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Systematics, Phylogeny, and Evolution of Orb-Weaving Spiders

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Systematics, Phylogeny, and Evolution of Orb-Weaving Spiders EN59CH25-Hormiga ARI 27 November 2013 16:54 Systematics, Phylogeny, and Evolution of Orb-Weaving Spiders Gustavo Hormiga1,∗ and Charles E. Griswold2 1Department of Biological Sciences, The George Washington University, Washington, DC 20052; email: [email protected] 2Department of Entomology, California Academy of Sciences, San Francisco, California 94118; email: [email protected] Annu. Rev. Entomol. 2014. 59:487–512 Keywords First published online as a Review in Advance on spiders, phylogeny, Orbiculariae, Araneoidea, Palpimanoidea, webs October 25, 2013 by University of Texas - Austin on 05/27/14. For personal use only. The Annual Review of Entomology is online at Abstract ento.annualreviews.org Annu. Rev. Entomol. 2014.59:487-512. Downloaded from www.annualreviews.org The orb-weaving spiders (Orbiculariae) comprise more than 25% of the This article’s doi: approximately 44,000 known living spider species and produce a remark- 10.1146/annurev-ento-011613-162046 able variety of webs. The wheel-shaped orb web is primitive to this clade, Copyright c 2014 by Annual Reviews. but most Orbiculariae make webs hardly recognizable as orbs. Orb-weavers All rights reserved date at least to the Jurassic. With no evidence for convergence of the orb web, ∗ Corresponding author the monophyly of the two typical orb web taxa, the cribellate Deinopoidea and ecribellate Araneoidea, remains problematic, supported only weakly by molecular studies. The sister group of the Orbiculariae also remains elusive. Despite more than 15 years of phylogenetic scrutiny, a fully resolved clado- gram of the Orbiculariae families is not yet possible. More comprehensive taxon sampling, comparative morphology, and new molecular markers are required for a better understanding of orb-weaver evolution. 487 EN59CH25-Hormiga ARI 27 November 2013 16:54 INTRODUCTION Ubiquitous, diverse, and exclusively predatory, spiders (Araneae) are among the largest animal groups and the dominant arthropod predators in most terrestrial ecosystems. About 44,000 spider species have been described to date (149); estimates of the total number of species range from 76,000 to 170,000 (1, 119). The orb-weavers (Orbiculariae, an informal name for the taxon con- taining the superfamilies Deinopoidea and Araneoidea) are among the most diverse lineages of spiders. With their highly geometric web designs and their ability to produce as many as seven different types of silk with different functions and mechanical properties (142), orb-weavers have captured the attention of biologists and the lay public alike. The basic architecture of an orb web includes a frame holding radii that support a spirally arranged sticky thread. The web must absorb the kinetic energy of the intercepted prey and retain it long enough for the spider to locate and subdue it (26). The oldest orb-weaver fos- sils are from the Jurassic (117) and the oldest fossilized orb web is from the Cretaceous (113). Two groups of spiders make geometrically similar orb webs using different silks but with pre- sumably homologous stereotypical behaviors, the deinopoids (Deinopoidea) and the araneoids (Araneoidea) (38). The sticky spiral of deinopoid webs comprises dry cribellate silk, which is metabolically expensive to produce and is formed by thousands of fine-looped fibrils woven on a core of two axial fibers (Figure 1g). The adhesive properties of the deinopoid sticky spiral are attained by hygroscopic and van der Vaals forces and mechanical interlock (109). In contrast, the sticky spiral thread of araneoid webs is coated with a viscid aqueous secretion that coalesces as regularly spaced droplets around the axial fibers (108) (Figure 1a). Specialized flagelliform glands produce the axial fibers and their viscous coating (aggregate) (139). This type of compos- ite sticky thread is produced faster, more economically, and with higher stickiness than the dry, fuzzy deinopoid counterpart (108). In addition, the axial fibers of the araneoid capture thread are more extensible than those of deinopoid cribellar threads (21), which contributes to its in- creased stickiness by allowing longer spans of capture thread to contact the prey (110). Cribellar silk is plesiomorphic relative to the viscid araneoid silk. About 27% of the described extant spider species belong to Orbiculariae, of which the vast majority belong to Araneoidea (18 families and 11,997 extant species). Their putative sister group, Deinopoidea, is depauperate in comparison: Only 326 species in two families spin orb webs with cribellate silk. This asymmetry in diversity has been attributed to the shift in type of capture thread, from dry, fuzzy cribellate silk to vis- cid sticky silk, combined with changes in the silk spectral reflective properties and a transition from horizontal to vertical orb webs (23, 33, 134). Most araneoid species build foraging webs that by University of Texas - Austin on 05/27/14. For personal use only. are no longer recognizable as geometric orbs, such as sheet webs (e.g., Linyphiidae) or cobwebs (e.g., Theridiidae). Some orbicularian lineages have abandoned the use of capture webs altogether Annu. Rev. Entomol. 2014.59:487-512. Downloaded from www.annualreviews.org (e.g., Mimetidae). Here we provide an overview of orbicularian phylogeny and systematics, focusing on the re- search published since 1998. Any rigorous attempt to explain orb web evolution and diversifica- tion requires an empirically robust phylogenetic context, so we emphasize studies with the most −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ Figure 1 Examples of the diversity of orbicularian webs and lifestyles (all are ecribellate araneoids except Deinopis sp.). (a) Phonognatha sp. (Araneidae; Australia). (b) Forstera sp. (Cyatholipidae; Australia). (c) Mangua medialis (Synotaxidae; New Zealand). (d ) Anapidae (Madagascar). (e) Mysmenidae (Cameroon). ( f ) Laetesia sp. (Linyphiidae; Australia). ( g) Deinopis sp. (Deinopidae; Madagascar), a cribellate orb-weaver. (h) Australomimetus sp. (Mimetidae; Australia), a webless araneophagic araneoid. (i ) Exechocentrus lancearius (Araneidae; Madagascar), a bolas spider that presumably uses chemical mimicry to lure its prey. (j) Achaearanea sp. (Theridiidae; Australia). (k) Patu sp. (Symphytognathidae; Dominican Republic). All photos courtesy of G. Hormiga. 488 Hormiga · Griswold EN59CH25-Hormiga ARI 27 November 2013 16:54 aabb c d e ffgg by University of Texas - Austin on 05/27/14. For personal use only. Annu. Rev. Entomol. 2014.59:487-512. Downloaded from www.annualreviews.org hhii j jkk www.annualreviews.org • Systematics of Orb-Weaving Spiders 489 EN59CH25-Hormiga ARI 27 November 2013 16:54 comprehensive taxon samples; studies treating only subsets of araneoid families (13, 29) remain ambiguous. In documenting the current level of understanding of orbicularian phylogeny and diversity, we aim to expose the major gaps in the phylogenetic knowledge required to build the Entelegynae: the largest clade of foundation for comparative studies. All diversity figures (e.g., number of described taxa) for ex- araneomorphs tant and extinct taxa are from Platnick (120) and Dunlop et al. (37), respectively. The literature characterized by treating the evolutionary biology of orbicularians is too extensive to be summarized here. Several complex copulatory recent works have reviewed a diversity of topics, including silk and webs (20, 32), behavior (25, organs in both sexes, 69), ecology and ecophysiology (105, 146), sociality (91), and neurobiology (16), in which a few including external copulatory openings in emblematic orb-weaving species figure prominently as study subjects. females, and by cylindrical silk glands ORB WEB MONOPHYLY Synapomorphy: a shared derived trait; Whether ecribellate and cribellate orbs have a single origin or evolved convergently began to be provides the empirical rigorously examined in the late 1980s. Most research in the past two decades, based mainly on be- evidence for clades havioral and spinning organ data, supports a single origin of the orb web (22, 28, 29, 38, 52, 57, 59). The most taxon- and character-inclusive morphological/behavioral examinations of this question have been the analyses of Griswold et al. (59), which tested orbicularian monophyly and placement in a broader entelegyne taxonomic context. Unfortunately, under equal character weights their cladistic analysis neither corroborated nor refuted orbicularian monophyly. Their implied weight analyses did recover orbicularians as a clade (including Nicodamidae, which do not build orbs and at the time were not considered orbicularians) on the basis of one silk plus ten web-building behav- ior synapomorphies. A related problem, inextricably linked to the monophyly question, centers around the limits of the superfamily Palpimanoidea. Forster & Platnick (48) suggested membership of a number of araneoid groups in the distantly related Palpimanoidea on the basis of two putative cheliceral synapomorphies: the promarginal peg teeth and the retromarginal gland mounds on the cuticle. Palpimanoidea sensu Forster and Platnick would include the families Palpimanidae, Archaeidae, Mecysmaucheniidae, Huttoniidae, Stenochilidae, Pararchaeidae, Holarchaeidae, Micropholcommatidae, and Mimetidae. This suprafamilial circumscription has been a highly controversial hypothesis because it included a subset of families otherwise thought to be members of the Orbiculariae. Schutt¨ (131, 132) investigated the limits of Araneoidea and Palpimanoidea and
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