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Cophylogeny provides a framework for the study of historical ecology and community evolution. Plant-insect cophylogeny has been investigated across a range of ecological conditions including herbivory (Farrell and Mitter 1990; Percy et al. 2004), mutualism (Chenuil and McKey 1996; Kawakita et al. 2004), and seed parasitism (Weiblen and Bush 2002; Jackson 2004). Few examples of cophylogeny across three trophic levels are known (Currie et al. 2003), and none have been studies of plants, herbivores, and their parasitoids. This chapter compares patterns of diversification in figs (Ficus subgenus Sycomorus) and three fig-associated insect lineages: pollinating fig wasps (Hymenoptera: Agaonidae: Agaoninae: Ceratosolen ), nonpollinating seed gallers (Agaonidae: Sycophaginae : Platyneura), and their parasitoids (Agaonidae: Sycoryctinae: Apocrypta). Molecular phylogenies of each participant in this tritrophic interaction can illuminate histories of ancient association ranging from codivergence to host switching. We distinguish cospeciation, the simultaneous speciation of a host and an associate (Page 2003), from coevolution , strictly defined as reciprocal evolutionary change between lineages acting as agents of selection upon each other (Stearns and Hoekstra 2000). Tests of cospeciation and alternative hypotheses, including host switching, can evaluate whether evolutionary change in host use was associated with speciation (Coyne and Orr 2004). Nonpollinating fig wasps have not received as much attention as the pollinating wasps, and so little is known about their evolutionary history (Ulenberg 1985; Bronstein 1991; Lopez-Vaamonde et al. 2001; Cook and Rasplus 2003). Weiblen and Bush (2002) argued from phylogeny that nonpollinating seed gallers are less closely cospeciated with figs than pollinators sharing the same hosts. It is not known if the same is true for fig wasp parasitoids. Robust phylogeny estimates inform our inference of past evolutionary processes from patterns of diversity seen in the present. Topological congruence between the phylogenies of host organisms and their associated lineages is the first line of evidence for cospeciation. On the other hand, phylogenetic incongruence may indicate other historical patterns of association , including host switching. When host and associate topologies and divergence times are more closely congruent than expected by chance (Page 1996), ancient cospeciation may have occurred. Incongruence between phylogenies requires more detailed explanation, including the possibility that error is associated with either phylogeny estimate. Ecological explanations for phylogenetic incongruence include extinction, “missing the boat,” host switching, and host-independent speciation (Page 2003). “Missing the boat” refers to the case where an associate tracks only one of the lineages following a host-speciation event. For most plant-insect interactions , these other events are more common than cospeciation (Farrell and Mitter 1990). A few highly specialized interactions, including obligate pollination mutualisms (Weiblen and Bush 2002; Kawakita et al. 2004), show evidence of cospeciation. We examined patterns of historical association across three trophic levels in the fig microcosm, comparing mitochondrial DNA phylogenies for pollinators, gallers, and parasitoids to multigene phylogenies of the host figs. Given that nonpollinators play no direct role in fig reproductive isolation, we tested the prediction that gallers and parasitoids show less evidence of cospeciation with their hosts than do pollinators influencing patterns of host gene flow. Some background on fig pollination is needed to understand this prediction in more detail. Background Fig Pollination More than 800 fig species (Ficus, Moraceae) occur in the tropics and subtropics worldwide (Berg 1989). Fig species exhibit a wide array of growth forms including shrubs, trees, 225 S EVE NTE E N Cophylogeny of Figs, Pollinators, Gallers, and Parasitoids SUMMER I. SILVIEUS, WENDY L. CLEMENT, AND GEORGE D. WEIBLEN climbers, and hemi-epiphytic stranglers. The genus is characterized by an obligate mutualism with pollinating fig wasps (Chalcidoidea: Agaonidae: Agaoninae) and a specialized inflorescence called a syconium, which comprises an enclosed cavity filled with numerous, highly reduced unisexual flowers (Bronstein 1992). At the apex of the syconium is a bract-lined opening, or ostiole, that is the point of entry for pollinating fig wasps. Pollinators depend on figs for the rearing of their offspring, and figs depend on wasps for pollination. Pollinators are very small, approximately a millimeter in body length, and often bear specialized thoracic pockets for the transport of pollen grains (Weiblen 2002). Most fig species are pollinated by unique fig wasp species (Wiebes 1979), but not all cases involve one-to-one species specificity. Molbo et al. (2003) found cryptic pollinator species on the same host in sympatry, whereas Rasplus (1994) reported instances of peripatric pollinator species on widespread hosts with intervening zones of contact (Michaloud et al. 1996). Chemical volatiles are the primary cues that attract unique pollinators...


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