'Dispersification' of Agalinis (Orobanchaceae) into South America is associated with hummingbird pollination and perennial life history shifts

Abstract

AimSeveral mechanisms contribute to the plant biodiversity of the Neotropics, with the highlands of South America serving as important hotspots of diversity. In particular, the Brazilian highlands exhibit high biodiversity due to complex diversification dynamics and a mixture of contributions from different biomes. In this study, we reconstruct the timing and potential triggers of diversification of Agalinis, hemiparasitic plants that inhabit open grassland habitats, to investigate their biogeographic history and migration patterns across the Americas. LocationNorth, Central, and South America TaxonAgalinis. MethodsWe reconstructed dated phylogenies of Agalinis using a secondary calibration approach, sampling 73% of the known species, including multiple species from the Andes and Brazilian highlands. We inferred ancestral distributions to understand migration patterns between North and South America and within South America. Additionally, we investigated shifts in diversification rates within the genus and reconstructed ancestral pollination syndrome and life history strategy states. All analyses were performed across a distribution of trees to account for phylogenetic uncertainty. ResultsAgalinis likely originated in southeastern North America during the early Miocene and rapidly diversified, followed by movement into South America in the Late Miocene or Early Pliocene. We propose two possible routes for Agalinis movement into South America: either through the Andes or via the South American lowland grasslands (e.g., Chaco, Pampas, Cerrado, Caatinga, Llanos), using grassland corridors for dispersal within the continent. After its arrival in South American highlands, the clade underwent rapid diversification. State reconstructions indicated that the genus had a bee-pollinated ancestor and that hummingbird pollination evolved only once, with many transitions back to bee pollination. In contrast, the perennial life strategy evolved multiple times within the genus, including at least once in the ancestor of all South American species and twice in the North American species. Main ConclusionsAgalinis likely originated in North America and later migrated to South America, followed by rapid diversification (i.e., dispersification). Thus, Agalinis is a clade that refutes the tropical conservatism hypothesis and the out-of-the-tropics model. Moreover, the dispersal to the Brazilian highlands was from nearby species pools and not from other highland habitats such as the Andes, followed by several in situ speciation events. These high diversification rates were partly associated with Quaternary climatic oscillations, and perennial and hummingbird-pollinated species exhibited higher turnover rates.