Patterns of positive selection in seven ant genomes.

Julien Roux,Josephine T Daub,Marc Robinson-Rechavi,Eyal Privman,Laurent Keller,Sébastien Moretti

doi:10.1093/molbev/msu141

Abstract

The evolution of ants is marked by remarkable adaptations that allowed the development of very complex social systems. To identify how ant-specific adaptations are associated with patterns of molecular evolution, we searched for signs of positive selection on amino-acid changes in proteins. We identified 24 functional categories of genes which were enriched for positively selected genes in the ant lineage. We also reanalyzed genome-wide data sets in bees and flies with the same methodology to check whether positive selection was specific to ants or also present in other insects. Notably, genes implicated in immunity were enriched for positively selected genes in the three lineages, ruling out the hypothesis that the evolution of hygienic behaviors in social insects caused a major relaxation of selective pressure on immune genes. Our scan also indicated that genes implicated in neurogenesis and olfaction started to undergo increased positive selection before the evolution of sociality in Hymenoptera. Finally, the comparison between these three lineages allowed us to pinpoint molecular evolution patterns that were specific to the ant lineage. In particular, there was ant-specific recurrent positive selection on genes with mitochondrial functions, suggesting that mitochondrial activity was improved during the evolution of this lineage. This might have been an important step toward the evolution of extreme lifespan that is a hallmark of ants.

Highlights

Ants constitute an extremely successful lineage of animals which has colonized virtually all ecosystems on Earth (Holldobler and Wilson 1990)
To detect positive selection episodes that acted on proteincoding genes during the evolution of the ant lineage, the branch-site test of Codeml was run on 4,261 protein alignments of single-copy orthologs composed of four to seven ant and three to five outgroup species
This proportion is similar in magnitude to the values observed in the other two insect lineages that we reanalyzed in this study: 20% in the 10 bee species and 36% in the 12 flies species

Summary

Introduction

Ants constitute an extremely successful lineage of animals which has colonized virtually all ecosystems on Earth (Holldobler and Wilson 1990). We take advantage of the recent availability of seven sequenced ant genomes (Bonasio et al 2010; Nygaard et al 2011; Smith, Zimin, et al 2011; Smith, Smith, et al 2011; Suen et al 2011; Wurm et al 2011) to perform a genome-wide scan for positive selection on amino-acid changes in protein coding genes during the evolution of the ant lineage. Previous large-scale scans for positive selection in animals indicated that positive selection predominantly affects certain types of genes, such as those involved in evolutionary arms races, sexual selection, or conflicts with pathogens

Methods

Results

Conclusion