Phylogenomics Resolves a Spider Backbone Phylogeny and Rejects a Prevailing Paradigm for Orb Web Evolution

Abstract

Spiders represent an ancient predatory lineage known for their extraordinary biomaterials, including venoms and silks. These adaptations make spiders key arthropod predators in most terrestrial ecosystems. Despite ecological, biomedical, and biomaterial importance, relationships among major spider lineages remain unresolved or poorly supported. Current working hypotheses for a spider "backbone" phylogeny are largely based on morphological evidence, as most molecular markers currently employed are generally inadequate for resolving deeper-level relationships. We present here a phylogenomic analysis of spiders including taxa representing all major spider lineages. Our robust phylogenetic hypothesis recovers some fundamental and uncontroversial spider clades, but rejects the prevailing paradigm of a monophyletic Orbiculariae, the most diverse lineage, containing orb-weaving spiders. Based on our results, the orb web either evolved much earlier than previously hypothesized and is ancestral for a majority of spiders or else it has multiple independent origins, as hypothesized by precladistic authors. Cribellate deinopoid orb weavers that use mechanically adhesive silk are more closely related to a diverse clade of mostly webless spiders than to the araneoid orb-weaving spiders that use adhesive droplet silks. The fundamental shift in our understanding of spider phylogeny proposed here has broad implications for interpreting the evolution of spiders, their remarkable biomaterials, and a key extended phenotype--the spider web.

The Nephila clavipes genome highlights the diversity of spider silk genes and their complex expression

“…Many of these motifs occur in iterated groups, and we catalog as many as 506 unique 'cassettes' that feature two to four contiguous motifs and that are themselves organized into larger repetitive units (~200 amino acid residues) known as ensemble repeats 30,36 . The N. clavipes genome provides evidence for evolutionary mechanisms like tandem duplication that may underlie spidroin diversification, and our data support estimates that rapid silk evolution accompanied the emergence of the orb web ~213 million years ago 37 .…”

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

“…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.…”

Phylogenomic resolution of scorpions reveals multilevel discordance with morphological phylogenetic signal

“…direct sperm transfer; median ocelli; paired tarsal claws), and spiders (e.g. unsegmented opisthosoma; venom glands; labidognathous chelicerae), and these evolutionary trends have been robustly validated by phylogenomic data [14,54,[59][60][61][62][63][64]. In the case of scorpions, barring the clear separation of buthids from non-buthid lineages, there has been little agreement as to how scorpion families are related.…”