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Araneae: Tetragnathidae) in Hawai'il Pacific Science (1997), vol. 51, no. 4: 380-394 © 1997 by University of Hawai'i Press. All rights reserved Phylogenetic Relationships and Adaptive Shifts among Major Clades of Tetragnatha Spiders (Araneae: Tetragnathidae) in Hawai'il ROSEMARY G. GILLESPIE,2 HENRIETTA B. CROOM,3 AND G. LUKE HASTy2 ABSTRACT: The role of adaptive shifts in species formation has been the subject of considerable controversy for many years. Here we examine the phylogeny of a large radiation of Hawaiian spiders in the genus Tetragnatha to determine the extent to which species splitting is associated with shifts in ecological affinity. We use molecular data from ribosomal 12S and cytochrome oxidase mitochondrial DNA, and allozymes to assess phylogenetic affinity. Ecological associations were recorded for all species under study, and shifts are considered in the context of the phylogeny. Results indicate that there are two major clades of Hawaiian Tetragnatha, one of which has abandoned web building (spiny-leg clade), while the other retains the ancestral condition of web building. Within the spiny-leg clade, the molecular information suggests that the species on anyone island are generally most closely related to each other. Preliminary results for the web-building "complex" of species indicate that there may be groups of web builders that have speciated in a similar manner. Results ofthe study suggest that, at least within the spiny-leg clade, matching sets of taxa have evolved independently on the different Hawaiian islands. There appears to have been a one-to-one convergence of the same set of"ecomorph" types on each island in a manner similar to that of lizards of the Caribbean. THE FORMATION OF new species is a key element (Cooke et aI. 1960), crickets (Otte 1994, Shaw in evolutionary advancement and diversification 1995, 1996), and pomace flies (DeSalle 1995, (Mayr 1963). Our research has focused on the Kaneshiro et aI. 1995). However, what makes pattern and process of speciation in a lineage of the Hawaiian archipelago ideal for examination spiders in the Hawaiian Islands. The archipelago of the process of species formation among such offers a unique opportunity for examining radiations is that it consists of a series of volca­ microevolutionary events culminating in the for­ noes arranged within an identifiable chronologi­ mation of species, largely because its extreme cal framework, ranging from Kaua'i, the oldest isolation has allowed repeated and explosive tax­ of the currently high islands, to Hawai'i, the onomic diversification from one or a few ances­ youngest, largest, and highest island (Carson and tors (c. Simon 1987). Such rampant speciation Clague 1995). It is therefore reasonable to con­ is well illustrated in Hawaiian birds (Freed et sider the archipelago as a series of historical al. 1987, Tarr and Fleischer 1995), land snails snapshots, with population divergence being currently instigated on the youngest island and developed on the successively older islands. I This paper is contribution no. 1996-019 of the Hawai'i Biological Survey. The study was supported by grants from One of the keys to understanding the process the Hawai'i Bishop Research Initiative, the Hawai'i Natural of speciation is the elucidation of behavioral Area Reserves System, The Nature Conservancy ofHawai'i, or ecological changes associated with species and the University of Hawai'i Research Council to R.G.G., and NSF BSR-8604969 to H.B.C. Additional support was splitting. Such changes frequently may be linked provided by the Bishop Museum, Haleakala National Park, to sexual selection (e.g., Kaneshiro and Giddings and The Nature Conservancy of Hawai'i. Manuscript 1987). However, where sexual behaviors are less accepted 3 February 1997. apparent, behavioral or ecological changes at 2 Center for Conservation Research and Training, Uni­ versity of Hawai'i at Manoa, Honolulu, Hawai'i 96822. speciation have been most frequently associated 3 Department of Biology, University of the South, with foraging mode (e.g., Grant 1986). For a Sewanee, Tennessee 37383. predator, there are three primary mechanisms 380 Adaptive Shifts in Hawaiian Spiders-GILLESPIE ET AL. 381 through which it could shift foraging mode: (1) extent of the radiation of Tetragnatha in Hawai'i microhabitat selection, which therefore deter­ has been uncovered only recently (Gillespie mines the number and type of prey encountered; 1991a, 1992a, 1994), previously being known (2) behavioral modification in foraging strategy, only from descriptions of a single species by which becomes tailored to a specific prey type; Karsch (1880) and of eight species by E. Simon and (3) morphological modification in feeding (1900, redescribed by Okuma [1988, 1990]), the structures, which become tailored for capture of latter based on Perkins' collections. Over the last a specific prey type. Even the most generalist few years an additional 19 species of Hawaiian predators usually exhibit some form of micro­ Tetragnatha have been described (Gillespie habitat selection; the most specialized exhibit 1991a, 1992a, 1994), and more than 50 new morphological and behavioral adaptations to a "morphospecies" have been collected (Gillespie specific prey type in addition to selecting a and Croom 1995; R.G.G., unpubl. data). This microhabitat in which this prey is likely to occur. species radiation spans a huge spectrum of col­ To what extent are these modifications associ­ ors, shapes, sizes, ecological affinities, and ated with species formation? behaviors. Many are web building (plesiomor­ Our study examines changes in ecological phic for Tetragnatha), with structural modifica­ affinity associated with species splitting for rep­ tions of the abdomen that allow concealment resentatives of a lineage of spiders in the long­ within specific microhabitats. Some species jawed orb-weaving genus Tetragnatha. Tetra­ have modifications of the cheliceral armature, gnatha is a large genus, with 295 described spe­ apparently to allow specialization on specific cies (Platnick 1993). Until recently it was prey types. One clade of 16 species ("spiny-leg" considered "primitive" (Bristowe 1958) within clade) has abandoned web building, with the the Araneoidea because of the simplicity of the concomitant development of long macrosetae female genitalia (absence of an epigynum). along the legs and adoption ofa vagile, cursorial However, based on characters such as the eyes predatory strategy (Gillespie 1991a). (showing the derived absence of a tapetum) and Phylogenetic analysis ofthe group to date has other features, it is now recognized that the epig­ revealed that there are three clades of Hawaiian ynum has been lost secondarily (see Hormiga Tetragnatha and at least two independent origins et al. [1995] for a list of Tetragnathinae synapo­ (Figure 1 [Gillespie et al. 1994]): (1) The T. morphies and placement within the family). Use hawaiensis clade appears to have split earliest of the chelicerae in mating seems to have pre­ from the others. It is a nonspeciose lineage simi­ cluded the need for an epigynal coupling (Levi lar in gross morphology to its continental conge­ 1981). The genus Tetragnatha is tremendously ners. (2) The spiny-leg clade contains all abundant and of worldwide distribution (Levi individuals with long macrosetae on their legs. 1981). Traditionally, it has been recognized as (3) The remaining taxa comprise a complex of one of the most homogeneous genera of spiders, web-building species. The spiny-leg clade and in both morphology (elongate form [Kaston the complex of web-building species may have 1948]) and ecology (associated with riparian arisen from one or two separate colonization habitats [Gillespie 1987]). events. The T. hawaiensis clade seems to have Based on the collection of R. C. L. Perkins, arisen from another colonization event. An addi­ E. Simon (1900) recognized the speciose nature tional natural colonization seems to have given of the genus Tetragnatha in Hawai'i. However, rise to Doryonychus raptor, the sole representa­ Perkins' spider collection, by his own admission, tive of a genus very similar to Tetragnatha was incomplete and unrepresentative (Perkins (Okuma 1990, Gillespie 1991b, 1992b). To date, 1913): spiders were collected only in passing phylogenetic analysis of the spiny-leg clade during his daylight searching for birds and based on morphological characters has indicated insects or while he collected insects attracted to a that the most closely related species are on dif­ light at night. The majority ofendemic Hawaiian ferent islands (Gillespie 1993, Gillespie and spiders are strictly nocturnal and extremely diffi­ Croom 1995). "Green" species share a suite of cult to find during the day (pers. obs.), and they apparent synapomorphies that group them cannot be attracted by lights. Accordingly, the together (Figure 2). 382 PACIFIC SCIENCE, Volume 51, October 1997 Soinv- .r----­ T. PERREIRAI OA leg cladel '----- T. WAIKAMOI MA * Web-buildin~ T.ACUTA HI _-----tspecles complex T. STELAROBUSTA HI T. pallescens N. America T. HAWAIENSIS HI 1_*-T. versicolor N. America • T. nitens Circumtropical I T. mandibulata Circumtropical * D.RAPTOR KA FIGURE 1. Phylogeny of endemic Hawaiian Tetragnathidae relative to representative continental species, showing at least three (two Tetragnatha, one Doryonychus) introductions into Hawai'i (Gillespie et al. 1994). Maximum likelihood tree based on 12S mtDNA sequences, log likelihood -982.1. Hawaiian taxa shown in bold-faced capital letters. * indicates colonization events.
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