Phylogenomics unveils Afrotropical origin, trans-oceanic global diversification and climatic niche conservatism in the sedentary Zodariidae ant spiders

Abstract

Ancient origin and continental drift are commonly invoked to explain the worldwide distribution of poor dispersers, but this has not been thoroughly tested, including among most highly diversified groups. Here, we reconstructed the deep phylogeny of the globally distributed ant spiders (Zodariidae, >1300 species) through ~1000 Ultraconserved Elements (UCE-) loci from 76 of the 90 nominal genera plus multiple outgroups. We then estimated zodariids' diversification timeline using alternative methods and inferred its key biogeographic processes at the continental scale through ancestral range estimation and biogeographical stochastic mapping. Our robust phylogeny supports Zodariidae's monophyly, sister relationship with Penestomidae, and the subfamily classification—with Procydrela transferred to a new subfamily. Surprisingly, zodariids originated and diversified from the end of the Early Cretaceous onwards, after Earth's major landmasses separated. Multiple range changes between realms were inferred, all via jump dispersal, and most originating in the Afrotropics. Most routes were taken only once, except for increased connectivity between the Afrotropics, Madagascar and the Indomalayan regions. Of 14 jump dispersal events with reliably inferred routes, 10 were trans-oceanic whereas 3 were trans-climatic. We conclude that trans-oceanic dispersal was pivotal in zodariids' global distribution and diversification, giving origin to ~60% of its biota, and that climatic niche conservatism has limited trans-climatic colonization between land-connected regions. Our study provides a solid framework for interpreting additional aspects of zodariids' unique evolution. It also exemplifies how poor dispersers may overcome geographic barriers over sufficiently long timeframes, leading to remarkable diversification.