Global diversification of Anelosimus spiders driven by long distance overwater dispersal and Neogene climate oscillations

Vicariance and dispersal events, combined with intricate global climatic
history, have left an imprint on the spatiotemporal distribution and
diversity of many organisms. Anelosimus cobweb spiders (Theridiidae), are
solitary-social organisms with a cosmopolitan distribution in temperate-
to-tropical areas. Their evolutionary history and the discontinuous
distribution of species richness suggest that 1) long distance overwater
dispersal, and 2) climate change during the Neogene (23–2.6 Ma), may be
major factors in explaining their distribution and diversification. Here
we test these hypotheses, and explicitly test if global Miocene/Pliocene
climatic cooling in the last 8 Ma affected Anelosimus radiation in
parallel in South America and Madagascar. To do so, we investigate the
phylogeny and spatiotemporal biogeography of Anelosimus through a
culmination of a 20-year comprehensive global sampling at the species
level (69 species, including 84% of the known 75 species worldwide,
represented by 268 individuals) using nucleotide data from seven loci (5.5
kb). Our results strongly support the monophyly of Anelosimus with an
Oligocene (~30 Ma) South American origin. Major clades on other continents
originate via multiple, long-distance dispersal events, of solitary or
subsocial—but not social—lineages, from the Americas. These
intercontinental dispersals were to Africa, Madagascar (twice), and SE
Asia/Australasia. The early diversification of Anelosimus spiders
coincides with a sudden thermal increase in the late Oligocene (~27–25
Ma), though no causal connection can be made. Our results, however,
strongly support the hypothesis that global Neogene climatic cooling in
the last 8 Ma drove Anelosimus radiation in parallel in S. America and
Madagascar, offering a rare empirical evidence for diversification of a
socially diverse group driven by an interplay between long distance
dispersal and global Neogene climatic changes.