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The Phylogenetic Basis of Sexual Size Dimorphism in Orb-Weaving Spiders (Araneae, Orbiculariae)

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The Phylogenetic Basis of Sexual Size Dimorphism in Orb-Weaving Spiders (Araneae, Orbiculariae) Syst. Biol. 49(3):435–462, 2000 The Phylogenetic Basis of Sexual Size Dimorphism in Orb-Weaving Spiders (Araneae, Orbiculariae) GUSTAVO HORMIGA,1,2 NIKOLAJ SCHARFF,3 AND JONATHAN A. CODDINGTON2 1 Department of Biological Sciences, George Washington University, Washington, D.C. 20052, USA; E-mail: [email protected] (address for correspondence) 2Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, USA 3 Department of Entomology, Zoological Museum, University of Copenhagen, Copenhagen, DK 2100, Denmark Abstract.—Extreme sexual body size dimorphism (SSD), in which males are only a small fraction of the size of the females, occurs only in a few, mostly marine, taxonomic groups. Spiders are the only terrestrial group in which small males are relatively common, particularly among orb-weavers (especially in the families Tetragnathidae and Araneidae) and crab spiders (Thomisidae). We used a taxonomic sample of 80 genera to study the phylogenetic patterns (origins and reversals) of SSD in orb-weaving spiders (Orbiculariae). We collected and compiled male and female size data (adult body length) for 536 species. Size data were treated as a continuous character, and ancestral sizes, for males and females separately, were reconstructed by using Wagner parsimony on a cladogram for the 80 genera used in this study. Of these 80 genera, 24 were female-biased dimorphic (twice or more the body length of the male); the remaining 56 genera were monomorphic. Under parsimony only four independent origins of dimorphism are required: in the theridiid genus Tidarren, in the distal nephilines, in the “argiopoid clade,” and in the araneid genus Kaira. Dimorphism has reversed to monomorphism at least seven times, all of them within the large “argiopoid clade.” The four independent origins of dimorphism represent two separate instances of an increase in female size coupled with a decrease of male size (involving only two genera), and two separate instances of an increase in female size with male size either remaining the same or increasing, but not as much as females (involving 30 genera). In orb-weaving spiders, far more taxa are sexually dimorphic as a result of female size increase (22 genera) than as a result of male size decrease (two genera). SSD in orb-weaving spiders encompasses several independent evolutionary histories that together suggest a variety of evolutionary pathways. This multiplicity strongly refutes all efforts thus far to nd a general explanation for either the origin or maintenance (or both) of SSD, because the different pathways very likely will require distinctly different, possibly unique, explanations. Each pattern must be understood historically before its origin and maintenance can be explained in ecological and evolutionary terms. The most frequently cited example of male dwarsm in spiders, the golden orb-weaving spider genus Nephila (Tetragnathidae), is in fact a case of female giantism, not male dwarsm. [Araneae; continuous characters; Orbiculariae; parsimony; sexual size dimorphism; spiders.] Sexual size dimorphism (SSD) is a clas- be >12 times that of the adult males (e.g., sic problem in evolutionary biology, empha- in Nephila pilipes; Robinson and Robinson, sized by Darwin (1871) and addressed by 1973). Extreme sexual body size dimorphism many subsequent authors (see references in is most common among orb-weavers (es- Ghiselin, 1974; Shine, 1989; Hanken and pecially in the families Tetragnathidae and Wake, 1993; Andersson, 1994). Extreme sex- Araneidae) and crab spiders (Thomisidae) ual body size dimorphism, in which males but the phenomenon does not respect taxo- are only a small fraction of the size of the nomic boundaries; other cases can be found females, occurs in only a few, mostly ma- in very disparate spider taxa, including my- rine, taxonomic groups. Bonelliids (Echiura, galomorphs (Main, 1990). Bonelliidae), some barnacles (Cirripedia), Extreme SSD in spiders (by convention, and ceratioid angler shes (Lophiiformes, females at least twice the male size) has several families within Ceratioidea) provide usually been interpreted as male dwarsm classic examples of male miniaturization. (Elgar et al., 1990; Elgar, 1991; Main, 1990; Spiders are the only terrestrial group in Vollrath and Parker, 1992), although alter- which small males are relatively common. In native explanations have been proposed most species of spiders the females are larger (Simon, 1892:753; Gerhardt, 1924) and the than the males. In some cases this dispar- male dwarsm interpretation has recently ity is extreme (Fig. 1), as in the often-cited been disputed (Head, 1995; Hormiga et al., orb-weaving genus Nephila (Tetragnathidae), 1995; Coddington et al., 1997; Scharff and in which the body length of females may Coddington, 1997; Prenter et al., 1997, 1998). 435 436 S YS TE M ATI C BIOLOG Y FIGURE 1. Extreme sexual size dimorphism in orb-weaving spiders. (a) Male (top) and female Nephila clavipes (Tetragnathidae). (b) Male (right) and female Argiope bruennichi (Araneidae). VOL. 49 2000 HORMIGA ET AL.—SEXUAL SIZE DIMORPHISM IN ORB-WEAVING SPIDERS 437 In phylogenetic terms, male dwarsm is, by larians comprise two sister clades ranked as denition, an apomorphic decrease in male superfamilies: the species-poor Deinopoidea size. Although the selective agents that bi- ( 300 species in two families) and the large ologists have invoked to explain this phe- Araneoide» a (some 10,000 species in 12 fami- nomenon vary, male dwarsm hypotheses lies). SSD has been reported in 3 of the 14 or- are alike in focusing only on size change in bicularian families (all of them within Ara- males, despite the obvious fact that SSD is neoidea): Araneidae, Tetragnathidae, and the ratio in size of both sexes. Evolutionarily Theridiidae. Our taxonomic sample includes speaking, changes in either sex can produce 79 genera from nine orbicularian families “dimorphism” and therefore identical size and the outgroup genus Dictyna (80 genera ratios may originate in different ways. Tabu- in total). The araneoid families Cyatholip- lating only body size ratios, without track- idae, Synotaxidae, Anapidae, Symphytog- ing which sex changed and how (increase nathidae, and Mysmenidae were not in- or decrease), may conate different biolog- cluded in our taxonomic sample because ical phenomena that require different expla- all known members are monomorphic and nations. The hypothesis that the SSD of a because representatives of the subclades to particular taxon is due to male dwarsm im- which they belong (the “Spineless femur plies that male size has decreased over evo- clade” and the “Symphytognathoid clade”; lutionary time. This prediction can be tested see Griswold et al., 1998) were included in cladistically by reconstructing the phyloge- the study. The families Araneidae and Tetrag- netic history of size changes in each sex sep- nathidae have been more densely sampled arately, which in turn allows the reconstruc- (57 and 14 genera included, respectively), be- tion of ancestral size ratios under parsimony. cause it is within these two lineages that the Cladistic methods are especially useful be- majority of cases of SSD among orb-weavers cause they can disentangle the contribution can be found and because cladistic analy- of many factors to evolutionary pattern by ses of these two groups are available. Even viewing them in a historical context (Nylin though this is the most comprehensive phy- and Wedell, 1994) and thus clarify the inde- logenetically based analysis of SSD in spi- pendence, distinctiveness, and sequence of ders thus far, the taxonomic sample available evolutionary events. has been constrained to a large extent by the In this paper we use a taxonomic sample available phylogenetic hypotheses. of 80 genera to study the phylogenetic basis The tree topology relating the 80 genera of SSD in orb-weaving spiders (Orbiculariae) used in this study (Fig. 2) is a composite and address the following questions. First, is cladogram that has been derived from three there a common origin ofSSD in orb-weaving of our own quantitative cladistic analy- spiders? Second, if that is not the case, as the ses of araneoid spiders using the logic of taxonomic distribution alone seems to sug- “supertree” techniques (Sanderson et al., gest, how many independent origins of SSD 1998). These three primary sources are have to be hypothesized under parsimony matrix-based cladistic parsimony analyses to explain its current taxonomic distribution? of morphological and behavioral characters Does SSD reverse to monomorphism? How and should be consulted for detailed infor- and where did these differences in size arise mation on phylogenetic relationships, tree during the diversication of orb-weavers? Is choice, and cladistic support. The interfa- each instance of SSD the result of changes in milial and theridioid relationships are from male size, female size, or a combination of Griswold et al. (1998). The original matrix of both? Griswold et al. has 31 taxa scored for 93 char- acters; the parsimony analysis of this data set produces a single minimal-length tree of MATERIALS AND METHODS 170 steps (CI = 0.64, RI = 0.81). Tetragnathid The orb-weaving spiders (Orbiculariae) in- relationships follow Hormiga et al. (1995). clude 14 families and >1000 genera. More The original tetragnathid dataset has 22 taxa than 10,000 species of orbicularians have scored for 60 characters and the parsimony been described so far, accounting for ap- analysis results in three minimal length trees proximately one-third of all described spi- of 130 steps (CI = 0.56, RI = 0.72) that differ ders (Coddington and Levi, 1991). Orbicu- only in the relationships among the outgroup 438 SYSTEMATIC BIOLOGY VOL. 49 FIGURE 2. Cladogram for a taxonomic sample of orb-weaving families and genera of the spider families Tetrag- nathidae and Araneidae (Hormiga et al., 1995; Scharff and Coddington, 1997; Griswold et al., 1998), plus their outgroups. taxa. Hormiga et al. (1995) preferred one of (1997) analysis of 70 taxa and 82 charac- these three most-parsimonious cladograms ters, which results in 16 slightly different (their Fig.
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