Reconstructing web evolution and spider diversification in the molecular era

Abstract

The evolutionary diversification of spiders is attributed to spectacular innovations in silk. Spiders are unique in synthesizing many different kinds of silk, and using silk for a variety of ecological functions throughout their lives, particularly to make preycatching webs. Here, we construct a broad higher-level phylogeny of spiders combining molecular data with traditional morphological and behavioral characters. We use this phylogeny to test the hypothesis that the spider orb web evolved only once. We then examine spider diversification in relation to different web architectures and silk use. We find strong support for a single origin of orb webs, implying a major shift in the spinning of capture silk and repeated loss or transformation of orb webs. We show that abandonment of costly cribellate capture silk correlates with the 2 major diversification events in spiders (1). Replacement of cribellate silk by aqueous silk glue may explain the greater diversity of modern orb-weaving spiders (Araneoidea) compared with cribellate orb-weaving spiders (Deinopoidea) (2). Within the ''RTA clade,'' which is the sister group to orb-weaving spiders and contains half of all spider diversity, >90% of species richness is associated with repeated loss of cribellate silk and abandonment of prey capture webs. Accompanying cribellum loss in both groups is a release from substrate-constrained webs, whether by aerially suspended webs, or by abandoning webs altogether. These behavioral shifts in silk and web production by spiders thus likely played a key role in the dramatic evolutionary success and ecological dominance of spiders as predators of insects.Araneidae ͉ behavioral evolution ͉ cribellate silk ͉ orb web ͉ speciation S piders are exceptionally diverse and abundant in terrestrial ecosystems. In contrast to megadiverse orders of insects, evolutionary diversification of spiders is not coupled with major trophic shifts. All spiders are predators of arthropods, and spiders are dominant consumers at intermediate trophic levels (1, 2). Spider diversification is instead linked to key innovations in silk use (3-7). For instance, the araneoid orb web (Fig. 1) with stretchy capture spirals, coated by adhesive viscid silk secretions, provides access to abundant flying insects (3,8). However, many spiders produce cribellate silk, a radically different dry adhesive that adheres to prey, using van der Waals interactions and hygroscopic forces (9). Some cribellate spiders also construct aerial orb webs, whereas most spin sheet-like webs on the substrate (Fig. S1) or have abandoned capture webs altogether. Furthermore, the most diverse families within ''orb-weavers'' (Orbiculariae) no longer build orb webs, but instead spin aerial sheet webs (Linyphiidae) or cobwebs (Theridiidae) (Fig. S2). Thus, discovering the pattern of evolution of web spinning behaviors is essential for understanding spider diversification.Orb webs possessing dry cribellate capture spirals are architecturally similar to those spun from aqueous viscid silk ( Fig. 1 ...

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

“…More than 380 million years of evolution have produced >46,000 extant spider species, exhibiting an incredible diversity of silks used for prey capture and reproduction [1][2][3] . Spider silks can be stronger than steel and tougher than Kevlar, yet are much lighter weight than these manmade materials 4 .…”

Silk elasticity as a potential constraint on spider body size

“…Silk has played a key role in the radiation of spiders (Blackledge et al, 2009;Vollrath and Selden, 2007) following the colonisation of land by their ancestors in the early Devonian (Selden et al, 1991;Shear et al, 1989). The number of silk-producing glands and silk types that individual spiders produce has increased during the evolution of the group, and orb-weaving spiders spin seven different kinds of silk, including five fibrous silks that contain unique sets of proteins (Foelix, 1996).…”

Cues guiding uloborid construction behavior support orb web monophyly

“…Most recent phylogenetic analyses of morphological and behavioral traits (Griswold et al 1998;Kuntner et al 2008), as well as molecular traits (Garb et al 2006;Blackledge et al 2009;Dimitrov et al 2012) have supported the single origin hypothesis for orb webs. The degree of support has been controversial, however (Dimitrov et al 2012), and the question of how ecribellate sticky lines evolved and replaced cribellate sticky lines without any known intermediate orb web forms that lacked sticky lines is still a puzzle (Opell & Schwend 2009).…”

“…Until last year, a general consensus that favored the single origin hypothesis for orb webs seemed to be emerging, based on morphological and behavioral (Griswold et al 1998;Kuntner et al 2008) as well as molecular traits (Garb et al 2006;Blackledge et al 2009;Dimitrov et al 2012). In 2014, however, a pair of molecular analyses, which attempted to correct for several potential problems, including artificial inflation of support due to missing data, unequal rates of evolution in different lineages, compositional heterogeneity, and heterotachy (Fernandez et al 2014, Bond et al 2014, found support for linking the deinopoids more closely with a large group of about 40 non-orb weaving (and largely webless) families (the "RTA clade"), rather than with araneoids.…”