The impact of Quaternary Amazonian river dynamics on patterns and process of diversification in uakari monkeys (genus Cacajao)

Abstract

AimWestern Amazonia is a region that underwent several landscape changes during the Quaternary. While Riverine Barrier Hypothesis is traditionally used to explain the influence of rivers on speciation, processes such as river rearrangements have been overlooked to explain the geographic distribution and evolutionary history of the Amazonia biota. Here we test how river rearrangements in western Amazonia influenced the evolutionary history of uakari monkeys, a primate group most associated with seasonally flooded forests in western Amazonia. LocationWestern Amazonia TaxonThe uakari monkey (genus Cacajao) MethodsWe performed a continuous phylogeographic analysis using 77 cytochrome b sequences and used digital elevation models to identify the role of landscape and riverscape characteristics in the geographic distribution of Cacajao. Finally, we used genome-wide SNPs variation (ddRADseq) to investigate population structure, gene flow and demographic history in three Cacajao species that were impacted by river rearrangements. ResultsOur continuous phylogeographical reconstruction points that the ancestral Cacajao lineage occupied the flooded forests of the Solimoes River at [~]1.7 Mya, and descendant lineages dispersed throughout western Amazonia more recently. We identified gene flow among both black and bald-headed uakari populations, even across rivers considered barriers (e.g., the Negro River). Landscape analysis showed that river rearrangements influenced the geographic distribution and population structure in Cacajao. The demographic analysis indicates that C. calvus, C. amuna, and C. rubicundus went through a population decline in the last 70 Kya and have a low effective population size. Main conclusionOur results support that the river rearrangements have shaped the geographic distribution and divergence of recently diverged Cacajao lineages. Landscape and riverscape changes, along with retractions of the flooded forests, isolated some Cacajao populations in floodplain areas. Our study also suggests that these events led to the recent population decline in species with a restricted geographic distribution.