Global Diversification of Anelosimus Spiders Driven by Long-Distance Overwater Dispersal and Neogene Climate Oscillations

Abstract

Abstract 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 organisms ranging in behavior from solitary to highly social, 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 ($\sim $30 Ma) South American origin. Major clades on other continents originate via multiple, long-distance dispersal events, of solitary or subsocial—but not social—lineages, from the Americas. These intercontinental dispersals were to Africa, Madagascar (twice), and SE Asia/Australasia. The early diversification of Anelosimus spiders coincides with a sudden thermal increase in the late Oligocene ($\sim $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 South 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. [Cobweb spiders; diversification; global biogeography; long-distance dispersal; molecular phylogenetics; neogene climate changes; sociality; vicariance.]