Spider phylogenomics: untangling the Spider Tree of Life

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.

Comparative study of spinning field development in two species of araneophagic spiders (Araneae, Mimetidae, Australomimetus)

“…In a SEM study of 156 PLS from 1 st to 6 th instars of Mimetus, nine (6%) had a cuticular protuberance in a location consistent with an araneoid AG-FL triad (three spigots: two AG, one FL) (Townley and Tillinghast 2009). These protuberances were tentatively identified as phylogenetic nubbins, possibly of AG or FL spigots, a suggestion consistent with a growing consensus that mimetids are closely related to the araneoid family Tetragnathidae (Blackledge et al 2009, Dimitrov and Hormiga 2011, Dimitrov et al 2012, Bond et al 2014, Hormiga and Griswold 2014, Garrison et al 2016, Wheeler et al 2016. Putative sensilla associated with these nubbins and with AG/FL spigots in typical araneoids (several indicated in Figs 9-11), and similarities between these nubbins and those occasionally seen in the same location in the araneid Cyrtophora, have been discussed previously (Townley andTillinghast 2009, Townley et al 2013).…”

“…The ducts of non-tartipore-accommodated (non-T-A) silk glands lose their connection to the old exoskeleton around apolysis, do not give rise to tartipores, and therefore the spider cannot draw silk from them during proecdysis. In some spider clades, such as the ecribellate haplogyne Synspermiata (Platnick et al 1991, Michalik and Ramírez 2014, Garrison et al 2016, Wheeler et al 2016, all silk glands are non-T-A. The two Australomimetus species examined in this study have both T-A and non-T-A versions of major ampullate, minor ampullate, and piriform silk glands (MaA, MiA, PI).…”

“…Several recent cladistic analyses, based partly or solely on sequence data, agree in placing Mimetidae within Araneoidea, and further agree that mimetids are closely related to the orb-web-building family Tetragnathidae (Blackledge et al 2009, Dimitrov and Hormiga 2011, Dimitrov et al 2012, Bond et al 2014, Hormiga and Griswold 2014, Garrison et al 2016, Wheeler et al 2016. The possibility of a close relationship between these two families was raised earlier by Shear (1981) and Schütt (2000) based on morphological similarities and indicates that araneophagy, combined with a loss of web-building capacity, is a derived state in this family.…”

“…It is noteworthy that the two species, A. tasmaniensis and A. djuka, constitute the tasmaniensis-group in the cladistic analysis of Harms and Harvey (2009b), sister to all other Australomimetus species included in that analysis. Possession of 2° MiA has been considered the plesiomorphic condition for araneoids on phylogenetic grounds (Forster et al 1990, Scharff and Coddington 1997, Griswold et al 1998, which remains valid despite substantial changes proposed in higher-level spider phylogeny in recent years (Bond et al 2014, Fernández et al 2014, Garrison et al 2016, Wheeler et al 2016). The consistent occurrence of an apparent phylogenetic 2° MiA nubbin on the PMS of 1 st instars of A. djuka corroborates this view, clearly indicating the absence of 2° MiA in this species represents a secondary loss.…”

Nanofibre production in spiders without electric charge

“…1A). To evaluate the general validity of the findings, threads of another Uloboridae, Zosis geniculata, as well as the distantly related Amaurobiidae Amaurobius ferox, Desidae Badumna longinqua and the Filistatidae Kukulcania hibernalis were examined (Bond et al, 2014;Fernández et al, 2014;Garrison et al, 2016). Capture threads of these species differ greatly in shape from those of Uloboridae (Fig.…”