Phylogenomics illuminates the evolution of orb webs, respiratory systems and the biogeographic history of the world’s smallest orb-weaving spiders (Araneae, Araneoidea, Symphytognathoids)

Abstract

The miniature orb weaving spiders (symphytognathoids) are a group of small spiders (<2 mm), including the smallest adult spider Patu digua (0.37 mm in body length), that have been classified into five families. The species of one of its constituent lineages, the family Anapidae, build a remarkable diversity of webs (ranging from orbs to sheet webs and irregular tangles) and even include a webless kleptoparasitic species. Anapids are also exceptional because of the extraordinary diversity of their respiratory systems. The phylogenetic relationships of symphytognathoid families have been recalcitrant with different classes of data, such as, monophyletic with morphology and its concatenation with Sanger-based six markers, paraphyletic (including a paraphyletic Anapidae) with solely Sanger-based six markers, and polyphyletic with transcriptomes. In this study, we capitalized on a large taxonomic sampling of symphytognathoids, focusing on Anapidae, and using de novo sequenced ultraconserved elements (UCEs) combined with UCEs recovered from available transcriptomes and genomes. We evaluated the conflicting relationships using a variety of support metrics and topology tests. We found support for the phylogenetic hypothesis proposed using morphology to obtain the “symphytognathoids'' clade, Anterior Tracheal System (ANTS) Clade and monophyly of the family Anapidae. Anapidae can be divided into three major lineages, the Vichitra Clade (including Teutoniella, Holarchaea, Sofanapis and Acrobleps), the subfamily Micropholcommatinae and the Orb-weaving anapids (Owa) Clade. Biogeographic analyses reconstructed a hypothesis of multiple long-distance transoceanic dispersal events, potentially influenced by the Antarctic Circumpolar Current and West Wind Drift. In symphytognathoids, the ancestral anterior tracheal system transformed to book lungs four times and reduced book lungs five times. The posterior tracheal system was lost six times. The orb web structure was lost four times independently and transformed into sheet web once.