New synthesis--back to the future: new approaches and directions in chemical studies of coevolution.

Published online: 9 June 2011# Springer Science+Business Media, LLC 2011The concept of an arms race between herbivores and plants, associatedwith increases in diversity of plant secondary compounds, has longprovided an appealing theoretical framework for evolutionary biologistspondering adaptive radiations, and has been a stimulus for studies ofchemical ecology. While publications on coevolution are steadilyincreasing in ecology and evolutionary biology, such studies havestagnated in chemical ecology, even though modern chemical techniqueshavemadeiteasiertoexaminecoevolutionarypredictionsforphytochem-icaldiversification.Anexampleofwhatcanbeaccomplishedisillustratedby Kursar et al. (2009), who documented considerable divergence ineffective antiherbivore defenses of the tropical plant genus Inga,indicating that an arms race between plants and herbivores caused rapid,divergent trait evolution. Interestingly, closely related Inga species thatoccur together in tropical forests al so have distinct defensive profilesdriven by tritrophic interactions. Thus, diffuse multitrophic coevolution-ary interactions, mediated in part by plant chemistry, help structurediverse communities, allowing for high alpha diversity for Inga.ThestudyofInga and related studies on Quercus, Piper,andBurserautilize modern approaches to natural history, ecology, phylogenetics, andchemistry, and indicate that the time is ripe for chemical ecologists toreturn to coevolution as a unifying research theme. For natural productschemistry, synthesis and complex mixture analysis have improveddramatically (Hoye and Sizova 2009) with advances in MS sources,including electrospray ionization, matrix-assisted laser desorptionionization, and atmospheric pressure chemical ionization. Theseapproaches permit rapid elucidation of a broad array of compounds ina taxon of interest, which is necessary for testing causes andconsequences of increases of chemical diversity. Such input fromchemists can synergize with advances in molecular ecology. Forexample, new sequencing technologies present the opportunity togenerate high resolution population genomic data that can be used totest the hypothesis that host plant affiliations are associated with distinctchemical profiles and population genetic differentiation.How will these new technologies contribute to understandingchemical mediation of coevolution? The answer includes a long list oftheoretical advances, but here I provide two examples of excitingresearch directions.First, a major problem with any approach to studying insect-plantcoevolution is that there is a bias t owards examining individual plantcompounds and their effects on the physiology of herbivores and theirpredators. Redundancy in plant defenses has long been appreciated, andcommon effects such as synergy obfuscate results from traditionalmechanistictestsofcoevolutionaryhypotheses.Forexample,innumerouscoevolutionary studies, the failure to demonstrate negative correlations inperformance on hosts with different defensive compounds or todemonstrate defensive efficacies of secondary metabolites could easilybe due to the fact that compounds do not function in isolation. It is quitepossible that phytochemical synergy is the rule rather than the exception,even for putatively induced defenses, and we need new initiatives ofchemicalecologicalresearchthataimtotestfordefensiveefficacyofsuitesof compounds or cross-host tradeoffs for different synergistic mixtures.Second, any new approach to studying coevolution must acknowl-edgethatplantsandparasitesinteractwithincomplexfoodwebs.Thus,itmakes sense to examine the phylogenetic histories and ecologicalinteractions of both the hosts and the parasites of focal herbivores.Forister and Feldman (2011) take this approach when they present theconcept of a “phylogenetic cascade,” in which diversification at onetrophic level affects two or more other levels, resulting in a sharedevolutionary history across a food chain. Classic coevolutionaryhypotheses are a subset of the phylogenetic cascades framework, andchemistry can play a major role in these interactions, as evidenced fromnumerous ecological studies that demonstrate strong indirect trophiceffects of variation in plant chemistry. If future research on chemicalmediationofcoevolutionisconsideredwithinsynergisticorphylogeneticcascades contexts, by utilizing the latest technological advances, ourunderstanding of diversity of animals, plants, and secondary metabolitesshould improve dramatically.