Systematics, Phylogeny, and Evolution of Orb-Weaving Spiders€¦ · 69), ecology and ecophysiology...

EN59CH25-Hormiga ARI 27 November 2013 16:54

Systematics, Phylogeny,and Evolution ofOrb-Weaving SpidersGustavo Hormiga1,∗ and Charles E. Griswold2

1Department of Biological Sciences, The George Washington University, Washington,DC 20052; email: [email protected] of Entomology, California Academy of Sciences, San Francisco, California 94118;email: [email protected]

Annu. Rev. Entomol. 2014. 59:487–512

First published online as a Review in Advance onOctober 25, 2013

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-011613-162046

Copyright c© 2014 by Annual Reviews.All rights reserved

∗Corresponding author

Keywords

spiders, phylogeny, Orbiculariae, Araneoidea, Palpimanoidea, webs

Abstract

The orb-weaving spiders (Orbiculariae) comprise more than 25% of theapproximately 44,000 known living spider species and produce a remark-able variety of webs. The wheel-shaped orb web is primitive to this clade,but most Orbiculariae make webs hardly recognizable as orbs. Orb-weaversdate at least to the Jurassic. With no evidence for convergence of the orb web,the monophyly of the two typical orb web taxa, the cribellate Deinopoideaand ecribellate Araneoidea, remains problematic, supported only weakly bymolecular 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 comprehensivetaxon sampling, comparative morphology, and new molecular markers arerequired for a better understanding of orb-weaver evolution.

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INTRODUCTION

Ubiquitous, diverse, and exclusively predatory, spiders (Araneae) are among the largest animalgroups and the dominant arthropod predators in most terrestrial ecosystems. About 44,000 spiderspecies have been described to date (149); estimates of the total number of species range from76,000 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 ofspiders. With their highly geometric web designs and their ability to produce as many as sevendifferent types of silk with different functions and mechanical properties (142), orb-weavers havecaptured the attention of biologists and the lay public alike.

The basic architecture of an orb web includes a frame holding radii that support a spirallyarranged sticky thread. The web must absorb the kinetic energy of the intercepted prey andretain 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 ismetabolically expensive to produce and is formed by thousands of fine-looped fibrils woven ona core of two axial fibers (Figure 1g). The adhesive properties of the deinopoid sticky spiral areattained 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 coalescesas regularly spaced droplets around the axial fibers (108) (Figure 1a). Specialized flagelliformglands 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 threadare 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). Cribellarsilk is plesiomorphic relative to the viscid araneoid silk. About 27% of the described extant spiderspecies belong to Orbiculariae, of which the vast majority belong to Araneoidea (18 families and11,997 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 diversityhas 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 transitionfrom horizontal to vertical orb webs (23, 33, 134). Most araneoid species build foraging webs thatare 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(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 1Examples 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.

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www.annualreviews.org • Systematics of Orb-Weaving Spiders 489

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Entelegynae:the largest clade ofaraneomorphscharacterized bycomplex copulatoryorgans in both sexes,including externalcopulatory openings infemales, and bycylindrical silk glands

Synapomorphy:a shared derived trait;provides the empiricalevidence for clades

comprehensive taxon samples; studies treating only subsets of araneoid families (13, 29) remainambiguous. In documenting the current level of understanding of orbicularian phylogeny anddiversity, we aim to expose the major gaps in the phylogenetic knowledge required to build thefoundation for comparative studies. All diversity figures (e.g., number of described taxa) for ex-tant and extinct taxa are from Platnick (120) and Dunlop et al. (37), respectively. The literaturetreating the evolutionary biology of orbicularians is too extensive to be summarized here. Severalrecent works have reviewed a diversity of topics, including silk and webs (20, 32), behavior (25,69), ecology and ecophysiology (105, 146), sociality (91), and neurobiology (16), in which a fewemblematic orb-weaving species figure prominently as study subjects.

ORB WEB MONOPHYLY

Whether ecribellate and cribellate orbs have a single origin or evolved convergently began to berigorously examined in the late 1980s. Most research in the past two decades, based mainly on be-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 questionhave been the analyses of Griswold et al. (59), which tested orbicularian monophyly and placementin a broader entelegyne taxonomic context. Unfortunately, under equal character weights theircladistic analysis neither corroborated nor refuted orbicularian monophyly. Their implied weightanalyses did recover orbicularians as a clade (including Nicodamidae, which do not build orbs andat 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, centersaround the limits of the superfamily Palpimanoidea. Forster & Platnick (48) suggested membershipof a number of araneoid groups in the distantly related Palpimanoidea on the basis of two putativecheliceral synapomorphies: the promarginal peg teeth and the retromarginal gland mounds onthe 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 highlycontroversial hypothesis because it included a subset of families otherwise thought to be membersof the Orbiculariae. Schutt (131, 132) investigated the limits of Araneoidea and Palpimanoideaand concluded that several families included in the Forster and Platnick Palpimanoidea are in factaraneoids (micropholcommatine anapids, holarchaeids, pararchaeids, mimetids, and malkarids).Recent phylogenetic analyses (125) corroborated the placement of these families in Araneoidea,and Wood et al. (147) both corroborated the placement of holarchaeids, pararchaeids, andmimetids in Araneoidea and definitively excluded them from the Palpimanoidea, which compriseonly Archaeidae, Huttoniidae, Mecysmaucheniidae, Palpimanidae, and Stenochilidae. Whereascircumscription of Palpimanoidea appears solved, that of Orbiculariae remains problematic.

The relatively recent surge of cladistic analyses on araneoid families (e.g., 13) have not fullyaddressed orbicularian monophyly. These studies have focused on resolving within-family rela-tionships and have included representatives of a fraction of the families, providing a weak test (orno test) of earlier hypotheses that included a broader sample at the family level. Only the analysesof Lopardo & Hormiga (89), Rix & Harvey (124), and Dimitrov et al. (36) have approached acomprehensive taxon sample, but even these samples (and results) differ. The preponderance ofcomparative data with broad taxon representation suggests that orb-weavers are monophyletic,but support for this hypothesis is weak, resting mainly on the architectural features of the web andthe stereotypical web-building behaviors.

Nonbehavioral evidence for orbicularian monophyly is scarce. One character that might sup-port orbicularian monophyly, albeit incompletely surveyed, is a particular gland morphology in


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MAP: majorampullate silk gland

Haplogynae:a putative clade ofaraneomorphs; sisterto Entelegynae

Spidroin: spider silkstructural proteins;encoded by membersof a diverse genefamily andcharacterized by ahighly repetitivestructure

Opisthothelae: theclade that contains thesister lineagesMygalomorphae andAraneomorphae andincludes all spidersexcept liphistiids

Mygalomorphae:the clade that includesthe tarantulas andtrap-door spiders

Araneomorphae:a large lineage thatincludes all spidersexcept liphistiids andmygalomorphs

RTA clade: a largegroup of entelegynesthat includes manycursorial spiders,characterized byhaving a retrolateraltibial apophysis (RTA)in the male palps

the duct of the major ampullate gland spigot, which controls dragline spinning. Wilson (145)conducted a broad but sparse survey of the major ampullate silk gland (MAP) spigot morphologyacross multiple families. Haplogynes lack any gland. Non-orbicularian entelegynes have a simpleduct operated by a valve-tensor muscle. Uniquely, the orbicularian species studied (an uloborid,two araneids, a linyphiid, three tetragnathids, and two theridiids) have a second valve muscle aswell, the duct-levator, although in a slightly different position. Wilson considered the similarvalves a case of convergence between the cribellate and ecribellate orb-weavers, but this mightbe the lone morphological synapomorphy of Orbiculariae. A study of silk genes concluded thatthe collective combination of the spidroins Flag, MiSp, MaSp1, and MaSp2 in araneoids anddeinopoids suggests a common ancestor equipped with the molecular elements necessary for orbweb construction (52). But shortly thereafter, two types of spidroins were reported in a taran-tula (Theraphosidae), including “Spidroin 2,” classified as a MaSp2-like spidroin, nesting withinorbicularian sequences (19). This finding refuted MaSp2 as an orbicularian synapomorphy, im-plied that MaSp2 spindroins and major ampullate silks are plesiomorphic for Opisthothelae, andsuggested these spindroins must have been present in spiders at the mygalomorph-araneomorphsplit, approximately 240 mya.

Molecular sequence data are helping researchers answer the orbicularian monophyly ques-tion. Using 28S ribosomal sequences for eight araneomorph species, Hausdorf (66) found thatOrbiculariae (represented by four species) are actually paraphyletic by having the RTA clade(two species), instead of the Deinopoidea, as the sister group of Araneoidea. Using sequences ofthe nuclear protein-coding gene elongation factor-1 gamma, Ayoub et al. (12) also found thatorbicularians are paraphyletic with respect to the RTA clade in their parsimony analyses butmonophyletic in maximum-likelihood analyses. More recently, Blackledge et al. (22) addressedorbicularian relationships and monophyly using DNA sequences from six genes, now conven-tional in spider phylogeny (COI, 16S rRNA, 18S rRNA, 28S rRNA, histone H3, and wingless),and morphological and behavioral characters. In their analyses, which included representativesfrom only 12 of the 22 orbicularian families, orbicularian monophyly was recovered (with Nico-damidae nested within Orbiculariae) only when the morphological and behavioral data were in-cluded. Their molecular data suggested orbicularian paraphyly: RTA-clade representatives cameout nested within the orbicularians. Dimitrov et al. (36) provided the first empirical support for themonophyly of Orbiculariae based exclusively on conventional genetic markers for a broad higher-level taxon sample, but the cladistic support offered by these markers is slender. Furthermore,these nucleotide data fail to resolve relationships among orbicularian families: Most deeper andinterfamilial internodes are very short and lack statistical support. Using the same conventionalmarkers, a molecular analysis designed to test the placement of psechrids (an RTA-clade lin-eage) found Orbiculariae either paraphyletic (Bayesian) or monophyletic (maximum likelihood),depending on the analytical method (5). Informative nucleotide data would be extremely use-ful, because a number of araneoid lineages have been difficult to place using morphological data(or the conventional markers) and their exact positions have varied across studies (87, 89). Or-bicularian phylogeny is an inherently difficult problem to resolve, both for morphological andgenetic data, because it involves ancient cladogenetic events compressed in a relatively narrowtime span. Ayoub et al. (12) estimated that the orb-weavers originated around 200 mya. Averdam(11), assuming a molecular clock for hemocyanin data, estimated divergence time between anorbicularian (Nephila) and an RTA-clade member (Cupiennius sp.) to be 213–231 mya. Dimitrovet al. (36) suggested a Triassic origin of orb-weavers and a Late Jurassic–Early Cretaceous originfor most araneoid families. Finally, whereas orbicularian monophyly or paraphyly (with respect toNicodamidae, or the whole RTA clade) is still unresolved, no evidence favors convergence of theorb web.


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Cribellum: a spinningplate homologous tothe anterior medianspinnerets found incribellate spiders thatproduces dry sticky silk

PLACEMENT OF ORB-WEAVERS AMONG ENTELEGYNES

That the position of Orbiculariae among entelegynes remains unresolved is due in part to thescale of the problem, because identifying the outgroup of orb-weavers involves resolving therelationships of the largest clade of araneomorphs. Resolving Entelegynae relationships requiresadequate comparative data scored across a vast swath of spider diversity, a daunting task owing tothe large number of taxa and characters. The most comprehensive morphological analysis is that ofGriswold et al. (59). Under their equal character weights analysis, the authors found Orbiculariae(including the true palpimanoids Huttoniidae and Archaeidae, but not necessarily Nicodamidae)to be sister to all entelegynes except Eresoidea. Under implied weights analysis, Orbiculariae (nownot including the two true palpimanoids) were sister to Eresoidea (Eresidae and Oecobiidae) andnicodamids fell outside Orbiculariae as sister to the Divided Cribellum clade. The most inclusivemolecular analysis is that of Dimitrov et al. (36), who found that the sister group of Orbiculariaeis a large clade that included the RTA clade sister to Hersiliidae + Oecobiidae (and this moreinclusive clade is sister to Eresidae), but the nodal support was also low. In sum, given the lowsupport, topologically this problem remains a four-clade polytomy: Orbiculariae, Hersiliidae +Oecobiidae, RTA clade, and Eresidae (Figure 2a).

OVERVIEW OF INTERFAMILIAL RELATIONSHIPS OF ORBICULARIAE

Since Griswold et al. (57), only three analyses have used taxonomic samples broad enough to testinterfamilial relationships (36, 89, 125). Here we attempt to synthesize our current understandingof orbicularian interrelationships, recognizing the problems of conflicting results.

Deinopoidea

Although the morphological analyses of Griswold et al. (57) and Lopardo & Hormiga (89)did not test the monophyly of Deinopoidea per se, it did suggest six putative synapomorphies.Griswold et al. (59) also found deinopoids monophyletic under equal character weights, but underimplied weights Uloboridae were sister to Araneoidea, rendering Deinopoidea paraphyletic. Themolecular analysis of Blackledge et al. (22) contested Deinopoidea monophyly: Deinopidae weresister to Nicodamidae + Araneoidea, this clade was sister to the RTA clade, and uloborids weresister to a lineage that contained the RTA clade and the remaining orbicularians. Only addition ofa sparsely scored morphological data matrix resulted in deinopoid monophyly, although the nodalsupport was low. According to Dimitrov et al. (36), Deinopoidea are monophyletic, with lowclade support, but small analytical variations result in the loss of deinopoid monophyly (in theirpreferred topology Uloboridae are sister to Araneoidea + Nicodamidae, rendering Deinopoideaparaphyletic). At this time the monophyly of Deinopoidea remains dubious.

Nicodamidae

The classification history of nicodamids is complex: Ecribellate species from Australia had beenassociated with theridiids, which they resemble superficially, and the cribellates from New Zealandwere associated with dictynids (46, 85), hence the name Megadictyna. Forster (46) was the first toassociate the cribellate and ecribellate taxa in the Nicodamidae. Griswold et al. (59) suggested thata unique form of the male palpal tibial apophysis is synapomorphic for Nicodamidae. Griswoldet al. (58) grouped Nicodamidae with Phyxelididae and Titanoecidae, although the authors notedthat “[i]n one alternative parsimonious topology for this dataset. . . the orbicularian sister group is


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1

2

3

Deinopidae

Uloboridae

Nicodamidae

Holarchaeidae

Pararchaeidae

Malkaridae

Araneidae

Nephilidae

Tetragnathidae

Mimetidae

Linyphiidae

Pimoidae

Theridiidae

Nesticidae

Synotaxidae

Cyatholipidae

Synaphridae

Theridiosomatidae

Mysmenidae

Anapidae

Symphytognathidae

Deinopoidea

Araneoidea

Eresidae

RTA clade

Hersiliidae

Oecobiidae

Orbiculariae

Palpimanoidea

Entelegynae

Orbiculariae

a

b

Linyphioids

Theridioids

Symphytognathoids

Figure 2(a) The position of Orbiculariae among entelegynes; internal branches in orange denote low bootstrap support (modified withpermission from Reference 46). (b) Summary cladogram of interfamilial relationships of Orbiculariae based on the nine mostcomprehensive phylogenetic analyses of morphological and/or sequence data published to date (see text for references). Each node issupported by at least one study. Polytomies represent conflicting hypotheses (except in the case of Holarchaeidae, Pararchaeidae, andMalkaridae, which have not been included in sufficiently taxon-dense analyses to resolve their placement within Araneoidea).� “Spineless Femur” clade, � “Truncate Sternum” clade, � “Clawless Female Palp” clade.

Nicodamidae (Megadictyna),” thus associating Nicodamidae with the orbicularian problem. Latermorphological analyses were inconclusive for placement of nicodamids: Griswold et al. (59) placedthem either in Orbiculariae (equal weights) or sister to the Divided Cribellum clade (impliedweights). Molecular analyses generally associate nicodamids with orbicularians (36, 60, 101) andsupport nicodamid monophyly (36).


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PLS: posterior lateralspinneret

Araneoid Monophyly

Araneoidea monophyly is well supported by both morphological and molecular data. AlthoughGriswold et al. (59) found homoplasious occurrences in nonorb-weaver species of some classic ara-neoid characters (such as the serrate accessory claw setae and imbricate/squamate cuticle), severalunambiguous morphological synapomorphies support Araneoidea, most notably the paracymbiumand flagelliform and aggregate silk glands (57, 89). The placement of Mimetidae in Araneoideais further corroborated by the presence of a putative vestigial homolog of either the aggregate orthe flagelliform spigot (138).

Araneoid Interfamilial Relationships

Araneidae and Nephilidae are often recovered as sister groups (13, 35, 36). Among the potential(yet homoplasious) synapomorphies for this clade are the female chelicerae with denticles, susten-taculum, and vertical orb webs. The placement of the nephilids as sister to tetragnathids (74) is notsupported by recent analyses (35). The Oarcinae, a small lineage of Chilean mimetid-like spiders,are nested within Araneidae, to which they were formally transferred from the Mimetidae on thebasis of molecular evidence (36). Wunderlich (150) split the araneid genus Zygiella into four generaand proposed that these genera, along with the tetragnathid genus Chrysometa, belong to a newfamily (“Zygiellidae”). “Zygiellidae” monophyly has been consistently refuted by all phylogeneticanalyses so far (36). Mimetidae (pirate spiders), Tetragnathidae, and the Arkyinae [a group witha convoluted taxonomic history, formerly placed in the argiopoid clade of Araneidae (51, 128)]form a clade (22, 35, 36).

The monophyly of linyphioids (Linyphiidae + Pimoidae) has been corroborated by analysescombining morphology and multigene data (10). The placement of Cyatholipidae compromiseslinyphioids in some molecular analyses (36), although this may be an artifact of poor sampling.Linyphioid morphological synapomorphies include the cheliceral stridulatory striae, patella–tibiaautospasy, and possibly the sheet web. The ultrastructure of spermatozoa (96) has addedadditional empirical support to this clade (a 9 + 0 axonemal pattern in all linyphioids studied sofar). Although Li & Wunderlich (86) erected a new araneoid family (Sinopimoidae) for a singlespecies from China, the apparent absence of conductor and median apophysis suggests that thegenus Sinopimoa is a member of Linyphiidae, possibly an erigonine (73), so there is no empiricalsupport for the family rank.

The informal label symphytognathoids was used by Griswold et al. (57) for a clade that in-cludes the families Theridiosomatidae, Mysmenidae, Anapidae, and Symphytognathidae, and issupported mainly by behavioral characters: the out-of-plane radii, the modification of the webafter laying down the sticky spiral, and the doubly attached egg sacs (28, 38, 39). Additionalsupport came from modifications of the fourth tarsal median claw found in most symphytog-nathoids. Symphytognathoid monophyly has never been recovered by any subsequent analysesbased on DNA data for a sufficiently dense taxon sample. Recent work, using morphologicaland nucleotide sequence data, has been driven by studies on micropholcommatine anapids (124–126) and on mysmenids (87). Rix & Harvey (124) revised micropholcommatine classification andphylogeny, erecting 12 new genera (for a total of 18 genera in this subfamily). In an extendedmorphological reanalysis of Griswold et al. (57) and Lopardo & Hormiga (89), these authorsproposed a new name for the clade uniting Anapidae, Symphytognathidae, “teutoniellids,” and“Micropholcommatidae” [EbCY clade, in reference to the enlarged basal cylindrical gland in theposterior lateral spinneret (PLS)]. Their micropholcommatine clade (which they treated at the


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family rank) was circumscribed to exclude “teutoniellids” (Teutoniella and its relatives). Rix &Harvey (124) aptly pointed out that anapids, which are poorly known phylogenetically, are “atthe center of all problems ‘symphytognathidan’ in nature.” Lopardo et al.’s (87) analyses, withthe most dense symphytognathoid taxon sampling to date, did not recover this clade when onlyDNA data were analyzed but did support symphytognathoid monophyly with extensive morpho-logical and behavioral characters. Dimitrov et al.’s (36) analyses, using a much denser outgroupsample, suggest that results from Lopardo et al. (87) might not simply be an artifact of outgroupsampling: Only Symphytognathidae (represented by four species) were monophyletic in anal-yses by Dimitrov et al. (36). Mysmenidae, represented by 15 species, were not monophyletic,due to a single species (Trogloneta sp.) moving out of an otherwise well-supported lineage withall other mysmenids. Theridiosomatidae and Anapidae came out polyphyletic, but the supportvalues of most of the nodes involved in their polyphyly are very low. An analysis using 18Sand 28S rRNA sequences and a smaller taxon sample did not resolve this problem either (125).Lopardo et al. (87) did demonstrate that micropholcommatines are nested within Anapidae [assuggested by Schutt (132)] and that a family rank for this clade would render the latter fam-ily paraphyletic, so consequently micropholcommatines were synonymized with Anapidae. Theircombined analysis also supports in part the monophyly and the relationships of symphytognathoidsproposed by Griswold et al. (57), as modified by Schutt (132). Theridiosomatidae are sister to aclade with all other symphytognathoid families, informally known as the Anterior Tracheal Sys-tem (ANTS) clade. Mysmenidae are sister to a clade composed of Synaphridae and Anapidae +Symphytognathidae.

The sister group relationship between Nesticidae and Theridiidae (a clade informally knownas theridioids) is well supported in cladistic analyses of morphological and behavioral data (3,57), but such a clade has not been recovered in any molecular analyses. Unambiguous theridioidsynapomorphies include the lobed PLS aggregate silk gland glands, the cobweb, and sticky silk ongum-foot lines (3). Distribution of the famous theridiid tarsal comb is more complex: A specializedform occurs in theridiids other than hadrotarsines, whereas a comb of curved, serrate setae areshared between theridioids and at least the genus Synotaxus (3).

Several other families (Synotaxidae, Cyatholipidae, Synaphridae, Holarchaeidae, Pararchaei-dae, and Malkaridae) have been placed consistently in the Araneoidea, but their relationships toother families have shown conflict or have remained ambiguous. Synotaxidae affinities have beenexamined in morphological analyses, though each with incomplete taxon samples: Griswold et al.(57) and Agnarsson (2) suggested a relation to Cyatholipidae on the basis of the cup-like paracym-bium, whereas Lopardo & Hormiga (89) placed them as outgroup to the clawless female clade.Synotaxus has been included in some molecular analyses (9, 10, 36), but these studies could notrobustly resolve its phylogenetic placement within Araneoidea. Lopardo & Hormiga (89) placedCyatholipidae with Synaphridae. Molecular analyses have not yet resolved placement of Cy-atholipidae within Araneoidea (36, 125). Synaphridae were suggested to be sister to Anapidae +Symphytognathidae (87), a hypothesis considered tentative because this study did not includemolecular data for synaphrids and the taxonomic sample did not include any cyatholipids. Nosynaphrids have been sequenced so far.

Placement of the Pararchaeidae among the Araneoidea is still unresolved, though Schutt(131) suggested a relation to Malkaridae in her armored clade (which also included Anapidae).Wunderlich (150) suggested that malkarids belong to a clade that includes mimetids, pararchaeids,and holarchaeids on the basis of the presence of cheliceral peg teeth. Recent molecular analyses(36, 125) have not found holarchaeids and pararchaeids to be close relatives: The mysteriousholarchaeids may be related to some anapids of Tasmania (36). On the basis of this discussion, wepropose a tree that summarizes our limited knowledge of orbicularian phylogeny (Figure 2b).


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ORBICULARIAN FAMILIES

Deinopoidea: The Cribellate Orb Builders

Deinopidae build a characteristic highly modified and reduced orb web (27) with cribellate capturesilk manipulated by the spider’s first and second legs (Figure 1g). At least in Deinopis the posteriormedian eyes are greatly enlarged, hence the name ogre-faced spiders. Extant deinopids comprisetwo genera and 60 species and are distributed worldwide in the tropics and subtropics. The oldestfossils come from Cretaceous Lebanese amber, but deinopids are also known from Baltic andDominican amber. Highly autapomorphic morphology and behavior mean the monophyly ofDeinopidae has never been in doubt: Synapomorphies (89) include the loss of the conductor fromthe male palp and the unique modified orb web. Menneus has been revised and its phylogeny wasreconstructed on the basis of morphological and behavioral data (30). Although deinopid webarchitecture is unique, Coddington (27) interpreted their web-building behaviors as homologousto those of other orb weavers and thus was able to recognize deinopoids as orb builders.

Uloboridae are a worldwide family comprising 18 extant genera and 266 species. They have arich and ancient fossil record; the oldest species come from Cretaceous deposits in Spain, Myanmar,and New Jersey. Uloborids are among the few spiders to lack venom glands, instead relying onwrap attack to subdue prey (43, 144). Uloborids are the only spiders that build typical orb webswith cribellate capture lines, although some genera make webs reduced to a triangle (Hyptiotes) or asingle sticky line (Miagrammopes). They exhibit all stereotypical behaviors of constructing the orbweb. Uniquely, tertiary radii are doubled during orb construction (28, 38). Hyptiotes gertschi hasan unusually long small-subunit ribosomal RNA (18S rRNA) sequence (136), among the longest18S genes sequenced in any arachnid. Opell’s (106) morphology-based cladogram for Uloboridaegenera has yet to be superseded and has no molecular counterpart. Sequence data also supportuloborid monophyly (36). Uloboridae has been a model family for the study of histology andmorphology of spinning organs (81, 118), of webs and silk (109), and of morphological changesaccompanying web modification (107). Some genera are in great need of modern revision (e.g.,Miagrammopes). The lack of taxonomic work in some areas of the world, such as Asia and Australia,suggests that a significant fraction of uloborid diversity remains to be discovered.

Araneidae

Araneids, particularly the genera Araneus and Argiope, are model organisms in arachnology andare among the most intensively studied. The family is diverse morphologically, ecologically, andbehaviorally. Most araneids weave typical orbs (Figure 1a), including some of the largest orb webs,although web architecture is highly variable and some species have dramatically reduced foragingwebs or have abandoned them altogether. Nevertheless, the biology of most araneid species re-mains little-studied. For example, more than 120 years have separated the original description ofthe Malagasy spider Exechocentrus lancearius and the discovery that it uses a highly modified bolasweb and chemical mimicry to capture its prey (129) (Figure 1i). Araneidae currently have morethan 3,000 species in 170 genera, but many more species are predicted to exist, as demonstratedby revisionary work in tropical Asia (130) and Australia (50). The araneid fossil record dates to theLower Cretaceous but the majority of the approximately 70 described species come from Balticand Dominican amber (127). Araneids have long been recognized as a natural group. Putativearaneid synapomorphies include the radix in the male palp and the narrow posterior median eyetapetum. The most thorough phylogenetic study of araneids remains the analysis of Scharff &Coddington (128). Subsequent analyses have built on this matrix, mainly to infer the placement of


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one or a few genera (51), sometimes for analyses at the genus level (e.g., 92). None of the molecularanalyses of Blackledge et al. (22) recovered the monophyly of Araneidae. An expanded taxon sam-ple with the same markers (36) recovered araneid monophyly with relatively high clade supportand suggested also that nephilids are their sister group. This analysis showed that the “mimetid”subfamily Oarcinae (with two genera and eight species from Chile and Argentina) was nestedwithin Araneidae. Oarcines may be web-invading predators on other spiders (S. Lew, personalcommunication; C. Griswold, personal observation). Much of what is known about spider biologyis based on the study of a few araneid species. Given this large, diverse, and increasing body ofdata, future work should focus on building a phylogenetic framework for comparative studies.

Nephilidae

Nephilids are a small lineage of primarily large to very large (their leg span is up to ∼10 cm)orb-weaving spiders that inhabit tropical and subtropical regions. Four genera and 61 species arecataloged. All genera but Nephila (Clitaetra, Herennia, and Nephilengys, 23 species in total) have beenrevised (34, 82, 83). Given the conspicuous nature of most species and the intense attention theyhave received, nephilids are among the few orbicularian clades considered unlikely to significantlyincrease in species number. The number of valid species will certainly decline when Nephila,currently 38 species, is formally revised and monographed, as junior synonyms abound (65). Thenephilid fossil record, although sparse, dates to the Middle Jurassic; some Cretaceous fossils existbut are poorly preserved. The fossil taxa that clearly suggest nephilid membership are mainly fromBaltic and Dominican amber (37, 149, 150). The discovery of the beautifully preserved Nephilajurassica (135), in strata from Inner Mongolia, makes it the oldest orb-weaving spider (as well asthe largest fossil spider) and thus important for dating phylogenetic events. The monophyly of thefour extant nephilid genera is well supported by morphological (74, 84), molecular (13, 36), andcombined analyses (13, 35). Nephilid synapomorphies include the striated cheliceral boss surfaceand the presence of the nonsticky spiral in the finished web (74, 84). Although for most of itstaxonomic history this group was considered a subfamily of Araneidae, Nephilinae were raised tofamily rank on the basis of cladistic analyses that suggested that the lineage is not closely relatedto Tetragnathidae, where at the time they were classified, and also because the available data didnot resolve their placement in Araneoidea (82). Regarding the latter issue, there has been someprogress, as analyses using sequence data and morphology indicate that nephilids are indeed alineage of araneids; that is, Araneidae and Nephilidae are sister groups (13, 36). For this reasonit has been suggested that nephilines should be returned to their original subfamily rank withinAraneidae to better reflect their phylogenetic position and evolutionary history (36). Nephilidphylogenetic relationships at the species level are relatively well understood (84). Although nopublished molecular phylogeny for the group exists, molecular and combined analyses that haveincluded representative species of all nephilid genera indicate that the clade comprising Herenniaplus Nephilengys is the sister group of Nephila (13, 34, 36). Some species of Nephila have beenintensively studied in a diversity of contexts (16, 20, 25, 32, 69).

Tetragnathidae

Tetragnathids build typical orb webs with open hubs that are often oriented horizontally ratherthan vertically; a few species have abandoned foraging webs (54). This worldwide family com-prises 957 species in 47 genera, but a large proportion of taxa remain undescribed. Althoughfossil tetragnathids date back to the Early Cretaceous (134, 144), most fossils have been foundin Dominican and Baltic amber (37, 117, 149, 150). The monophyly of Tetragnathidae is well


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supported. The most notable morphological synapomorphies are the conductor wrapping theembolus and the absence of a median apophysis. Phylogenetic work on tetragnathids has usedmorphological, behavioral, and molecular data and has identified some well-supported lineages(Tetragnathinae, Metainae, Leucauginae, and the Nanometa clade), but the relationships amongthese clades remain poorly resolved (13, 35). Despite extensive taxonomic work on the family, thetwo largest genera, Tetragnatha and Leucauge, are in dire need of world revisions. A few species inboth genera have played prominent roles in studies of behavior and ecology (69). Future work ontetragnathid higher-level systematics should focus on resolving subfamilial relationships and theplacement of several genera of uncertain affinities, such as Azilia and Chrysometa. Further researchis needed to test the hypothesis, based on sequence data (36), that the Arkyinae are the sister groupof Tetragnathidae. This, along with the notion that mimetids, arkyines, and tetragnathids form aclade, is important for understanding character and life-history evolution in Tetragnathidae.

Mimetidae

Mimetids are a small lineage (13 genera and 156 described species) of araneoids that do not buildforaging webs (Figure 1h). Many species use web-invading aggressive mimicry to prey on otherspiders, often araneids and theridiids (77). Although the natural history of most species is unknown,mimetids are not exclusively araneophagic: Substantial insectivory, kleptoparasitism, and oophagyhave also been documented (78). The mimetid fossil record is scarce and consists of mostly Balticand Dominican amber species in extant genera (62). The oldest fossil is from the Eocene CambayFormation of India (115). Because the fossil record of their sister group (Tetragnathidae) goes backto the Early Cretaceous, mimetids are predicted to be at least as old as tetragnathids. The mostconspicuous synapomorphy of Mimetidae is their characteristic prolateral spination pattern of thetibiae and metatarsi of the first and second legs, in which long macrosetae alternate with rows ofshorter macrosetae. Harms & Harvey (63) studied the Australasian mimetid fauna and carried outa morphological cladistic analysis of Australomimetus, the only one published for the family. Theirwork suggests that mimetids and malkarids have abandoned web-based foraging strategies inde-pendently. Future research on mimetids should include both revisionary and phylogenetic analysesand detailed studies of morphology and behavior, especially for poorly known tropical species.

Linyphioids

Linyphioids include the sister families Pimoidae and Linyphiidae; the latter group is the largestfamily-rank lineage of Orbiculariae. Pimoids are a relictual group of sheet web builders in westernNorth America, Asia, and southern Europe. Pimoidae comprise four genera and 37 extant speciesand probably had a broader Holarctic distribution (70, 72, 143). So far six fossil species of Pimoahave been described from Baltic amber (150). Pimoid monophyly and phylogenetic relationshipshave been based on morphological characters (70, 73, 76); synapomorphies include the ectalmarginal cymbial process, often with cymbial cuspules (or modified macrosetae) and a uniquecymbial sclerite (10). The monophyly and intergeneric relationships of pimoids, based on a subsetof the genera used in morphological analyses, have been largely corroborated by Dimitrov et al.(36). Most of the recent newly discovered pimoid taxa come from Asia. Future inventory work inthe Himalayas and elsewhere should yield additional pimoid species.

Linyphiids are diverse and cosmopolitan, with peak diversity in northern temperate andcolder regions, where they account for a large fraction of spider species richness. Approximately4,400 species in 590 genera have been described. Fossil taxa are known from Baltic and Domini-can amber; the oldest fossil is a putative “micronetine” described from Cretaceous-age Lebanese


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AG: aggregate silkgland

amber (116). Linyphiid webs are often built as a sheet (Figure 1f ), with various elaborations suchas an upper and lower scaffolding (or none at all), but very few detailed descriptions of their webconstruction exist (18, 72). Compared with other araneoids, linyphiids have a relatively uniformsomatic morphology, but their genitalia, especially in males, are among the most complex known,so it is not surprising that genitalic features dominate phylogenetic morphological character ma-trices. Many male Erigoninae species have bizarre cephalic modifications (71), which provide richfodder for studies of sexual selection (97). The monophyly of linyphiids is well established onthe basis of morphological data (10, 75, 104). Synapomorphies supporting Linyphiidae includethe suprategulum and the absence of the araneoid median apophysis and conductor (10). WithinLinyphiidae, the monophyly of the subfamilies Mynogleninae and Erigoninae is also robustlysupported on the basis of morphological (71, 104) and molecular data (10). Much cladistic workon linyphiids has focused on Erigoninae, the largest linyphiid subfamily (71, 104, 140).

Theridioids

Theridiidae comprise one of the largest spider families. The seemingly endless accumulation oftheridiid singletons in surveys of tropical spider communities (137) suggests that the total numberof theridiid species will be much greater than the 2,351 total recognized today. Theridiids arefound worldwide; the living fauna is classified into 121 genera and there is an extensive fossilfauna going back to the Cretaceous. Morphological (3) and molecular (9) phylogenies largelyagree, except for the placement of the ant-eating subfamily Hadrotarsinae. Theridiid synapomor-phies include the loss of the paracymbium, a bulb-cymbium lock mechanism, and highly flattenedanterior PLS aggregate silk gland (AG) spigots (3). Theridiids are among the behaviorally andmorphologically most diverse families. The widow spiders, comprising as many as 40 species ofLatrodectus, include species dangerous to humans (53, 141). Theridiidae provide model organismsfor the study of mating systems (98) and include several well-studied instances of sexual canni-balism (7, 8), sometimes obligate (45), and male genital mutilation (79, 80, 98). Maternal care iswidespread in theridiids and is hypothesized to have led through parallel paths to kleptoparasitismand araneophagy in argyrodines (3). There are also more instances of social behavior in Theridi-idae than in any other spider family, again probably related to maternal care (3, 4). Theridiidwebs are highly diverse (Figure 1j,k), both among and within species (17, 42). Whereas somebehaviors may be homologized to those of other Orbiculariae, the sticky silk wrap attack andprovision of gum-foot lines appear unique to theridiids and nesticids. Nesticidae by contrast aremuch less rich than Theridiidae (209 described extant species). They are found worldwide (butnot in Madagascar and New Zealand) and comprise nine genera. Their fossil record goes back tothe Palaeogene and are known from Baltic and Dominican amber. Synapomorphies of Nesticidaeinclude the small anterior median eyes and a unique, enlarged paracymbium. Nesticid webs andprey capture behavior are similar to that of theridiids, including star-shaped cobwebs and stickysilk wrap attack (3). Nesticids have received far less study than theridiids,but are model organismsfor the evolution of troglophily (cave dwelling) (67). Future systematic work on theridioids shouldaddress the undescribed fraction of their diversity, but even for described species work remains tobe done. For example, Latrodectus includes some of the most emblematic spiders of indisputablemedical importance yet is in need of a modern monographic treatment.

Symphytognathoid Families

We report here progress on the systematics of the families Theridiosomatidae (16 gen-era, 89 species), Mysmenidae (23 genera, 123 species), Anapidae (including the subfamily


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Micropholcommatinae; 57 genera, 219 species in total), and Symphytognathidae (7 genera,66 species). Symphytognathoids are small spiders, including the smallest on record (in Sym-phytognathidae), that are morphologically diverse and poorly studied, due in part to their smallsize and often cryptic lifestyles. Their webs are highly modified and variable, within and amongfamilies, ranging from small orbs (Figure 1d,j,k) to sheets to three-dimensional ovoid orb webs,with out-of-plane radii (Figure 1e). Some species in this clade, such as several in the SouthAmerican–African vicariant mysmenid clade Mysmenopsis and Isela, are web-less kleptoparasitesthat inhabit webs of other spiders. This rich diversity of web architectures and the concomitantstereotypical web-building behaviors have provided a fruitful source of phylogenetic characters(39, 57, 60, 89, 122), but the evolution of web architecture in symphytognathoids is insufficientlyunderstood. The fossil record of symphytognathoids goes back to the Cretaceous, with the old-est theridiosomatid fossils from the Lower Cretaceous. Most fossils in this family come fromBaltic, Bitterfeld, Dominican, and Myanmar amber. Anapid fossils date to the Paleogene and aremostly from Baltic amber, and mysmenid fossils are mostly from Baltic and Dominican amber andMalagasy copal. There is no fossil record of Symphytognathidae. The most thorough examina-tion of symphytognathoid phylogeny (87), although focused on Mysmenidae, includes represen-tatives of all symphytognathoid families and combines morphological, behavioral, and moleculardata.

We provide here some of the synapomorphies of these families (87), although few of thesemorphological synapomorphies are exempt from homoplasy. Theridiosomatidae synapomorphiesinclude sternal pits and long trichobothria on third and fourth tibiae. The monophyly of Mys-menidae is supported by the metatarsal clasping spine of males and the cymbium oriented ventrallyor prolatero-ventrally on the palp and distinctly modified prolaterally and/or apically into an inter-nal cymbial conductor. In addition, mysmenid females have a distinct modification (a sclerotizedspot or a projection) on the apical ventral surface of the femur. Anapidae (including Micropholcom-matinae) synapomorphies include the absence of a paracymbium, the pore-bearing prosomal pits,and the internal female copulatory openings. Synapomorphies of Symphytognathidae include theloss of anterior median eyes, one or two promarginal cheliceral teeth originating from a commonbase or raised plate, and the reduced palp of females. The traditional symphytognathoid diagnos-tic feature, the chelicerae fused along the midline (47), was ambiguously optimized as a familysynapomorphy. A three-dimensional orb is the ancestral architecture for symphytognathoids butthe evolutionary chronicle of web architecture is complex (87). For example, the three-dimensionalwebs of the mysmenid Maymena, which are similar to those of most anapids, have most likelyevolved convergently in these two groups. The planar orb web evolved twice independently fromthree-dimensional orb webs, by the loss of the above-the-plane radii (Symphytognathidae anddistal Anapidae). The ancestral orb web has been secondarily and independently modified into asheet or cobweb at least three times in symphytognathoids. The unique, spherical web of mostMysmeninae evolved once and was never lost. Given the incomplete status of this group, futurestudies on symphytognathoids will require a revision of these hypotheses, as well as hypothesesrelating to kleptoparasitism, which has evolved independently at least three times within the sym-phytognathoid clade: in mysmenids, inferred to have originated a single time, in anapids and insymphytognathids (87). Future research on symphytognathoids should continue to address theirlargely undocumented diversity. A study of the Gaoligong Mountains of China (103), in whichsix new genera and 36 new species were described, provides a window into how taxonomic workmay dramatically increase symphytognathid diversity. Similar surveys in other areas will increasethe number of taxa and shed light on the phylogenetic relationships of these minute and crypticspiders.


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CY: cylindrical(tubiliform) silk gland

Synotaxidae

Synotaxids are mostly slender, long-legged spiders resembling theridiids. Synotaxus, from theAmerican tropics, builds a unique and highly autapomorphic vertical chicken-wire or chain-linkweb of modular units using sticky silk (2, 15, 41, 57). Other synotaxids occur mostly in the tem-perate parts of South America, Australia, and New Zealand, building sheet or dome webs beneathwhich they hang (Figure 1c), although some are tiny kleptoparasites that inhabit webs of otherspiders (C. Griswold & G. Hormiga, personal observation). The extant Synotaxidae comprise14 genera and 82 species; there is also a rich fossil record extending back to the Oligocene fromBaltic and German amber. Forster et al. (49) first recognized synotaxids as a distinct lineage. Syno-taxid synapomorphies (89) include the cymbial retromargin with a groove, a cup-like paracymbium,and a complex, terminal conductor on the male palp. Synotaxid monophyly remains controversial:Synotaxus has spinning organs similar to theridioids, with enlarged PLS AG and two PLS cylindri-cal (tubiliform) silk gland (CY) spigots, whereas in Physogleninae and Pahorinae the PLS has smallAG spigots and only one CY spigot, similar to Cyatholipidae. The study of the Australian fauna willundoubtedly continue to uncover new taxa (44). Future work should test whether these two lineageswith dramatically different webs (synotaxines versus pahorines and physoglenines) are a clade.

Cyatholipidae

This relictual family of 23 extant genera and 58 extant species is scattered across the temperateand tropical mountain areas of Africa, Madagascar, Australia, and New Zealand. The family alsohas a rich European fossil record from Oligocene to Miocene amber deposits from Germany andthe Baltic. Cyatholipids make sheet webs and hang beneath them (Figure 1b); males retain thearaneoid PLS triplet and are frequently found beneath webs with adult or juvenile females, oreven alone. Cyatholipid synapomorphies (89) include a laterally expanded cymbium, a cup-likeparacymbium, and the unique cymbial retromedian process. Griswold (56) revised the world fauna,provided a cladogram for the extant species and genera, and examined some European fossils.Living cyatholipids comprise two main clades: One is disjunct between Africa, Madagascar, andNew Zealand, and the other is unique to Australia. The Australian cyatholipids may be related toextinct Baltic genera. Cyatholipidae are exemplars of Afromontane biogeography, disjunct amongscattered localities in temperate southern Africa and mountains in tropical Africa, with two cladesdisjunct between the Eastern Arc Mountains of tropical Africa and Madagascar (55, 56). Thelarge proportion of monotypic genera and distribution across inaccessible areas of tropical Africapromise many more species to be discovered.

Synaphridae

Synaphrids were originally described as a subfamily of Anapidae (149) but were subsequently ele-vated to family rank (95). This is a small (3 genera and 13 species), cryptic, and poorly known groupof araneoids from southern Europe, the Middle East, and Africa (Canary Islands, Madagascar).Some species build sheet webs, but the biology of most synaphrids remains unknown. Synaphridaeare represented in the fossil record by a single species from Baltic amber. Support for the mono-phyly of the family is robust. Lopardo et al. (87) proposed 23 synapomorphies for Synaphridae,including a wide and advanced posterior spiracular opening, a modified tracheal system, and ametatarsus-tarsus joint with both segment tips constricted (90). Most recent taxonomic work onsynaphrids has come from regional or isolated studies (88, 100). Because elucidating their phy-logenetic placement is critical to understanding araneoid evolution, future studies should focus


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on obtaining genetic data, documenting web architecture, and expanding the meager taxonomicknowledge base.

Malkaridae

Since the discovery of this family in Australia in 1980, malkarids have remained very poorly known.Malkarids are leaf-litter inhabitants and do not seem to build foraging webs. The group includes11 named species, one in Chile and the rest in Australia. At least a dozen species, all new, exist inNew Zealand, and numerous Australian species of Malkara, currently a monotypic genus, awaitdescription (G. Hormiga & N. Scharff, unpublished data). No fossil record exists for this family.Synapomorphies of Malkaridae include a conductor flange in the male palp, deep alveolations onthe carapace, and the presence of a small unsclerotized area behind the epigastric furrow (121). Inaddition to revisionary work, future research should focus on finding the closest relatives of thiscryptic family and assessing whether the similarities between malkarids and mimetids are due toa common origin or convergence.

Holarchaeidae and Pararchaeidae: Erstwhile Palpimanoids

Holarchaeidae comprise a small family (one genus with two species) of minute spiders fromTasmania and New Zealand with no known fossil record. Holarchaeids have been collected invery moist places, either by sieving moss and leaf litter (150) or by beating shrubbery or collectingthem from silk lines on ferns during rain (123; C. Griswold, personal observation). Their biologyis otherwise unknown: They appear to lack venom glands, with no obvious pore at the endof the fang (48), and lack the PLS triplet necessary for producing viscid sticky silk. Potentialsynapomorphies for Holarchaeidae may be the elongate chelicerae arising from a distinct butventrally unsclerotized foramen, a swollen (anteriorly projecting) clypeus, and the widened femalepedipalps. More members of this rarely collected family likely await discovery (112).

Pararchaeidae are small spiders and comprise 2 species from New Zealand, 32 species fromAustralia, and one species from New Caledonia from seven genera. There is no fossil record. Manyare found in moist areas, but in Australia some species occur in the semiarid interior of the country.They are sometimes called snap-jaw spiders because of their predatory behavior. The cheliceraeare spread widely; when prey contact a set of trigger hairs, the jaws snap together quickly (123).This seems adapted to capture fast-moving prey and is convergent with the palpimanoid trap-jawspiders (Mecysmaucheniidae) (147, 148): Perhaps similar rearrangements in the carapace musclesof these families accommodate the chelicerae reorientation and gape that have led to the raisedcephalic region of both families (147). Pararchaeidae have been collected from single lines and donot seem to make webs for prey capture; indeed, the spinning complement is reduced, but uniquelywithin the Araneoidea, they retain two MAP spigots for spinning draglines. Synapomorphies forPararchaeidae may include the cheliceral trigger hairs and peg teeth and the elevated chelicerae,which arise from a distinct, fully sclerotized foramen in the cephalothorax. Rix (123) recentlymonographed Pararchaeidae.

Extinct Orbicularian Families

Five fossil orbicularian families have been described, all of which are classified within Araneoidea,and approximately a dozen species are grouped in six genera (37, 117). Because of its age, perhapsthe most significant is Juraraneidae, with a single specimen from the Jurassic (Juraraneus rasnit-syni ). A redescription of this specimen (133) suggests the presence of a functional calamistrum (no


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cribellum is visible) and postulates that J. rasnitsyni is a cribellate araneoid, possibly an araneid,but evidence that this animal was cribellate is inconclusive. The remaining fossil families (Baltsuc-cinidae, Pumiliopimoidae, Praetheridiidae, and Protheridiidae) are all from Baltic amber, exceptProtheridiidae, which are also represented by a species from Cretaceous Jordanian amber. Fossilorbicularian taxa have extinct morphological features, and recent advances in X-ray computedtomography have enabled detailed morphological descriptions of minute fossil specimens (114,115), but no fossil families have been studied at this level. So far, fossils have contributed little toresolve phylogenetic relationships. This is due in part to the absence of fossil species in quantita-tive phylogenetic analyses (but see 127, 147). The main contribution of fossils has been to offer atemporal scale to spider diversification (116) and to provide calibration points to estimate the ageof events in molecular phylogenies (12, 36, 148).

Nicodamidae: Beyond the Orb Web?

Nicodamidae comprise a morphologically and behaviorally disparate family known only from9 genera and 29 extant species (64). All Australian representatives are ecribellate and seem tobe cursorial, whereas the two New Zealand species, each in its own genus (Megadictyna andForstertyna), make substrate-limited cribellate sheet webs for prey capture (59, 64). Megadictynawebs are indistinguishable architecturally from many RTA-clade spiders, e.g., Phyxelididae.The placement of Nicodamidae is unsettled: molecular analyses have suggested (22, 36) thatnicodamids nest within Orbiculariae, as the sister to Araneoidea. This latter phylogenetichypothesis implies a notable course of web evolution from the primitive, homologous orb ofdeinopoids and araneoids to a substrate-limited sheet of cribellate nicodamids, unrecognizablearchitecturally as an orb, with consequent loss of any foraging web in the ecribellate species. Theevolution of the whole RTA clade from an orbicularian ancestor is thus conceivable.

EVOLUTION OF ORBS

Several shortcomings prevent researchers from understanding the evolution of the orb web. Thestereotypical web-building behavior of a few species, which mainly produce typical orbs, is wellknown but there has been a bias against nonorb orbicularians in ethological studies. The poorresolution of interfamilial relationships limits inferences about web evolution. The picture is likelyto be intricate, as suggested by the complex paths of web evolution in symphytognathoids (87).How the sticky glue araneoid orb web evolved is also mysterious. This complex multicharactertrait is hypothesized as a key innovation to explain the increase in diversity of Araneoidea (23).Suggested advantages of the araneoid orb include viscous adhesive capture spiral (lower cost andincreased stickiness, strength, and extensibility) (108), flat and low UV reflectance of silk (websare less visible to insects) (33), web function in dim and bright-light environments (31, 33), andthe vertical orientation of webs (intercepts more prey) (40). No transitional webs between thecribellate and viscid orbs are known, and until recently there has been no hypothesis about howsuch transitions in the composition of prey capture thread may have occurred. Opell et al. (111)suggested an evolutionary pathway from the dry, cribellate orb web of deinopoids to the stickyglue orb web of araneoids (see sidebar, The Protoaraneoid Hypothesis).

ORBICULARIAN SYSTEMATICS: PROSPECTS AND CHALLENGES

Advancing our understanding of orbicularian phylogeny and systematics faces a number of chal-lenges. Spiders, including the orb-weavers, remain largely undescribed. Estimating the actual


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THE PROTOARANEOID HYPOTHESIS

When second instar uloborid spiderlings emerge from egg sacs, they cannot produce cribellar silk (because they lacka cribellum) and they build horizontal sheet webs with a framework of threads and a temporary spiral covered withnonsticky radii. In contrast, second instar araneoids build orb webs with a sticky spiral. Opell et al. (111) hypothesizedthat viscid glue evolved to enable second instars to construct orb webs, and that early araneoids (“protoaraneoids”)may have spun composite cribellar-viscous capture threads. It seems unlikely that deinopoid second instar sheetwebs can work in vertical positions because the secondary radii are not anchored to the temporary spiral. Thishypothesis requires that viscid silk and the cribellate fibrils can combine to form a functional adhesive system andthat the stickiness of this composite silk fiber must have been similar (or better) to that of the two components.Opell et al. artificially created composite cribellar-viscous fibers and measured their stickiness. The stickiness of thecomposite threads was greater than that of either native cribellar or viscid threads alone. Aggregate glands may haveevolved to provide a viscous coating to the axial fibers of second instars so that a typical orb web could be built. Ifthe cribellum and the calamistrum continued to function after the aggregate glands appeared, a functional capturethread could still be spun. The presence of axial fibers covered by viscous material would not have interfered withthe spinning of a composite cribellar-viscous thread.

diversity is an academic exercise in itself (93), but regardless of the estimates (1, 61, 119), there islittle doubt that a significant fraction of spider and orbicularian diversity remains to be discovered.As evidenced by a cursory look at most modern revisionary work, what is “known” is fragmentary,as it is often based on a few museum specimens and whatever has been recorded on the specimenlabel. In other words, the number of “known” species is only a small subset of the number of“described” species. This problem is aggravated by the biodiversity crisis and accelerating ratesof biological extinction (24). Given the narrow geographic distribution of many tropical orbic-ularians (e.g., 99), it seems plausible that with habitat loss many species are vanishing withoutever having been collected. Inventory work and targeted collecting (with specimens suitable forboth morphological and molecular work) remain essential, and thus a priority, for the future ofsystematic studies. Part of such efforts should include documenting natural history traits, such asweb architecture; these data should be included in taxonomic monographs (e.g., 103). Biodiver-sity informatics combined with cybertaxonomic approaches will make descriptive taxonomic datamore accessible, comprehensive, and usable (102).

During the past 15 years, arachnologists have collected an extraordinary amount of new com-parative data on orbicularians. These efforts have been facilitated by advances in digital imagingand an increased reliance on scanning electron microscopy and advances in micro-CT scanning,combined with the rigor “imposed” by the current practice of compiling data in character matricesfor phylogenetic analysis. Except for the reanalyses by Lopardo & Hormiga (89) and Rix & Harvey(124), the study by Griswold et al. (57) remains the most taxon-rich inquiry into the relationships oforbicularian families using morphological data alone. Orbicularian morphological phylogeneticshas indeed raised the quality bar, as evidenced by the high number of characters scored in matrices(e.g., 357 morphological characters in Reference 87) and the extensive level of character documen-tation (e.g., more than 850 images in Reference 14). But these high standards in turn have become adaunting challenge for scoring an updated morphological matrix of orbicularian families and theirrelatives. Much of the morphological (and behavioral) variation described (and scattered acrossmore narrowly focused studies) remains to be assessed in a broad phylogenetic context. Perhaps notsurprisingly, the most taxon-rich analyses of orbicularian relationships have used genetic markersthat could be sequenced across a broad range of species. As discussed above, the results at the level


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of interfamilial relationships have been mixed, if not disappointing, in many instances owing tothe limited resolving power of these loci. Advances in genomics facilitated by the broad use ofnext-generation sequencing should advance orbicularian molecular systematics rapidly and offerpromise for recovering ancient nodes, thus elucidating interfamilial relationships and providing ro-bust support for clades. For example, Hedin et al. (68), using 350 orthologous genes from Illuminatranscriptomes, showed the utility of these methods to resolve the deep divergences of Opiliones,an arachnid group older than spiders but one order of magnitude less diverse. Their study achievedresolution in the deepest areas of the cladogram where traditional sequencing techniques oftenfailed. Transcriptome-based sequencing approaches are not without problems and challenges (e.g.,contig assembly, alternative splicing, and orthology recognition), but the field is advancing rapidly(6) and has more stringent specimen requirements that should be taken into account for the futuregrowth of research collections. Because recollecting all relevant taxa is neither practical nor feasi-ble, the existing ethanol collections must be used for target-gene capture techniques (94) or withthe developing technology, for whole-genome sequencing. When this diversity of approaches anddata is combined, we can expect a clearer image of the evolutionary chronicle and the underlyingdiversity patterns that have resulted in one of the most extraordinary radiations of animals.

SUMMARY POINTS

1. Orb web monophyly is uncontested, but Orbiculariae monophyly is only weakly sup-ported and paraphyly with respect to the RTA clade cannot be ruled out.

2. Orbicularians are of at least Jurassic age, making them one of the oldest major lineagesof spiders.

3. Molecular and morphological data together circumscribe the Palpimanoidea to includeonly Archaeidae, Huttoniidae, Mecysmaucheniidae, Palpimanidae, and Stenochilidae;former palpimanoid members Holarchaeidae, Micropholcommatinae, Mimetidae, andPararchaeidae nest within the Araneoidea.

4. Araneoidea monophyly is robustly supported, but relationships among several includedfamilies have yet to be resolved.

5. The orb web is primitive relative to many other web forms, e.g., sheets, but web evolutionwithin Orbiculariae is likely to be more complex than envisioned by Griswold et al. (57).Reduced orbs, aerial sheets, and substrate-limited sheets may have evolved in parallelmultiple times.

6. Currently available molecular and morphological data are insufficient to robustly resolverelationships among orbicularian families. New sources of data are needed.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We thank many of our colleagues and students for fruitful discussions during the past fifteenyears. Miquel Arnedo, May Berenbaum, Gonzalo Giribet, Lara Lopardo, Jeremy Miller, and two


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anonymous reviewers provided comments and feedback on this article. Ligia Benavides assistedwith the references and Thiago Moreira assembled the webs plate. GH was supported by USNSF grants DEB 1144492 and DEB 114417 (to GH and Gonzalo Giribet) and by a SelectiveExcellence Grant from The George Washington University. CG acknowledges generous supportfrom the Schlinger Foundation.

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EN59-FrontMatter ARI 27 November 2013 17:34

Annual Review ofEntomology

Volume 59, 2014Contents

Nancy E. Beckage (1950–2012): Pioneer in InsectHost-Parasite InteractionsLynn M. Riddiford and Bruce A. Webb � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Emerald Ash Borer Invasion of North America: History, Biology,Ecology, Impacts, and ManagementDaniel A. Herms and Deborah G. McCullough � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �13

Invasion Biology of Aedes japonicus japonicus (Diptera: Culicidae)Michael G. Kaufman and Dina M. Fonseca � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �31

Death Valley, Drosophila, and the Devonian ToolkitMichael H. Dickinson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �51

Mosquito DiapauseDavid L. Denlinger and Peter A. Armbruster � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �73

Insect Mitochondrial Genomics: Implications for Evolution andPhylogenyStephen L. Cameron � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �95

Response of Native Insect Communities to Invasive PlantsT. Martijn Bezemer, Jeffrey A. Harvey, and James T. Cronin � � � � � � � � � � � � � � � � � � � � � � � � � 119

Freshwater Biodiversity and Aquatic Insect DiversificationKlaas-Douwe B. Dijkstra, Michael T. Monaghan, and Steffen U. Pauls � � � � � � � � � � � � � � � 143

Organization and Functional Roles of the Central Complex in the InsectBrainKeram Pfeiffer and Uwe Homberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 165

Interactions Between Insect Herbivores and Plant Mating SystemsDavid E. Carr and Micky D. Eubanks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 185

Genetic Control of MosquitoesLuke Alphey � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 205

Molecular Mechanisms of Phase Change in LocustsXianhui Wang and Le Kang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 225

vii

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EN59-FrontMatter ARI 27 November 2013 17:34

Traumatic Insemination in Terrestrial ArthropodsNikolai J. Tatarnic, Gerasimos Cassis, and Michael T. Siva-Jothy � � � � � � � � � � � � � � � � � � � � � 245

Behavioral Assays for Studies of Host Plant Choice and Adaptation inHerbivorous InsectsLisa M. Knolhoff and David G. Heckel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 263

Biology and Management of Psocids Infesting Stored ProductsManoj K. Nayak, Patrick J. Collins, James E. Throne, and Jin-Jun Wang � � � � � � � � � � � � 279

Chemical Ecology of Bumble BeesManfred Ayasse and Stefan Jarau � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 299

Model Systems, Taxonomic Bias, and Sexual Selection: Beyond DrosophilaMarlene Zuk, Francisco Garcia-Gonzalez, Marie Elisabeth Herberstein,

and Leigh W. Simmons � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 321

Insect Speciation Rules: Unifying Concepts in Speciation ResearchSean P. Mullen and Kerry L. Shaw � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 339

Neural and Hormonal Control of Postecdysial Behaviors in InsectsBenjamin H. White and John Ewer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Using Semifield Studies to Examine the Effects of Pesticides on MobileTerrestrial InvertebratesS. Macfadyen, J.E. Banks, J.D. Stark, and A.P. Davies � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 383

The Development and Functions of OenocytesRami Makki, Einat Cinnamon, and Alex P. Gould � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 405

Sexual Selection in Complex EnvironmentsChristine W. Miller and Erik I. Svensson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 427

Significance and Control of the Poultry Red Mite, Dermanyssus gallinaeO.A.E. Sparagano, D.R. George, D.W.J. Harrington, and A. Giangaspero � � � � � � � � � � � 447

Evolutionary Interaction Networks of Insect Pathogenic FungiJacobus J. Boomsma, Annette B. Jensen, Nicolai V. Meyling, and Jørgen Eilenberg � � � 467

Systematics, Phylogeny, and Evolution of Orb-Weaving SpidersGustavo Hormiga and Charles E. Griswold � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 487

Advances in Silkworm Studies Accelerated by the Genome Sequencingof Bombyx moriQingyou Xia, Sheng Li, and Qili Feng � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 513

The Role of Mites in Insect-Fungus AssociationsR.W. Hofstetter and J.C. Moser � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 537

Movement of Entomophagous Arthropods in Agricultural Landscapes:Links to Pest SuppressionN.A. Schellhorn, F.J.J.A. Bianchi, and C.L. Hsu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 559

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ANNUAL REVIEWSIt’s about time. Your time. It’s time well spent.

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Statistical and Computational Issues, Martin J. Wainwright

• High-Dimensional Statistics with a View Toward Applications in Biology, Peter Bühlmann, Markus Kalisch, Lukas Meier

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