Social insect colony size is correlated with rates of substitution and DNA repair gene evolution

Abstract

AbstractLarger numbers of germline cell divisions can increase the number of mutations inherited by offspring. Therefore, in systems where the number of offspring is dependent on the number of germline cell divisions, a higher overall rate of molecular evolution may be expected. Here I examine whether colony size in social insects, which varies from tens to millions, influences molecular evolutionary rates by analyzing several recently collected datasets. First, I find that colony size is negatively correlated with GC-content across 115 ant genera, indicative of a positive relationship between substitution rate and colony size. Second, genome-wide rates of molecular evolution are positively correlated with colony size in three clades of social insects including eight species in the ant genusPseudomyrmex, seven fungus-growing ants, and 11 bee species. The additional germline cell divisions necessary to maintain large colony sizes might lead to mutation accumulation in the germlines of queens of these species, a process similar to that which occurs in aging human males. I also find intensified constraint on DNA repair genes in species with large colonies, suggesting that the additional mutations that occur in these taxa increase selective pressure for improved replication fidelity. Colony size, a fundamental facet of eusociality, plays a previously unappreciated role in genome evolution.