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Herbivorous Insects and the Hawaiian Silversword Alliance: Coevolution Or Cospeciation?L

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Herbivorous Insects and the Hawaiian Silversword Alliance: Coevolution Or Cospeciation?L Pacific Science (1997), vol. 51, no. 4: 440-449 © 1997 by University of Hawai'i Press. All rights reserved Herbivorous Insects and the Hawaiian Silversword Alliance: Coevolution or Cospeciation?l GEORGE K. RODERICK2 ABSTRACT: Numerous groups of herbivorous insects in the Hawaiian archipelago have undergone adaptive radiations. R. C. L. Perkins collected and documented species in nearly all of these groups. In this study I tested whether patterns of host plant use by herbivorous insects can be explained by host plant history. I examined a group ofinsects in the planthopper genus Nesosydne (Hemiptera: Delphacidae) that feed on plants in the Hawaiian silversword alliance, many of which are endangered or threatened. For these Nesosydne species feeding on the silversword alliance, mitochondrial DNA sequence data revealed a statistically significant pattern of cospeciation between these insects and their hosts. These planthoppers are highly host-specific, with each species feeding on only one, or a few closely related, plant species. Patterns ofhost plant use across the plant lineage, as well as within extensive hybrid zones between members of the silversword alliance, suggest that planthopper diversification parallels host plant diversification. Data collected thus far are consis­ tent with, but do not directly demonstrate, reciprocal adaptation. For other herbivo­ rous insects associated with members of the Hawaiian silversword alliance, patterns of host plant use and evolutionary history are not yet well understood. However, cospeciation appears not to be universal. For example, endemic flies in the family Tephritidae (Diptera) are less host-specific and demonstrate host-switching. Research is under way to reveal the mechanisms associated with cospeciation and host­ switching for different insect groups associated with the Hawaiian silversword alliance. INSECT LINEAGES AT the generic and family lev­ Cospeciation is the matching of speciation els appear to be largely conservative with respect events in two lineages, such that the two phylog­ to their host affiliations, and many species in enies resemble one another (see Brooks 1979, such lineages are highly host-specific (Dethier 1988, Mitter and Brooks 1983, Hafner et al. 1954, Ehrlich and Raven 1964, Farrell and Mit­ 1994, Page 1995a). Cospeciation of plants and ter 1993, but see Dobler et al. 1996). Current their herbivorous insects may increase herbivore patterns of host plant use by herbivorous insects diversity as insects track and diversify with their can be explained by one of two hypotheses, both hosts. Coevolution can lead to cospeciation but of which can lead to greater herbivore diversity: is not required. For example, major vicariant cospeciation with host plants and host-plant events to which both lineages respond, followed switching. by allopatric speciation, could also produce a pattern of cospeciation. Or one group may I This research was supported by the University respond to vicariance, with the other lineage Research Council of the University of Hawai'i and the U.S. "following" again without the need for strict Fish and Wildlife Service. Additional support for our labora­ tory is provided by grants from NSF, USDA, California coevolution. Department of Food and Agriculture, International Rice By contrast, host-plant switching is a change Research Institute, Rockefeller Foundation, and the Pacific ofhosts (see Futuyma 1983a,b, Thompson 1994) Biomedical Research Center, University of Hawai'i. Manu­ other than would be predicted by the host phy­ script accepted 3 February 1997. logeny, such that the two phylogenies are no 2 Center for Conservation Research and Training, 3050 Maile Way, Gilmore 409, University of Hawai'i at Manoa, longer congruent. Host-switching can result in Honolulu, Hawai'i 96822. greater herbivore diversity if, following a switch 440 Herbivorous Insects on Hawaiian Silverswords-RoDERlCK 441 to a new host, the herbivore becomes sufficiently concurrently. However, for many insect/plant isolated and divergent from the species on the relationships studied, especially in North original host. However, factors responsible for America, the radiations of plants and insects generating the diversity of herbivorous insects have not been coincident, usually with the plant relative to their hosts are less clear. Compilations group becoming established following retreat of ofresearch on herbivorous insects and their hosts the glaciers and the insects spreading northward indicate that although a few insect radiations do at some later time (Farrell and Mitter 1993, Funk appear to be tightly correlated with radiations et al. 1995). For such interactions in mainland of their hosts, most insect radiations show evi­ tropical regions, which are older than temperate dence of host-switching (Mitter et al. 1988, ones, historical patterns of host association are 1991, Farrell and Mitter 1993, Funk et al. 1995). likely also to be obscured by extinctions and Recently, it has been suggested that hybrids incomplete knowledge (B. Farrell, pers. comm.). between host species may be associated with Such circumstances may bias evidence away herbivorous insect diversity and, by extension, from cospeciation, likely discounting its impor­ parasite diversity (Floate and Whitham 1993, tance in the early stages of diversification of a Strauss 1994, Whitham et al. 1994, Christensen plant lineage. To know about the relative ages et al. 1995). Much ecological and genetic data of the cospeciation events requires some knowl­ have demonstrated that hybrid zones can repre­ edge of the historical frameworks of both the sent very different environments for herbivorous insect and plant radiations. insects (see Boecklen and Spellenberg 1990, Many radiations of herbivorous insects are Aguilar and Boecklen 1992, Floate et al. 1993, endemic to Hawai'i (see Simon 1987, Howarth Floate and Whitham 1994, Fritz et al. 1994, and Mull 1992, Nishida 1994, Asquith 1995, Roderick and Metz 1997). Hybrid hosts not only Eldredge and Miller 1995, Miller and Eldredge create new adaptive zones, but also may allow 1996, Roderick and Gillespie in press) and repre­ specialized parasites an escape from the evolu­ sent a unique opportunity to unravel the popula­ tionary dead end-hybrids may enable parasites tion genetic and phylogenetic processes that to increase their host range, possibly leading have led to current patterns of host plant affilia­ to genetic diversification and speciation. This tion and are responsible for the diversity of asso­ scenario has been termed the "hybrid bridge" ciated insects. The extreme isolation and hypothesis (Floate and Whitham 1993). Hybrid historical framework provided by the Hawaiian hosts thus can provide a means for host­ archipelago makes possible the set of features switching. necessary for the test of hypotheses to account Distinguishing between the relative impor­ for patterns of herbivore host affiliations and tance ofcospeciation and host-switching is diffi­ associated diversity. In particular, island and vol­ cult for several reasons. By necessity, much of cano age can be used to identify the age of our information concerning patterns ofcospecia­ particular insect/plant associations, indepen­ tion or coevolution must come from inferring dently from any information gained through past events from current observations. Recent molecular data. In this study, I examined the developments in both molecular biology and the­ evidence for cospeciation and host-switching for ory have made it possible to compare recon­ species of planthoppers in the genus Nesosydne structed phylogenies of pairs of interacting (Hemiptera: Delphacidae) that feed on the lineages and to test for significance of cospecia­ Hawaiian silversword alliance. Recently, Bald­ tion (Mitter and Brooks 1983, Brooks 1988, Mit­ win and Robichaux (1995) generated a phyloge­ ter et al. 1991, Maddison and Maddison 1992, netic hypothesis for the history of the species Moran and Baumann 1994, Funk et al. 1995, within the silversword alliance that makes this Page 1995a, b). However, reconstructing past work possible. associations between species can be more prob­ The current threats to biological diversity lematic (Mitter et al. 1988, 1991, Wiegmann et have necessitated the understanding ofthe forces al. 1993). For example, if cospeciation were to responsible for both its generation and demise occur, it demands that both insect and plant (or (Wilson 1988, 1996). Nowhere on earth is the parasite and host) have the potential to radiate extinction crises more acute than in the Hawaiian 442 PACIFIC SCIENCE, Volume 51, October 1997 archipelago (Gillespie et al. 1997, Liebherr and of planthoppers and their host plants; (2) it gives Polhemus 1997, Gillespie 1997). As such, insight into the degree of host specificity; and Hawai'i becomes a model system for the study (3) it establishes the relatedness between paren­ of both the generation of biodiversity and its tal plant species associated with each plant conservation. hybrid zone. Nesosydne PLANTHOPPERS. The genus Neso­ sydne in Hawai'i contains at least 80 species (Zimmerman 1948). In contrast to other delpha­ MATERIALS AND METHODS cid planthoppers that are mainly grass feeders Study Organisms (Denno and Roderick 1990), species within Nes­ osydne in Hawai'i feed on plants in an aston­ SILVERSWORD ALLIANCE. The silversword ishing 28 plant families (Figure 1) (Zimmerman alliance in Hawai'i comprises 28 species, pre­ 1948, Wilson et al. 1994). This diversity ofhost sumably with
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