Macroevolution and the biological diversity of plants and herbivores Douglas J. Futuymaa,1 and Anurag A. Agrawalb aDepartment of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11794-5245; and bDepartments of Ecology and Evolutionary Biology and Entomology, and Cornell Center for a Sustainable Future, Cornell University, Ithaca, NY 14853-2701 Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved July 29, 2009 (received for review May 11, 2009) Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of en- ergy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postu- lated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has re- vealed evidence for escalation in the potency or variety of plant lineages’ chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the co- evolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been tem- porally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. How- ever, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversifica- tion are inexorably intertwined. coevolution ͉ herbivory ͉ insect host range ͉ phylogenetic analyses ͉ plant defense theory ne hundred and fifty years lich and Raven (4) integrated these ideas whether or not the function (not just ago, Darwin’s concept of evo- into a historical scenario that inspired re- effect) of secondary compounds is de- lution replaced theological searchers for decades thereafter. fense, and attention shifted from expla- concepts of plenitude as an Ehrlich and Raven (4) suggested that nation of the variety of taxonomically Oexplanation for the almost boundless in response to herbivory a plant species restricted compounds to the costs and diversity of organisms. Since then, evo- may evolve a novel, highly effective benefits of varying degrees of invest- lutionary biologists and ecologists have chemical defense that enables escape ment in defense. For example, Feeny (6) sought to understand how such diversity from most or all of its associated herbi- suggested that investment should be has come to be, how it has changed over vores. By an unspecified mechanism, greater in ‘‘apparent’’ (large, long-lived, time, and why species diversity varies this advantage enables the plant lineage common species) plants than less appar- among taxa and environments. For the to radiate into diverse species, which ent (rarer, smaller, or more ephemeral) last several decades, plants and their share the novel defense (hence, related species; Janzen (7) and Coley et al. (8) herbivores, especially insects, have been plants tend to share similar chemistry). proposed that allocation to defense major subjects of such inquiries, for to- After some time, one or more insect would be especially high in plants that gether they account for more than half species colonize this plant clade and have inherently slow growth because of of the described species and play over- adapt to it, shifting from perhaps chemi- limited resources, a hypothesis for which whelmingly important ecological roles. cally similar, although distantly related, strong support has been adduced (e.g., Central to this topic has been the im- host plants. These insects, able to use ref. 9). This ecological (or microevolu- mense diversity of so-called secondary the ‘‘empty niches’’ afforded by a di- tionary) approach, based on assump- compounds or secondary metabolites verse clade of chemically distinctive tions of optimal adaptation, was comple- that distinguish species and higher taxa plants, themselves undergo adaptive ra- mented by studies of selection in of plants and the relatively narrow host diation, as new species arise and adapt populations, especially using methods of range of most phytophagous insects, to different, but related, plants. Hence quantitative genetics. This body of work most species of which feed on a small related insects will tend to use related has strongly established that secondary fraction of the plants in any area. Sec- plant hosts, a pattern long known to en- compounds are heritable, herbivores do ondary compounds are those not in- tomologists and that Ehrlich and Raven indeed exert selection for defense, and volved in the ‘‘primary’’ functions of described in detail as it is manifested by negative genetic correlations often exist plants, that is, resource acquisition and butterflies. Ehrlich and Raven proposed that imply tradeoffs in investment (10, allocation, and are often implicated in that repetition of such stepwise adaptive 11). An important outcome of these ap- defense. The suspicion that plant sec- radiations through time, in both plant– proaches was recognition that plants ondary chemistry had shaped specialized herbivore and other kinds of ecological may adapt to herbivory not only by ‘‘re- host associations (1) was elaborated and associations, accounts for a great deal of sistance’’ to herbivores (preventing or verified by Dethier (2) and others, and biological diversity (Fig. 1). minimizing attack), but also by ‘‘toler- Fraenkel (3) summarized the evidence However inspiring their article may that most secondary compounds had have been, most research in the next evolved to defend plants against insects three decades or so did not address the Author contributions: D.J.F. and A.A.A. wrote the paper. and other natural enemies. In one of the historical, macroevolutionary compo- The authors declare no conflict of interest. most frequently cited publications on nents that were Ehrlich and Raven’s This article is a PNAS Direct Submission. plant–herbivore interactions, ‘‘Butterflies focus (5). Considerable literature ad- 1To whom correspondence should be addressed. E-mail: and plants: A study in coevolution,’’ Ehr- dressed the still-debated question of [email protected]. 18054–18061 ͉ PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904106106 Downloaded by guest on September 23, 2021 SPECIAL FEATURE: PERSPECTIVE of plant features seem to form ‘‘defense syndromes’’ (29, 30) that may indicate adaptation to particular suites of herbi- vores and may potentially be dictated by the abiotic environment. Many classes of compounds seem to have evolved re- peatedly from widely shared biosynthetic pathways, suggesting that fairly minor changes in gene regulation may be en- tailed (31, 32), and some authors have suggested that many plant compounds may be derived either directly or by lat- eral gene transfer from symbiotic fungi (32). These suggestions imply that ram- pant parallelism or convergence is possi- ble, potentially providing plentiful op- portunity for phylogenetic comparisons. Fig. 1. A conceptualization of escape and radiate coevolution hypothesized by Ehrlich and Raven (4). In They also bear on the important ques- this hypothetical scenario, a plant phylogeny is on the left and insect herbivore phylogeny is on the right; tion of whether plants’ defense profiles arrows between the phylogenies indicate host use (species missing arrows feed on plants that are not are optimized (as they might be if most shown here). For the plant lineage, black indicates the ancestral defensive phenotype, yellow indicates the lineages retain the same biosynthetic evolution of some new defense, and yellow with red hatches indicates the evolution of an additional novel defense. The evolution of counteradaptations is similarly indicated on the insect phylogeny. Note that the capacities, so that specific families of evolution of novel traits related to the interaction is associated with an increased diversification rate (i.e., compounds can readily evolve) or are species accumulation per unit time). Insect counteradaptations have allowed for the colonization of historically contingent on the occurrence differentially defended plant clades, but in this case the counteradaptations have not escalated by adding of rare mutations. Does the chemical on new phenotypes; rather, two counteradaptations have independently evolved. Insect host use shows variation among plant lineages owe some phylogenetic signal (i.e., closely related species feed on related plants), but some insects also more to the origin of phenotypic varia- colonize distantly related plants. The insect lineage did not cospeciate with the plant lineage. In other tion or different histories of selection? words, the phylogenies are not parallel (i.e., mirror images of each other), but rather the pattern indicates Plant adaptations to herbivory can be that insects radiated onto existing plants (fossil