Phylogenomics of Messor harvester ants (Hymenoptera: Formicidae: Stenammini) unravels their biogeographical origin and diversification patterns

Abstract

As a major abiotic factor, climate change is expected to profoundly alter biological communities. On this basis, identifying how past temperature variations affected species diversification and distribution can help to predict the effects of the ongoing climate change. In this study, we focused on the harvester ant genus Messor Forel, which is adapted to dry environments by specializing in a granivorous diet. The phylogenomic analyses of 2524 ultraconserved-element loci obtained from 58 Messor species and subspecies support their monophyly. Phylogenetic relationships uncovered in this study enabled us to redefine historical taxonomic groups, providing a solid basis for future revisions that encompass the entire genus diversity. Molecular dating and biogeographical analyses indicate an emergence in the Irano-Indian area approximately 20 million years ago. Our results suggest a rapid geographical dispersal from their ancestral range towards the Western Palaearctic, reaching Northeastern Africa during the early Miocene. We found a major diversification event during the mid-Miocene climatic optimum, from which we inferred the emergence of the common ancestor of all Messor groups. Their diversification appears to be affected by temperature, suggesting a higher speciation rate during warmer periods. This confirms that the ecological specialization of Messor makes them strongly dependent on thermal conditions. Our results highlight the importance of abiotic factors on diversification processes, especially for highly specialized species that may exhibit predictable evolutionary responses to climate changes.