Genome-wide rates of molecular evolution are higher in mutualistic plant-nesting ants

The obligate mutualism between ants in the genus Pseudomyrmex and acacia trees is one of the most well known of any ant-plant relationship. In this particular mutualism, ants nest in and feed on the hollow thorns, food bodies, and extra-floral nectar provided by the acacia. In exchange for these resources, resident ants aggressively protect their hosts by attacking herbivores and parasites. This ant defense is incredibly effective and their absence ensures plant death. In addition to the acacia specialists, obligate mutualism has evolved convergently in two other clades of Pseudomyrmex species that nest in trees from the genera Triplaris and Tachigali. Despite differences in diet and nest structure, these ants behave in the same way as acacia-nesters, aggressively biting and stinging any intruders. We present three newly sequenced Pseudomyrmex genomes representing species from each mutualistic clade as well as four genomes of closely related non-mutualistic species. Despite their independent evolutionary origins, all three mutualists show genome-wide signatures of elevated rates of molecular evolution. This pattern is present in both coding and non-coding sequence and is unlikely to be the result of genetic drift, suggesting the occurrence of repeated selective sweeps or increased mutation rates. We also find a small set of genes related to muscle development and function with consistent signatures of positive selection in all mutualists, suggesting their involvement in the evolution of mutualistic behavior. Our findings provide a detailed understanding of the genetic features involved in and, possibly, resulting from, the evolution of this complex behavior.