Abstract
Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web, and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Terrestrial Revolution 125–90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Avicularoidea, Theraphosoidina, Araneomorphae, Entelegynae, Araneoidea, the RTA clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major paleocribellate and neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae is in need of revision, as our findings appear to support the newly conceived concept of Synspermiata. The sister pairing of filistatids with hypochilids implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.
Highlights
Spiders (Order Araneae; Fig. 1) are a prototypical, hyperdiverse arthropod group comprising >45,000 described species (World Spider Catalog, 2016) distributed among 3,958 genera and 114 families; by some estimates the group may include >120,000 species (Agnarsson, Coddington & Kuntner, 2013)
The newly constructed spider-specific core ortholog group (OG) set contained 4,934 orthologous groups (OGs), more than three times the number of arthropod core orthologs used in prior spider analyses (Bond et al, 2014) and represents a significant step forward in generating a pool of reasonably well-vetted orthologs for spider phylogenomic analyses
Following Coddington & Levi (1991), higher-level spider classification underwent a series of challenges from quantitative studies of morphology, producing provocative but weakly-supported hypotheses (Griswold et al, 1998; Griswold et al, 2005)
Summary
Spiders (Order Araneae; Fig. 1) are a prototypical, hyperdiverse arthropod group comprising >45,000 described species (World Spider Catalog, 2016) distributed among 3,958 genera and 114 families; by some estimates the group may include >120,000 species (Agnarsson, Coddington & Kuntner, 2013). The order represents an ancient group that has continued to diversify taxonomically and ecologically since the Devonian (>380 mya) They are relatively easy to collect and identify, and are one of few large arthropod orders to have a complete online taxonomic catalog with synonymies and associated literature (World Spider Catalog, 2016). In addition to their remarkable ecology, diversity, and abundance, spiders are known for the production of extraordinary biomolecules like venoms and silks as well as their utility as models for behavioral and evolutionary studies (reviewed in Agnarsson, Coddington & Kuntner, 2013). Spider silks are promising biomaterials, already benefiting humans in myriad ways—understanding the phylogenetic basis of such super-materials will facilitate efforts to reproduce their properties in biomimetic materials like artificial nerve constructs, implant coatings, and drug delivery systems (Blackledge, Kuntner & Agnarsson, 2011; Schacht & Scheibel, 2014)
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