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The Female Genital Morphology of the Orb Weaving Spider Genus Agriognatha (Araneae, Tetragnathidae)

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The Female Genital Morphology of the Orb Weaving Spider Genus Agriognatha (Araneae, Tetragnathidae) JOURNAL OF MORPHOLOGY 268:758–770 (2007) The Female Genital Morphology of the Orb Weaving Spider Genus Agriognatha (Araneae, Tetragnathidae) Dimitar Dimitrov,* Fernando Alvarez-Padilla, and Gustavo Hormiga Department of Biological Sciences, The George Washington University, Washington, D.C. 20052 ABSTRACT The female genital morphology of the spi- imply an understanding of the basic genital mor- ders in the araneoid genus Agriognatha (Tetragna- phology. Most taxonomic illustrations are done thidae) is described and illustrated. The female genitalia with the goal of depicting species diagnostic fea- of Agriognatha is characterized by a strong reduction of tures and do not necessarily provide the informa- the sperm storage organs (spermathecae) and by the pres- tion needed to understand genital morphology. ence of a specialized distal compartment of the median membranous chamber that functions as a sperm storage This is particularly true for species with complex organ (the posterior sac). The genital morphology of genital structures. This problem is also common Agriognatha species is unique among Tetragnathidae and for the descriptive work of species in which the it provides robust synapomorphic evidence for the mono- females present a low degree of sclerotization of phyly of genus. We discuss the phylogenetic implications the genitalia and do not have a well sclerotized of these new findings for the placement and monophyly epigynum (the sclerotized region that covers the of Agriognatha and for the monophyly of Tetragnathinae. internal genitalia), although there are a number of J. Morphol. 268:758–770, 2007. Ó 2007 Wiley-Liss, Inc. notable exceptions (e.g., Uhl, 1994, 2000; Michalik et al., 2005; Burger et al., 2003, 2006). It is not KEY WORDS: Tetragnathinae; spermathecae; homology; uncommon in taxonomic descriptions of the sperm storage; haplogyne; reduction females of such species to have their genital mor- phology insufficiently described and poorly illus- trated. The spider genus Agriognatha Cambridge, It has been known since the seventeenth century 1896 (Tetragnathidae) is a good example of this that different spider species differ in their genital problem. Agriognatha (Fig. 1) is a small genus of morphology. The first author to document spider Tetragnathinae spiders known from Central and genitalia in a taxonomic work was Clerck (1757), South America. Currently ten species are known who illustrated the male palp of some, but not all, to belong in Agriognatha, but ongoing research on the species he described in his monograph on the taxonomy on this genus will increase the num- Swedish spiders. Although the morphology of the ber to over 20 species (Dimitrov and Hormiga, per- female genitalia is also diagnostic for the species, sonal observation). Agriognatha females do not Clerck did not illustrate it. The morphology of cop- have an epigynum and the internal genital struc- ulatory organs in spiders is widely used now as tures are weakly sclerotized, a condition that is one of the most important diagnostic character typical of the members of the subfamily Tetragna- systems, especially at the species level (e.g., Plat- thinae. This low degree of sclerotization makes nick, 1975; Griswold, 1993; Foelix, 1996; see also morphological observations of the female genitalia Huber, 2004). The morphology of the copulatory of Agriognatha species difficult. Despite the avail- organs is also used in phylogenetic studies and in ability of female specimens in the original descrip- most of the recently published cladistic matrices it tions of several Agriognatha species the female accounts for more than half of the character data genital morphology is not discussed or illustrated (e.g., Griswold, 1990, 1993; Hormiga, 1994, 2000; at all (Bryant, 1940, 1945). Furthermore, two spe- Wang, 2002; Ramı´rez, 2003; Miller and Hormiga, 2004; Dimitrov and Ribera, in press; see Huber, 2004 for further discussion). Contract grant sponsor: U.S. National Science Foundation; Con- Despite their central role in spider systematics, tract grant numbers: DEB-0328644, EAR-0228699; Contract grant sponsors: Research Enhancement Fund and The George Washing- the copulatory organs of many species are poorly ton University. studied and their morphology is not well under- stood. This problem is not exclusive of old taxo- *Correspondence to: Dimitar Dimitrov, Department of Biological nomic treatments: it is not uncommon in modern Sciences, The George Washington University, WA, D.C. 20052. taxonomic revisions to find genital illustrations E-mail: [email protected] that are insufficient to understand the basic mor- Published online 30 May 2007 in phology of the species in question. Illustrating gen- Wiley InterScience (www.interscience.wiley.com) ital diagnostic characters does not necessarily DOI: 10.1002/jmor.10543 Ó 2007 WILEY-LISS, INC. FEMALE GENITAL MORPHOLOGY OF AGRIOGNATHA 759 Fig. 1. Agriognatha rucilla in its web. Dominican Republic. Photo by Gustavo Hormiga. cies have been described from single female speci- type there are separate ducts for the seminal fluid mens but without providing a description or illus- to enter and leave (Austad, 1984). The haplogyne trations of the internal female genitalia (Cam- condition is primitive and consequently a symple- bridge, 1889; Mello-Leita˜o, 1947). siomorphy in Haplogynae. The entelegyne condi- Spiders in the large Araneoclada lineage (a clade tion is derived (apomorphic) and thus it provides that includes about 90% of the known spider spe- support to the monophyly of Entelegynae. Never- cies; see (Coddington et al., 2004) have been classi- theless this ‘‘division’’ is far from perfect: a number cally divided into two groups: Haplogynae and of taxa within Entelegynae have evolved haplo- Entelegynae (Simon, 1892; Wiehle, 1967; Platnick gyne genitalia (e.g., some tetragnathines; see et al., 1991; Uhl, 2002; but see Griswold et al., below) and some members of Haplogynae have fer- 2005). Support for these two groups, since they tilization ducts, such as some pholcids (Huber, were first proposed by Simon (1892), has come in 1997) or some tetrablemmids (Burger et al., 2006). part from the genital morphology. In haplogynes It seems clear that the notion that these two line- the female sperm storage organs (spermathecae) ages have somewhat uniform female genitalia is open to only one set of ducts, which function both not empirically supported (Uhl, 2002). as copulatory and fertilization ducts (or in some Most species of the family Tetragnathidae, as species, there are no ducts at all, as in the family well as the rest of araneoid spiders, have entele- Pholcidae). In entelegyne spiders the spermathe- gyne genitalia (but note that the exact circum- cae open to the exterior by means of the so-called scription of Araneoidea awaits resolution; see Gris- copulatory ducts and a separate set of ducts (the wold et al., 2005). In the tetragnathid subfamily fertilization ducts) connect the spermathecae to Tetragnathinae (which includes the genera Tetrag- the uterus externus. Haplogynes and entelegynes natha, Agriognatha, Glenognatha, and Pachygna- have been said to have ‘‘cul-de-sac’’ and ‘‘conduit’’ tha, among others; see Hormiga et al., 1995) the spermathecae, respectively, because in the first haplogyne condition has evolved independently of type of spermathecae the seminal fluid enters and that found in the Haplogynae clade and the basal exits through the same duct and in the second araneomorph lineages: the fertilization ducts have Journal of Morphology DOI 10.1002/jmor 760 D. DIMITROV ET AL. Fig. 2. The internal female genitalia of Agriognatha rucilla. SEM. (A) Dorsal view. Scale bar 30 lm. (B) Close up view of the cuticle of the posterior sac. Scale bar 2 lm. (C) Lateral view. Scale bar 100 lm. (D) Copulatory duct dorso-lateral view. Scale bar 10 lm. (E) Frontal view. Scale bar 10 lm. (F) Long ductules of the copulatory duct. Scale bar 1 lm. BL booklung. been secondarily lost and there has been a general the results under certain character weighting simplification of the female genital structures. analyses suggest that they may be primitively Such simplification of the entelegyne genitalia to a haplogyne (Griswold et al., 2005: Fig. 219). Primi- secondary haplogyny condition is a rare evolution- tive haplogyny had been previously proposed for ary event. Secondary haplogyny probably evolved Archaeidae (Forster and Platnick, 1984) but in independently several times within the entele- the light of the new evidence presented by Gris- gyne group, e.g., in the families Archaeidae and wold et al. (2005) both hypotheses are plausible. Huttoniidae. However, the phylogenetic place- Despite the enormous advances brought by the ment of these two families is still unresolved and work of Griswold et al. (2005), the answer to this Journal of Morphology DOI 10.1002/jmor FEMALE GENITAL MORPHOLOGY OF AGRIOGNATHA 761 Fig. 3. The internal female genitalia of Agriognatha espanola. SEM. (A) Dorsal view. Scale bar 100 lm. (B) Close up view of the cuticle of the posterior sac. Scale bar 10 lm. (C) Close up view of the cuticle of the median sac. Scale bar 2 lm. (D) Copulatory duct, fronto-lateral view. Scale bar 10 lm. (E) Copulatory duct, close up. Scale bar 10 lm. (F) Frontal view. Scale bar. 10 lm. question requires a more resolved and robust phy- nal female genitalia exhibited a very atypical mor- logenetic hypothesis. phology. The most unusual observation, together During the course of systematic studies of tet- with the reduced spermathecae, was the presence
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