Palaeoceanographic changes in the late Pliocene promoted rapid diversification in pelagic seabirds

Abstract

Aim: Palaeoceanographic changes can act as drivers of diversification and speciation, even in highly mobile marine organisms. Shearwaters are a group of globally distributed and highly mobile pelagic seabirds. Despite a recent well resolved phylogeny, shearwaters have controversial species limits, and show periods of both slow and rapid diversification. Here, we explore the role of paleoceanographic changes on the diversification and speciation in these highly mobile pelagic seabirds. We investigate shearwater biogeography and the evolution of a key phenotypic trait, body size, and we assess the validity of the current taxonomy of the group. Location: Worldwide. Taxa: Shearwaters (Order Procellariiformes, Family Procellariidae, Genera Ardenna, Calonectris and Puffinus). Methods: We generated genomic data (double-digest restriction site-associated DNA) for almost all extant shearwater species to infer a time-calibrated species tree. We estimated ancestral ranges and evaluated the roles of founder events, vicariance and surface ocean currents in driving shearwater diversification. We performed phylogenetic generalized least squares to identify potential predictors of variability in body size along the phylogeny. To assess the validity of the current taxonomy of the group, we analysed genomic patterns of recent shared ancestry and differentiation among shearwater taxa. Results: We identified a period of high dispersal and rapid speciation during the Late Pliocene - early Pleistocene. Species dispersal appears to be favoured by surface ocean currents, and biogeographic reconstructions support founder events as the main mode of speciation in these highly mobile pelagic seabirds. Body mass shows significant associations with life strategies and local conditions. The current taxonomy shows some incongruences with the patterns of genomic divergence. Main Conclusions: A reduction of neritic areas during the Pliocene seems to have driven global extinctions of shearwater species, followed by a subsequent burst of speciation and dispersal probably promoted by Plio-Pleistocene climatic shifts. Our findings extend our understanding on the drivers of speciation and dispersal of highly mobile pelagic seabirds and shed new light on the important role of paleoceanographic events.