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Family Ties: Molecular Phylogeny of Crab Spiders (Araneae: Thomisidae)

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Family Ties: Molecular Phylogeny of Crab Spiders (Araneae: Thomisidae) Cladistics Cladistics 24 (2008) 708–722 10.1111/j.1096-0031.2008.00202.x Family ties: molecular phylogeny of crab spiders (Araneae: Thomisidae) Suresh P. Benjamina,b* , Dimitar Dimitrova, Rosemary G. Gillespieb and Gustavo Hormigaa aThe George Washington University, Department of Biological Sciences, 2023 G Street NW, Washington DC, 20052, USA; bUniversity of California, Berkeley, Insect Biology Division—ESPM, 201 Wellman Hall 3112, Berkeley, CA 94720-3112, USA Accepted 2 November 2007 Abstract The first quantitative phylogenetic analysis of three sequenced genes (16S rRNA, cytochrome c oxidase subunit I, histone 3) of 25 genera of crab spiders and 11 outgroups supports the monophyly of Thomisidae. Four lineages within Thomisidae are recovered. They are informally named here as the Borboropactus clade, Epidius clade, Stephanopis clade and the Thomisus clade, pending detailed morphology based cladistic work. The Thomisus clade is recovered as a strongly supported monophyletic group with a minimal genetic divergence. Philodromidae previously widely considered a subfamily of Thomisidae do not group within thomisids and is excluded from Thomisidae. However, Aphantochilinae previously generally considered as a separate family falls within the Thomisus clade and is included in Thomisidae. The recently proposed new family Borboropactidae is rejected, as it is paraphyletic. Ó The Willi Hennig Society 2008. Thomisidae Sundevall, 1833, commonly called crab Gabritschevsky, 1927; Comstock, 1948). Misumena vatia spiders are often cryptically colored sit-and-wait preda- (Clerck, 1757) has a remarkable ability to change color, tors that do not build capture webs (Fig. 1). Thomisidae which takes place during migration to flowers of is the sixth largest spider family. It includes 2062 different color from spring to the early part of summer described species in 171 genera (Platnick, 2007) with (Comstock, 1948). Crab spiders are attracted by fra- many more species remaining to be described. They are grance components of flowers (Aldrich and Barros, mainly active during the day and ambush insects with 1995; Krell and Kraemer, 1998) and use visual and their well-adapted first and second legs (Homann, 1934; tactile cues for selecting flowers (Morse, 1988; Greco Comstock, 1948). Not surprisingly, they are an impor- and Kevan, 1994). They reach their ambush sites in a tant component of terrestrial ecosystems (Riechert, step-by-step process using several draglines and bal- 1974). As predators of agricultural pests, thomisids play looning events (Homann, 1934). an important part in natural pest control (Riechert and There are social crab spiders with maternal care in the Lockley, 1984; Nyffeler and Benz, 1987; Uetz et al., Eucalyptus forest of Australia (Main, 1988; Evans, 1999). 1995). Mother Diaea ergandros Evans (1995), catch Some thomisids (e.g., Misumena, Diaea, Runcinia and larger prey for their own offspring, but not for the Thomisus) possess the ability to change color and blend adopted offspring leading to large size and possibly into their habitat, in most cases flowers (Packard, 1905; better survival rates for the natural offspring (Evans, 1998). Mothers further increase survival of natural offspring by producing trophic oocytes used in a system *Corresponding author: of sacrificial care (Evans, 1998). E-mail address: [email protected] Present address: Department of Entomology, National Museum of Myrmecomorphism is known in a number of thomis- Natural History NHB 105, PO Box 37012, Smithsonian Institution, ids: Strigoplus albostriatus Simon, 1885, Amyciaea Washington, DC 20013-7012, USA. forticeps (O.P.-Cambridge, 1873), A. lineatipes Ó The Willi Hennig Society 2008 S. P. Benjamin et al. / Cladistics 24 (2008) 708–722 709 A B CD Fig. 1. Living thomisids sampled in this study. (A) ‘‘Monaeses’’ sp. A, Sri Lanka, Central Province; (B) Diaea placata, Sri Lanka, Western Province (not sampled); (C) Oxytate taprobane, Sri Lanka, Central Province; (D) ‘‘Lysiteles’’ sp. B, Sri Lanka, Central Province. All photos by SPB. O.P.-Cambridge, 1901 and Aphantochilus rogersi that did not fit into the above categories were included O.P.-Cambridge, 1870, are known to be ant mimics. in Misumeninae and Philodrominae. Species groups A. forticeps is of the same color as the ant Oecophylla were then formed within these subfamilies based on eye smaragdina and bears on the posterior part of the pattern and shape of prosoma. abdomen a pair of eye-like spots that correspond to eyes Since Simon (1892) the understanding of generic of the ant (Shelford, 1902). The similarity of A. rogersii relationships has not changed greatly. Holm (1940), on to some spiny South American ants is striking, and the grounds of embryological studies, and Homann forms a further instance of myrmecomorphism (Oliveira (1975), on the grounds of eye morphology, excluded and Sazima, 1984). Philodromids from Thomisidae. Philodromids were Given their ecological significance and appealing later given family status (Ono, 1988), which has been adaptations one would expect to see a plethora of accepted since (but see Roberts, 1995). Separately, phylogenetic studies. However, no such studies of family status was proposed for some thomisids, Steph- thomisids exist. Moreover, understanding the exact anopidae (Pickard-Cambridge, 1871) and Aphantochi- taxonomic limits of this large family has always been lidae (Thorell, 1873). Levi (1982) placed the Thomisidae problematic. Thomisidae was proposed to accommo- in a superfamily along with Aphantochilidae, which was date spiders with legs generally extended sideways not accepted by Ono (1988). In the most current study (laterigrade), instead of being oriented towards the front Thomisidae was separated into seven subfamilies (Ono, or back as in most other spiders. Originally all spiders 1988): Stephanopinae, Thomisinae, Bominae, Stiphro- with laterigrade legs such as Sparassidae and Philodr- podinae, Dietinae, Strophiinae and Aphantochilinae omidae were included. Simon (1892) was the first to using characters proposed by Simon (1892). Recently propose a hypothesis of generic groups for all thomisid (Wunderlich, 2004b) proposed a new family ‘‘Borborop- genera recognized during his time. Although his actidae’’ to include parts of Thomisidae. Thus, to date, ‘‘groups’’ were neither evolutionary nor phylogenetic the monophyly of Thomisidae remains untested. in the modern sense, he provided some information on A great part of our knowledge of evolutionary history Thomisidae morphology and arguments supporting his is derived from phylogenies, reconstructed by sampling ideas. His Stephanopsinae contained spiders with che- and grouping characters. Harvey and Pagel (1991) liceral teeth; Aphantochilinae and Strophiinae con- illustrated the richness of evolutionary questions that tained species with modifications such as elongated can be approached with phylogenies. Our current maxillae related to their ant mimicking habits; Stiphro- understanding of relationships within Thomisidae is podinae included species with an enlarged tarsus; spiders largely based on Simon (1892) and modifications to his 710 S. P. Benjamin et al. / Cladistics 24 (2008) 708–722 ideas by different workers (Schick, 1965; Homann, 1975; (P. Lehtinen, pers. comm.). We have included six species Ono, 1988). However, they do not provide much of Salticidae, one species each of Miturgidae and information, partly because the family has never been Corinnidae in our study. As Philodromidae have been subject to quantitative phylogenetic analysis. Recent in the past included as a subfamily of Thomisidae, we taxonomic work on tropical Asian crab spiders (Tikader, include three philodromid taxa in our study. 1980; Barrion and Litsinger, 1995) added more confu- sion, illustrating the fragile systematic state of the DNA sequencing and alignment family. Here we present the first cladistic analysis of Thom- Genomic DNA was extracted from either fresh or isidae. This analysis of molecular data aims to test the ETOH-preserved leg tissue using the Qiagen DNeasy monophyly of Thomisidae, including the validity of Tissue Kits (Qiagen, Valencia, CA, USA). Otherwise ‘‘Borboropactidae’’ and the placement of some enig- intact spiders, preserved in alcohol have been deposited matic taxa such as Epidius and Cebrenninus, which share as voucher specimens (Table 1). Partial fragments of the characters such as the presence of a conductor and mitochondrial genes cytochrome c oxidase subunit I median apophysis with ‘‘Borboropactidae’’. Epidius was (COI) and 16S rRNA (16S) and the nuclear gene histone provisionally placed in Thomisidae owing to its unusual H3 (H3) were amplified using the following primer pairs: male palp (Benjamin, 2000). Owing to the considerable (COI) C1-J-1751 and C1-N-2191 (Simon et al., 1994) volatility in thomisid systematics and paucity of mor- (16S) LR-N-13398 (Simon et al., 1994) and LR-J-12864 phological information for a large number of taxa, we (Arnedo et al., 2004) and (H3) H3aF and H3aR (Colgan do not formally name any higher-level taxa here. et al., 1998). PCR products were purified using the However, we provide putative morphological synapo- QIAquick PCR Purification Kit (Qiagen) and sequenced morphies for most of the largest clades. The first author directly in both directions using an ABI 3730 automated is presently undertaking a detailed morphological revi- sequencer (Applied Biosystems, Foster City, CA, USA), sion of Thomisidae. in combination with the ABI PRISM Big Dye Termi- nator Cycle Sequencing Ready Reaction
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