Phylogenomics resolve the systematics and biogeography of the ant tribe Myrmicini and tribal relationships within the hyperdiverse ant subfamily Myrmicinae

Abstract

Ants are a globally distributed and highly diverse group of eusocial animals, playing key ecological roles in most of the world’s terrestrial ecosystems. Our understanding of the processes involved in the evolution of this diverse family is contingent upon our knowledge of the phylogeny of the ants. While relationships among most subfamilies have come into resolution recently, several of the tribal relationships within the hyperdiverse subfamily Myrmicinae persistently conflict between or within studies, mirroring the controversial relationships of the Leptanillinae and Martialinae to the remaining ant subfamilies. Another persistent issue of debate in ant phylogenetics is the timing of major evolutionary events as inferred via divergence dating. Here, we test the topology of the myrmicine tribes using genome scale data, inspect gene tree-species tree concordance, and use posterior predictive checks and tests of compositional heterogeneity to infer sequence characteristics which potentially introduce systematic bias in myrmicine tribal topology. Furthermore, we test the placement of the Baltic amber fossil †Manica andrannae by integrating phylogenomic and morphological data from nearly all species within the genus Manica, and a broad sampling of its sister genus Myrmica. Subsequently, we demonstrate the effect of fossil placement on overall divergence times in the Myrmicinae. We then re-evaluate the historical biogeography of the Myrmicini and Pogonomyrmecini considering newly generated genetic data and insights from our phylogenomic results. We find that our current understanding of tribal topology in the Myrmicinae is strongly supported, but this topology is highly sensitive to compositional heterogeneity and gene-tree species-tree conflict. Our fossil placement analyses strongly suggest that †Manica andrannae is a stem Manica species, and analysis of this fossil in context of the Myrmicinae demonstrates that a single fossil calibration point can have broad-scale cascading effects on divergence dates within the entire subfamily. The results of our biogeographic reconstructions indicate a South American origin for the Pogonomyrmecini + Myrmicini. Additionally, our results suggest that the MRCA of Myrmica may have inhabited the western Nearctic in the early Miocene prior to repeated dispersal across Beringia throughout the Miocene and Pliocene. The MRCA of Manica, on the other hand, was inferred to have a Holarctic range prior to vicariance during the Pliocene. Unexpectedly, we found strong support in the Pogonomyrmecini for three coordinated dispersal events from South to Central America during the early Miocene, which has been previously proposed as an early biotic interchange event prior to the more commonly accepted 3.5 Ma closure of the Isthmus of Panama.