The phylogenomic landscape of an understory ant-plant symbiosis in the Neotropics

Obligate ant-plant mutualisms are often assumed to arise from a single evolutionary event within ant lineages. However, integrating phylogenomic data with detailed natural history reveals a more complex picture. In Myrmelachista (Hymenoptera: Formicidae), a genus of exclusively arboreal ants, species exhibit a wide range of nesting behaviors - from opportunistic generalists to obligate mutualists nesting within the live stems of a narrow set of host plants. Despite striking morphological and behavioral convergence among mutualistic taxa, phylogenomic analyses of 227 specimens using ultraconserved elements reveal at least four independent origins of mutualism – two in South America and two in Central America. These mutualistic lineages are nested within four well-supported clades: a Patagonian clade sister to the rest of the genus, two widespread Neotropical clades (each with one independent mutualist lineage), and a fourth clade concentrated in Mesoamerica and the Caribbean (with two independent origins).
Divergence dating and biogeographic reconstruction indicate a South American origin ~25 million years ago, followed by multiple dispersals during the Oligocene and Miocene. Mutualistic taxa are generally yellow-colored and restricted to mid- to lowland rainforests. However, we document a notable exception: a high-elevation South American lineage that retains the ancestral dark coloration, suggesting that elevation may influence pigmentation and potentially override phenotypic convergence driven by the evolution of mutualism. These findings open avenues for phylogenetic modeling to test how elevation, coloration, and mutualism co-evolve. Myrmelachista provides a promising system for disentangling the ecological and evolutionary dynamics of specialized symbioses across the Neotropical region.