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Host Conservatism, Host Shifts and Diversification Across Three Trophic doi: 10.1111/j.1420-9101.2011.02446.x Host conservatism, host shifts and diversification across three trophic levels in two Neotropical forests J. S. WILSON*, M. L. FORISTER*, L. A. DYER*, J. M. O’CONNOR ,K.BURLS*, C. R. FELDMAN*, M. A. JARAMILLOà,J.S.MILLER§,G.RODRI´GUEZ-CASTAN˜ EDA–, E. J. TEPE** ,J.B.WHITFIELD &B.YOUNG* *Program in Ecology, Evolution and Conservation Biology, Department of Biology, University of Nevada, Reno, NV, USA Department of Entomology, University of Illinois, Urbana, IL, USA àResearch Center for Environmental Management and Development, CIMAD, Jamundı´, Valle, Colombia §American Museum of Natural History, Division of Invertebrate Zoology, New York, NY, USA –Department of Ecology and Environmental Science, University of Umea˚, Umea˚, Sweden **Department of Biology, University of Utah, Salt Lake City, UT, USA Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA Keywords: Abstract coevolution; Host–parasite systems have been models for understanding the connection Eois; between shifts in resource use and diversification. Despite theoretical Parapanteles; expectations, ambiguity remains regarding the frequency and importance of Piper; host switches as drivers of speciation in herbivorous insects and their speciation; parasitoids. We examine phylogenetic patterns with multiple genetic markers tri-trophic. across three trophic levels using a diverse lineage of geometrid moths (Eois), specialist braconid parasitoids (Parapanteles) and plants in the genus Piper. Host–parasite associations are mapped onto phylogenies, and levels of cospeciation are assessed. We find nonrandom patterns of host use within both the moth and wasp phylogenies. The moth–plant associations in particular are characterized by small radiations of moths associated with unique host plants in the same geographic area (i.e. closely related moths using the same host plant species). We suggest a model of diversification that emphasizes an interplay of factors including host shifts, vicariance and adaptation to intraspecific variation within hosts. separate fronts, one focusing on patterns at a deep Introduction temporal and taxonomic scale, and the other focusing on Interactions between trophic levels play a central role in mechanisms driving recent population and species diver- the evolution of biological diversity (Page, 2003; Singer & gence, often with contemporary taxa at an incipient stage Stireman, 2005; Thompson, 2005). In particular, host– of divergence. At the deeper taxonomic level, the parasite relationships have figured prominently in our emphasis has been on major hosts shifts, for example, understanding of diversification by providing a frame- among different families of hosts where lineages of work for investigating the importance of exploitative parasites adapt to novel resources that subsequently adaptations and host defences (e.g. Ehrlich & Raven, drive adaptive radiations (Ehrlich & Raven, 1964; Sch- 1964; Rundle & Nosil, 2005; Becerra, 2007; Matsubay- luter, 2000). Evidence for the importance of major host ashi et al., 2010). Within this area of evolutionary shifts driving diversification comes from a number of ecology, research has advanced along at least two groups, such as the colonization of angiosperms by weevils (McKenna et al., 2009), and shifts to new plant Correspondence: Matthew L. Forister, Program in Ecology, Evolution and families by butterflies (Fordyce, 2010). Along the other Conservation Biology, Department of Biology, University of Nevada, Reno, NV, 89557, USA. major conceptual front in hypotheses of host–parasite Tel.: +1 775 784 6770; fax: +1 775 784 1302; diversification is the emphasis on host-switching at the e-mail: [email protected] lowest taxonomic levels (Berlocher & Feder, 2002; Dre`s ª 2012 THE AUTHORS. J. EVOL. BIOL. JOURNAL OF EVOLUTIONARY BIOLOGY ª 2012 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 J. S. WILSON ET AL. & Mallet, 2002; Funk et al., 2006), in which reproductive breadths, with most species feeding on a single or a few isolation between sister species is associated with host- Piper species (Dyer & Palmer, 2004; Connahs et al., specific adaptations (e.g. Funk, 1998; Lu & Bernatchez, 2009); though, recent evidence suggests that at least 1999; Nosil, 2004; Forister, 2005; Stireman et al., 2005). some host shifts away from Piper have occurred (Strut- Considering the phylogenetic evidence for the impor- zenberger et al., 2010). Piper is a species-rich genus tance of major host shifts and the importance of diver- composed of predominantly understory shrubs that gent, host-associated selection at low taxonomic levels, reach their highest diversity in the Neotropics, where one might conclude that shifts in diet are the major over 1000 species are found (Jaramillo & Manos, 2001; drivers of diversification in herbivorous insects. This Greig, 2004; Quijano-Abril et al., 2006). Because of the could be true if insect diversification is contemporary high diversity and abundance of Piper in the Neotropics, with host diversification, or temporally lags behind plant as well as the variety of ecological interactions and speciation (Percy et al., 2004). Futuyma & Agrawal chemical defences present in this genus, it has been (2009) have cautioned that this conclusion remains considered a model for studies of phytochemistry, ecol- unjustified and that the importance of other facets of ogy and evolution (Dyer & Palmer, 2004). At the third the parasitic life style, including more complex commu- trophic level, Parapanteles is a potentially large, but still nity interactions, has been insufficiently examined. poorly known genus within the diverse microgastrine Winkler & Mitter (2008) surveyed a large number of braconid wasps, with 16 species described from the published phylogenies for herbivorous insects and sim- Neotropics (Valerio et al., 2009). It is likely that there are ilarly concluded that the importance of both major many undescribed Parapanteles species because the (between families) and minor (between species) host majority of Neotropical microgastrines remain unde- switches has been overestimated. Specifically, fewer than scribed (Smith et al., 2008a; Whitfield et al., 2009). Like half of 145 sister species pairs from 45 phylogenies all microgastrines, Parapanteles are endoparasitoids of included different host species. This suggests that other lepidopteran larvae and although host associations are factors, such as historical vicariance, may also play a role known for only a small proportion of the species, they in parasite diversification. In fact, more general mecha- are expected to be highly host specific because high host nisms of speciation, such as divergence in allopatry, specialization has been found in a number of microgas- might interact with ecological processes in diversification trine genera (Smith et al., 2008a). (Nosil et al., 2005). The possibility of an interaction To investigate the role resource use plays in diversi- between historical and geographical factors and diver- fication, we bring together phylogenetic and ecological gence associated with alternate resource use has often data for Piper, Eois and Parapanteles. For each host– been overlooked in discussions of host–parasite diversi- parasite relationship – Eois feeding on Piper, and fication. Parapanteles feeding on Eois – we ask: what is the Although phylogenetic studies of host–parasite rela- phylogenetic distribution of host use? If diversification tionships are not rare, few studies have targeted highly at one level provides the ecological opportunity for diverse parasite lineages, particularly at appropriate diversification at another, then we expect the phyloge- spatial and temporal scales in which recent divergence netic histories of ecological associates to covary in could potentially be linked to macroevolutionary trends. predictable ways (Page, 2003; Forister & Feldman, Even fewer studies have investigated evolutionary 2011). For free-living (as opposed to symbiotic) parasites, dynamics in a community context across more than such as insect herbivores and parasitic wasps, we do not two trophic levels (but see Lopez-Vaamonde et al., 2005; expect a history of cospeciation to necessarily be man- Noda et al., 2007; Silvieus et al., 2008; reviewed by ifest as perfectly congruent phylogenetic histories. Forister & Feldman, 2011). Tropical communities provide Instead, the prediction based on cospeciation is for a species-rich assemblages in which questions regarding level of constrained or conserved cladogenesis, in which resource use and diversification can be addressed. In this closely related parasites tend to attack more closely study, we examine patterns of diversification in a related hosts (Futuyma & Agrawal, 2009). Alternatively, species-rich tropical moth genus, Eois Hu¨ bner (Lepidop- an absence of association between host and parasite tera: Geometridae: Larentiinae), its major host plant phylogenies would raise the possibility that other genus, Piper L. (Piperales: Piperaceae), and a group of mechanisms (i.e. biogeographic factors) rather than Eois-attacking parasitoid wasps in the genus Parapanteles host-associated ecological divergence have influenced Ashmead (Hymenoptera: Braconidae: Microgastrinae). diversification. We address these issues both with tests Eois is comprised of roughly 250 described species designed specifically to detect patterns of shared history (Scoble, 1999; Herbulot, 2000) as well as numerous in host–parasite phylogenies, and with more general genetically distinct morphospecies
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