Evolution of andrenine bees reveals a long and complex history of faunal interchanges between the Americas during the Mesozoic and Cenozoic

Abstract

Bees are presumed to have arisen in the early to mid-Cretaceous coincident with the fragmentation of the southern continents and concurrently with the early diversification of the flowering plants. Among the main groups of bees, Andreninae sensu lato comprise about 3000 species widely distributed with greatest and disjunct diversity in arid areas of North America, South America, and the Palearctic region. Here, we present the first comprehensive dated phylogeny and historical biogeographic analysis for andrenine bees, including representatives of all currently recognized tribes. Our analyses rely on a dataset of 106 taxa and 7952 aligned nucleotide positions from one mitochondrial and six nuclear loci. Andreninae is strongly supported as a monophyletic group and the recovered phylogeny corroborates the commonly recognized clades for the group. Thus, we propose a revised tribal classification that is congruent with our phylogenetic results. The time-calibrated phylogeny and ancestral range reconstructions of Andreninae reveal a fascinating evolutionary history with Gondwana patterns that are unlike those observed in other subfamilies of bees. Andreninae arose in South America during the Late Cretaceous around 90 Million years ago (Ma) and the origin of tribes occurred through a relatively long time-window from this age to the Miocene. The early evolution of the main lineages took place in South America until the beginning of Paleocene with North American fauna origin from it and Palearctic from North America as results of multiple lineage interchanges between these areas by long-distance dispersal or hopping through landmass chains. Overall, our analyses provide strong evidence of amphitropical distributional pattern currently observed in Andreninae in the American continent as result at least three periods of possible land connections between the two American landmasses, much prior to the Panama Isthmus closure. The andrenine lineages reached the Palearctic region through four dispersal events from North America during the Eocene, late Oligocene and early Miocene, most probably via the Thulean Bridge. The few lineages with Afrotropical distribution likely originated from a Palearctic ancestral in the Miocene around 10 Ma when these regions were contiguous, and the Sahara Desert was mostly vegetated making feasible the passage by several organisms. Incursions of andrenine bees to North America and then onto the Old World are chronological congruent with distinct periods when open-vegetation habitats were available for trans-continental dispersal and at the times when aridification and temperature decline offered favorable circumstances for bee diversification.