Cladistics Blackwell Publishing Cladistics 23 (2007) 1–71 10.1111/j.1096-0031.2007.00176.x Phylogeny of extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing morphological and ethological homologies Matjazˇ Kuntner1,2* , Jonathan A. Coddington1 and Gustavo Hormiga2 1Department of Entomology, National Museum of Natural History, Smithsonian Institution, NHB-105, PO Box 37012, Washington, DC 20013-7012, USA; 2Department of Biological Sciences, The George Washington University, 2023 G St NW, Washington, DC 20052, USA Accepted 11 May 2007 The Pantropical spider clade Nephilidae is famous for its extreme sexual size dimorphism, for constructing the largest orb-webs known, and for unusual sexual behaviors, which include emasculation and extreme polygamy. We synthesize the available data for the genera Nephila, Nephilengys, Herennia and Clitaetra to produce the first species level phylogeny of the family. We score 231 characters (197 morphological, 34 behavioral) for 61 taxa: 32 of the 37 known nephilid species plus two Phonognatha and one Deliochus species, 10 tetragnathid outgroups, nine araneids, and one genus each of Nesticidae, Theridiidae, Theridiosomatidae, Linyphiidae, Pimoidae, Uloboridae and Deinopidae. Four most parsimonious trees resulted, among which successive weighting preferred one ingroup topology. Neither an analysis of an alternative data set based on different morphological interpretations, nor separate analyses of morphology and behavior are superior to the total evidence analysis, which we therefore propose as the working hypothesis of nephilid relationships, and the basis for classification. Ingroup generic relationships are (Clitaetra (Herennia (Nephila, Nephilengys))). Deliochus and Phonognatha group with Araneidae rather than Nephilidae. Nephilidae is sister to all other araneoids (contra most recent literature). Ethological data, although difficult to obtain and thus frequently missing for rare taxa, are phylogenetically informative. We explore the evolution of selected morphological and behavioral characters, discuss and redefine the homology of palpal sclerites, disprove semientelegyny in spiders, trace the newly interpreted evolution of the orb web, and show that nephilid genital morphologies coevolve with sexual behaviors and extreme sexual size dimorphism. Phylogenetic interpretations of behavior suggest new insights into spider biology and avenues for future research. Ó The Willi Hennig Society 2007. Discovery of behavioral homologies has importance for biology (Fig. 1C,D) (Vollrath, 1980, 1998; Vollrath and Parker, and other human endeavors far beyond simply adding charac- 1992, 1997; Coddington, 1994; Coddington et al., 1997; ters for phylogenetic analyses. Greene (1994) Hormiga et al., 2000; Ramos et al., 2005), their unique Golden orb-weaving spiders (Nephila) and hermit webs of more than a meter diameter, and their unusual spiders (Nephilengys) are among the most prominent sexual behaviors (see Kuntner, 2007a,b), which may and most researched tropical arachnids (reviewed in involve sexual cannibalism by the female and ‘‘oppor- Kuntner, 2005, 2006, 2007a; Harvey et al., 2007). They tunistic’’ mating by the male when the female is teneral are famous for extreme sexual size dimorphism in which or feeding. The closely related genera Clitaetra (Fig. 1H) males are many times smaller than the giant females and Herennia (Fig. 1F,G) both build rectangular ladder webs with parallel side frames, and Herennia exhibits male sexual mutilation and epigynal plugging, which *Corresponding author: remain poorly understood but have interesting evolu- E-mail address: [email protected] tionary implications (Kuntner, 2005, 2006). The appar- Present address: Institute of Biology, Scientific Research Center of the ently Gondwanan nephilids are now treated as a family Slovenian Academy of Sciences and Arts, Novi trg 2, PO Box 306, SI- 1001 Ljubljana, Slovenia (see Kuntner, 2005, 2006, 2007a,b; Platnick, 2006), but Ó The Willi Hennig Society 2007 2 M. Kuntner et al. / Cladistics 23 (2007) 1–71 ABC D E F G H Fig. 1. Photographs of live nephilid spiders. (A–C) Pantropical genus Nephila (golden orb spider): (A) N. senegalensis, female from South Africa; (B) N. inaurata, female from South Africa; (C) N. clavipes, female (large) and male (small) from Costa Rica. (D, E) Pantropical genus Nephilengys (hermit spider): (D) N. borbonica, female (large) and male (small) from Madagascar; (E) N. cruentata, female from South Africa. (F, G) Australasian genus Herennia (coin spider): (F) H. etruscilla, female from Java; (G) H. multipuncta, female from Sri Lanka. (H) Afrotropical genus Clitaetra: C. irenae, female from South Africa. M. Kuntner et al. / Cladistics 23 (2007) 1–71 3 were formerly and occasionally still are treated as a 1993) and spider web architecture (Eberhard, 1982; tetragnathid subfamily (Nephilinae Simon, 1894). The Coddington, 1986a,b,c, 1989, 1990; Hormiga et al., genera Nephila (especially the common New World N. 1995; Griswold et al., 1998; Agnarsson, 2004; Kuntner, clavipes (Linnaeus, 1767)) and Nephilengys have been 2005, 2006, 2007a). This study makes extensive use of the subject of over 2000 studies (Google Scholar) both direct and indirect observations of behavior coded covering many aspects of their biology, and their as discrete characters, combines them with the evidence popularity has resulted in many species synonymies from morphology, and explores the usefulness of ethol- (Kuntner, 2007a; Kuntner, in preparation). For exam- ogy in araneoid spider phylogenetics. The results suggest ple, in the upcoming Nephila revision, Kuntner (in that behavioral data, while difficult to obtain (and thus preparation) will recognize only 15 valid species out of prone to the problem of missing entries), are phyloge- the over 150 available species-level names (Platnick, netically informative, and, in the case of nephilids, less 2006). homoplasious than morphology. Nephilids formerly contained eight genera placed as a subfamily in Tetragnathidae Menge, 1866 (Platnick, Prior work 1997). The first steps towards a species-level phylogeny were the removal of the African Singafrotypa and the The encyclopedic treatise of world spiders by Euge` ne Oriental Perilla from Nephilinae to Araneidae (Kuntner Simon (1892–1894) included a large family Argiopidae, and Hormiga, 2002; Kuntner, 2002), and the revisions of approximately equivalent in composition to today’s Herennia, Clitaetra and Nephilengys (Kuntner, 2005, Araneoidea. Simon’s argiopid subfamily Nephilinae 2006, 2007a). These revisions included species-level (Simon, 1894, p. 744) consisted of: phylogenetic analyses designed primarily to test the 1 Phonognatheae Simon (1894); with Phonognatha monophyly of nephilids and the genus being revised. Simon (1894); Singotypa Simon (1894) and Deliochus The Australian Deliochus and Phonognatha have not Simon (1894); been revised, and their phylogenetic position remains 2 Nephileae Simon (1894); with Nephila Leach (1815) controversial (Kuntner, 2005, 2006). The prior analyses (including Nephilengys L. Koch, 1872); contained only a subset of Nephila species. Here we 3 Clitaetreae Simon (1894); with Clitaetra Simon include all 15 known, valid Nephila species, based on (1889); two upcoming sources, the Australasian taxonomic 4 Herennieae Simon (1894); with Herennia Thorell treatment by Harvey et al. (2007), and the world (1877). revision of Kuntner (in preparation). Nephilidae now Simon thought the phylogenetic position of nephilids contains only Nephila, Nephilengys, Herennia and Clit- was ambiguous. Based on the ‘‘external genital charac- aetra (Kuntner, 2006; Platnick, 2006). ters’’ Simon (1894, p. 744) hypothesized Nephilinae to be Despite general interest in nephilid biology, the lack of close to tetragnathines (equivalent to Tetragnathidae) any species-level phylogeny has made evolutionary inter- through Phonognatha and to argiopines (equivalent to pretations of the available biological data difficult or the Araneidae) through Herennia. Simon described male impossible. The goals of this study were to test the and female genitalia for representative species of monophyly and composition of Simon’s Nephilinae in the Phonognatha, Herennia and Nephila (including in broadest sense, to reassess the placement of the group fig. 827 the palp of Nephilengys as Nephila malabarensis) within Araneoidea, to propose a species-level phylogeny but did not know the males of Singotypa, Deliochus or for extant species and to examine the homology and Clitaetra. Simon (1894, pp. 744–746) diagnosed Nephil- evolution of selected morphological and behavioral traits. inae by the male palp with a globular bulb (¼ tegulum), Ethological homologies are of broad biological inter- a semicircular basal piece (¼ subtegulum: fig. 827b), a est (Greene, 1994), although phylogenetic studies utiliz- denticulated basal part (¼ paracymbium: fig. 827c) and ing behavior are rare (Wenzel, 1992; Proctor, 1996; a complex distal part (¼ embolic conductor: fig. 827a). Danoff-Burg, 2002; see also Discussion). Behavior has According to Simon, the simple epigynum of some been repeatedly shown to be phylogenetically informa- species resembled that in Meta and the more com- tive (Coddington, 1986a,b,c; Prum, 1990; Wenzel, 1992; plex epigyna of others (Herennia and Nephilengys as deQueiroz and Wimberger, 1993; Proctor, 1996; Price Nephila malabarensis) resembled that in Argiope. and Lanyon, 2002) and its analysis is no different from Simon’s classification is translated into a dendrogram morphology