcvean

doi:10.1371/journal.pgen.0030197

Matthew W Hahn, Sang-Gook Han + Show 2 more

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https://doi.org/10.1371/journal.pgen.0030197

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Journal: PLoS Genetics	Publication Date: Nov 1, 2007
Citations: 403	License type: CC BY 4.0

Affiliation: Indiana University Bloomington

Abstract

Comparison of whole genomes has revealed large and frequent changes in the size of gene families. These changes occur because of high rates of both gene gain (via duplication) and loss (via deletion or pseudogenization), as well as the evolution of entirely new genes. Here we use the genomes of 12 fully sequenced Drosophila species to study the gain and loss of genes at unprecedented resolution. We find large numbers of both gains and losses, with over 40% of all gene families differing in size among the Drosophila. Approximately 17 genes are estimated to be duplicated and fixed in a genome every million years, a rate on par with that previously found in both yeast and mammals. We find many instances of extreme expansions or contractions in the size of gene families, including the expansion of several sex- and spermatogenesis-related families in D. melanogaster that also evolve under positive selection at the nucleotide level. Newly evolved gene families in our dataset are associated with a class of testes-expressed genes known to have evolved de novo in a number of cases. Gene family comparisons also allow us to identify a number of annotated D. melanogaster genes that are unlikely to encode functional proteins, as well as to identify dozens of previously unannotated D. melanogaster genes with conserved homologs in the other Drosophila. Taken together, our results demonstrate that the apparent stasis in total gene number among species has masked rapid turnover in individual gene gain and loss. It is likely that this genomic revolving door has played a large role in shaping the morphological, physiological, and metabolic differences among species.

Highlights

A major goal of evolutionary genetics is to understand the molecular changes underlying phenotypic variation within and between species
Our results demonstrate that the apparent stasis in total gene number among species has masked rapid turnover in individual gene gain and loss
Including the two questionable genomes gives k mel 1⁄4 0.0054 and k background 1⁄4 0.0011; excluding these two species gives k mel 1⁄4 0.0050 and k background 1⁄4 0.0010. These analyses demonstrate that the rate of gene turnover inferred in D. melanogaster is likely not an artifact of its relationship to D. sechellia, though the reduced dataset still includes the mosaic assembly of D. simulans

Summary

Introduction

A major goal of evolutionary genetics is to understand the molecular changes underlying phenotypic variation within and between species. The sequencing of whole genomes has made it possible to study not just individual mutations between orthologous sequences, but large-scale differences in gene complements between species Such comparative genomic studies have found large disparities among organisms in the number of copies of genes involved in distinct cellular and developmental processes (e.g., [1,2]) and have even revealed the loss of entire gene families from individual lineages (e.g., [3,4]). Though these studies begin to offer some insight into the molecular basis for phenotypic evolution, the timescales considered are often too long to provide evidence for the role of any single change (but see, e.g., [5,6,7,8]).

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