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.

Spiders were sampled worldwide between 1998 and 2018 and fixed in 95% ethanol. Seven pairs of primers were used to amplify sequences of mitochondrial (COI, 16S) and nuclear (18S, 28S, wingless, ITS2, H3) loci from the collected specimens with annealing temperatures optimized at 44–56 (table S2). New sequences were submitted to Genbank (table S1). We then combined these new sequences with previously published sequences from Agnarsson et al. (2007, 2010) and Agnarsson (2012a, 2012b). The total dataset contained 268 individuals representing at least 69 species of Anelosimus, 62 described and at least 7 as yet undescribed species. Our samples cover the majority of the distribution range of Anelosimus.