Macroevolution and the Biological Diversity of Plants and Herbivores

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 coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally 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 diversification 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 futuyma@life.bio.sunysb.edu.

18054–18061 ͉ PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904106106 Downloaded by guest on September 27, 2021 PCA ETR:PERSPECTIVE FEATURE: SPECIAL

of plant features seem to form ‘‘defense syndromes’’ (29, 30) that may indicate adaptation to particular suites of herbivores 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 entailed (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 possible, potentially providing plentiful opportunity 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 evidence or other means of dating could verify this pattern classified by several criteria, such as bio- of insect speciation on to a diversiﬁed group of plants). Parallel phylogenies are not predicted by coevolution, and could simply be a consequence of joint vicariance events that result in both insect and synthetic pathway, investment level, and plant speciation. effect on the target organisms. For example, tolerance rather than resistance may be advantageous if resources are ance’’ of tissue damage, based on an mate timing and the pattern of evolu- relatively abundant (9, 33). Chemical ability to regrow or reproduce, by using tion of characters of interest. resistance characters may act as toxins, stored resources (12, 13). Research on One consequence of this sea change inhibitors of digestion, or deterrents. phytophagous insects included explora- in evolutionary biology is a growing ap- Whether or not these classes of defense tions of sensory and other physiological preciation of the impact of deep evolu- differ in phylogenetic conservatism or aspects of choice of and adaptation to tionary history on the features of living the ecological context in which they are host plants (e.g., refs. 14 and 15), stud- organisms, including features that affect most often deployed is not known. One ies of host-plant-associated speciation their ecological distribution and associa- can easily imagine that alteration of (16–18), and especially quantitative ge- tions (23–25). As a prelude to the other many plant features could knock out netic approaches to the question of papers in this Special Feature, we necessary sign stimuli for oviposition or whether or not tradeoffs exist in adapta- briefly outline some of the major issues feeding by certain specialized insects, so tion to different host plants. The latter in the macroevolution of plant–herbivore that compounds that act as deterrents could be more variable among plant approach is the dominant hypothesis to interactions (see also ref. 26). Of taxa than toxins (34). Evidence that spe- explain the prevalence of specialized course, satisfying answers to most of cialist insects are deterred by a great host associations (19, 20). these questions will require integrating variety of compounds is consonant with Research on the historical, macroevo- macroevolutionary pattern with evi- this view (14). lutionary heart of Ehrlich and Raven’s dence from functional, genetic, and Phylogenetic analysis of ancestral and hypothesis (4) was slow in developing, ecological approaches. derived states of defense profiles, in- probably because the relevant fossil Evolution of Defenses cluding specific chemical families, has record is rather sparse (but see ref. 21) only begun, yet it can address some of and phylogenetic methods were in their Herbivory clearly imposes natural selec- the most important questions about de- infancy (and were embroiled in contro- tion on plants (e.g., refs. 11 and 27), fense evolution. Several of the articles in versy) in the 1960s. Important steps to- even enforcing habitat specialization (9), this Special Feature address the impact ward using phylogenies to infer the his- so the defensive function of many plant of ecological associations on the macro- tory of associations were first taken by secondary chemicals is no longer evolution of defense strategies, ranging Mitter and Brooks (22) at a time when doubted. That does not mean, however, from biotic defense via ants to invest- phylogenies were few and based on little that all secondary compounds have de- ment in sundry chemical classes (35, 36). (nonmolecular) data. Today, phyloge- fensive function, and criteria for deter- Plant life history, genetic attributes, and netic analysis, based on ever more so- mining this are still not fully developed. mating system also may play a role in phisticated analytical methods and abun- Phylogenies enable use of the compara- the macroevolution of defense strate- dant molecular data, enables us to infer tive method, in which patterns of con- gies; Johnson et al.’s (37) study of the with considerable confidence not only vergent evolution may provide evidence Onagraceae clearly demonstrates that the order of branching, but also approxi- of adaptation (28). In some cases, suites repeated evolution of asexual reproduc-

Futuyma and Agrawal PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 ͉ 18055 Downloaded by guest on September 27, 2021 tion influenced the evolution of defense defense. We predict that tradeoffs over (60) have shown that the phylogeneti- against herbivores. Phylogenetic recon- macroevolutionary scales will entail cally derived condition of producing fo- struction of ancestral states further al- tradeoffs in ‘‘strategies’’ (e.g., chemical liar defense resins in the genus Da- lows the dissection of some classic toxins vs. tolerance) more often than lechampia is deterrent to several predictions from defense theory. For in single compound types (29, 30, generalist and specialist herbivores. example, does continuing herbivore 35, 36). Ultimately, we suggest phylogenetic– pressure, especially if imposed by An important question is whether ecological studies that examine the im- steadily adapting herbivores, result in most chemical defenses are effective pact of herbivores on sister groups that ‘‘escalation’’ (38) in the potency or va- against a wide or narrow range of actual differ in defensive traits. Such studies riety of a plant lineage’s chemical de- and potential herbivores. High specific- would not only contribute to under- fense system? Or does adaptation to ity might imply that a diverse commu- standing the impact of novel traits on herbivory reside mostly in evolving nity of insects selects for multiple de- herbivory, but also on the association of novel defenses? There are clear cases fenses, as seen in many plants, and different herbivore communities with of evolutionary novelty, such as the could account for divergence in defense different defense strategies (see discus- origin of the sulfur-based glucosinolate– profiles among plant species. Thus co- sion on diffuse coevolution above). myrosinase defense system in the Bras- evolution (in the sense of reciprocal Ehrlich and Raven (4) also proposed sicaceae. This potent defense is diag- adaptive responses) would entail ‘‘pair- that the advantage provided by new de- nostic for the family; yet restricted wise’’ evolution of specific plant traits fenses could promote adaptive radiation genera in the Brassicaceae have addi- and specific enemies. In this scenario, of a plant lineage. Just why an individu- tionally evolved novel compound individual species of herbivores are each ally advantageous character might ele- classes [e.g., tropane alkaloids (39), abundant and damaging enough to im- vate speciation rates is not obvious (see cucurbitacins (40), and cardenolides pose significant selection and do not ref. 61), but diversification rates could (41)] that typically occur in other plant strongly interact over evolutionary time. be enhanced by larger population sizes, families. The evolution of furanocou- Alternatively, coevolution would be ‘‘dif- which encourage the colonization of marins in Apiaceae is thought to have fuse’’ if defense against various enemies marginal habitats, or by reducing the entailed progression toward more toxic were positively genetically correlated frequency of extinction. Ehrlich and forms (42), but a firm phylogenetic (51, 52); then selection for defense Raven’s hypothesis is best tested by framework has not yet been estab- could stem from the collective impact of comparing the diversity in multiple lin- lished. Among milkweeds (Asclepias many herbivores, some of which might eages, in which a proposed diversity- spp.), phenolic compounds and toler- be uncommon (34), and the evolution of enhancing character has evolved conver- ance to herbivory appear to have in- new defenses would be impelled not by gently, with their sister lineages. Using creased, but the toxic cardenolides for the identity of herbivores as much as by this approach, Farrell et al. (62) re- which these plants are renowned have their collective impact. Probably the ported that diversity is significantly declined during the diversification of question of the incidence of pairwise elevated in lineages that have evolved the genus (43, 44). In this Special versus diffuse defense evolution will latex- or resin-bearing canals. This ap- Feature, Becerra et al. (45) report a vary with factors such as plant organ pears to be the only such analysis to pattern of escalation in the Bursera sys- (e.g., fruit vs. leaf), defense type, and date. Other highly convergent and more tem, in which the diversity of terpenoid herbivore diet breadth. Even crude mea- or less discrete traits such as the produc- defenses has increased. sures of the toxicity or deterrent effects tion of glandular trichomes or alkaloids A phylogenetic pattern of escalation of specific compounds across a wide ar- are ripe for such analyses. or the progressive addition of novel ray of insects appear to be rather rare, In a quantitative sense, a directional defense strategies implicates coevolu- and those few suggest that effects are relationship between a continuous char- tion consistent with an arms race. Al- not highly correlated across herbivores acter and phylogenetic node depth sug- ternatively, a pattern of old defenses (53–55). Genetic correlations of resis- gests that the trait impacts diversifica- being replaced by new ones suggests tance of whole plants against various tion (63) (although cause and effect are that energetic cost or other tradeoffs herbivores are also rather low (56–58), not separable); such relationships have constrain the macroevolution of de- but these correlations, across genotypes been detected in the milkweeds (43, 44). fense (46). However, this explanation that vary in many characters, may say A final approach to addressing the role has been questioned because physiolog- little about the cross-effectiveness of any of plant defensive traits in adaptive radi- ical tradeoffs between different kinds one defense character. ation is to test Simpson’s classic ‘‘early of defenses seem not to be general (29, Finally, what are the macroecological burst’’ prediction, that trait diversity 47). Ecological costs, such as deterring and macroevolutionary consequences of within a lineage should evolve early in pollinators, have also been described defense evolution? Do evolutionarily the diversification process and plateau (48, 49). A more intriguing possibility new defense profiles result in escape toward the end of the radiation (64–66). is that like chemical insecticides, de- from some herbivores and reduced her- In this Special Feature, Agrawal et al. fenses become obsolete because herbi- bivory, as Ehrlich and Raven (4) postu- (67) provide some of the first phyloge- vores adapt to them. Cornell and lated? This seems likely, in view of the netic evidence for the early burst model, Hawkins (50) draw this conclusion different taxonomic composition of the implicating a contribution of plant de- from their metaanalysis of experimen- insects associated with different plant fenses to the adaptive radiation of the tal studies, in which taxonomically taxa, but we are aware of few rigorous milkweeds (Asclepias spp). broadly distributed compounds, which investigations of this question. Perhaps Cornell and Hawkins assume to be ple- the best circumstantial evidence comes Evolution of Herbivores siomorphic, display somewhat lower from the Brassicaceae (discussed above), Most herbivorous mammals have fairly toxicity than taxonomically restricted where the ancestral defenses (glucosino- broad diets, but among insects highly (presumably more recently evolved) lates) have been overcome by many spe- polyphagous species are relatively few, compounds. This proposition warrants cialist insects, yet several newer novel and most species are restricted to plants more detailed examination. Ultimately, defenses (39–41) strongly limit many of in a single family or even to a few tradeoffs must constrain investment in the specialists (59). Armbruster et al. closely related species (15, 68). The av-

18056 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904106106 Futuyma and Agrawal Downloaded by guest on September 27, 2021 erage herbivorous insect species col- some, but not all, of the plant hosts of tion in many of these cases, and approx- lected from trees in a highly diverse congeneric beetles, primarily to hosts of imately half of speciation events do not New Guinea forest feeds on three or closely related species. The genetic basis entail shift between plant species. For fewer plant species and has Ͼ90% of of host preferences and the interaction example, in the diversification of 14 As- individuals concentrated on a single spe- between such genetic variation and eco- phondylia gall midges on creosote bush cies (69). Moreover, many clades of phy- logical processes possibly leading to spe- (Larrea tridentata), shifts to different tophagous insects are models of phylo- ciation have recently been studied in plant tissues represent adaptive diversifi- genetic conservatism, having largely several other groups (77–80). More cation within a single host plant (87). retained association with the same studies of the relationship between the Other attributes, such as an internal ver- plant taxa for many millions of years, genetic processes and the historical pat- sus external feeding habit, may contrib- with few evolutionary excursions to tern of host shifts are needed, especially ute to insect diversification; Nyman et other taxa. In a broad-scale phyloge- in a comparative framework. al. (88) reported that in the sawfly sub- netic survey, Janz and Nylin (70) re- The prevalence of phylogenetic con- family Nematinae feeding habit was port that related butterfly larvae tend servatism in diet might suggest that spe- more conserved than host use and exter- to feed on related host plants and host cialized host associations are irreversible nal feeders host-shifted more than inter- shifts were more common between or nearly so. However, although change nal feeders, but that feeding habit was closely related plants than between dis- from one specialized host association to not consistently associated with the rate tantly related plants. In a more recent another is the prevalent pattern, the few of diversification. Winkler and Mitter compilation of phylogenies of phytoph- well-controlled studies of the phylogeny (71) conclude that although speciation agous insects, Winkler and Mitter (71) of host range indicate that specialists may be promoted by divergent host use found that only Ϸ8% of speciation give rise to generalists as often as gener- in some cases, the great diversity of phy- events included a host shift to a differ- alists give rise to specialists. Indeed, the tophagous insects may be attributed to ent plant family. In conformity with frequency of the direction of shifts be- the sheer diversity of ecological niches Ehrlich and Raven’s scenario (4), most tween these two states may be predict- (in terms of chemistry, structure, or- of the diversification of insect host as- able simply from the proportions of spe- gans, etc) afforded by the great diversity sociations is based on shifts among cialist and generalist species: shifts in of plants. plant lineages that had evolved earlier, either direction may be phylogenetically A key hypothesis in Ehrlich and for almost no instances of cospeciation ‘‘random’’ (71, 81). In nymphaline but- Raven’s coevolution scenario (4) was or congruence between plant and in- terflies, the phylogenetic distribution of that insect lineages that adapt to di- sect phylogenies have been described, generalist and specialist species and the verse, chemically distinct plant clades and molecular dating shows that at frequent parallel origins of specializa- should undergo adaptive radiation and least some insect clades are younger tion on the same few plant lineages led enhanced diversification. There is sur- than the plant clades with which they Janz and Nylin (82) to suggest the ‘‘os- prisingly little evidence on this point. are associated (71). For example, the cillation hypothesis.’’ They posit that Even the simple question, whether or radiation of pierine butterflies (cab- specialists retain a physiological ability not the species diversity of insect clades bage white and relatives) began Ϸ10 to use ancestral hosts and that expan- is correlated with that of their host- million years after the diversification sion of diet to include such ancestral plant clades, has been addressed by only of the glucosinolate-containing Brassi- hosts can serve as an evolutionary a few authors. Basal lineages of Lepi- cales (72). There is some evidence, as bridge to new specialized associations. doptera and the beetle clade Phyto- yet more intriguing than definitive, There is some evidence that ‘‘major’’ phaga tend to feed on conifers and are that the diversification of insect clades host shifts, to different plant families, far less diverse than their sister clades, is temporally correlated, although occur especially in insect lineages that which feed mostly on angiosperms (89, time-lagged, with the diversification of include polyphagous species (71). 90). In the most detailed such analysis, their host-plant clades, a point to What accounts for the great diversity Janz et al. (91) found that species diver- which we return later (71). of phytophagous insects? In a now clas- sity of host plants consistently contrib- Although chemical similarity of plant sic article, Mitter et al. (83) showed that utes to species diversity of clades of the taxa is correlated, overall, with their herbivorous clades are significantly more large butterfly family Nymphalinae. phylogenetic propinquity, the correlation species-rich than their plesiomorphically They suggest that increasing host diver- is not perfect. It has therefore been pos- nonherbivorous sister clades: the herbiv- sity may contribute to speciation by sible to show that host shifts of related orous habit appears to have promoted enabling geographic expansion and insects are more strongly correlated with diversification. Many authors have pos- therefore opportunity for spatial isola- plant chemistry than plant phylogeny. tulated that adaptation to different host tion and genetic divergence. Still less do Examples include shifts between both plants may cause speciation, i.e., con- we know whether adaptation to chemi- congeneric (73) and more distantly re- tribute to the evolution of reproductive cally distinct plants fosters adaptive radi- lated plants (74). Although this corre- isolation. Although much of this argu- ation. In perhaps the most convincing spondence is far from perfect (some ment has centered on the question of example, Wheat et al. (72) ascribe the shifts appear to have been facilitated sympatric speciation (16), ‘‘ecological radiation of the butterfly subfamily instead by ecological propinquity of the speciation’’ stemming from divergent Pierinae, which is much more diverse ancestral and derived host plants) it sug- ecological selection need not be sympat- than its sister group, to the evolution of gests that adaptation to all available ric (84, 85). There is evidence for both a nitrile-specifier protein that detoxifies plants is not equiprobable and evolution allopatric and sympatric ecological spe- the glucosinolate defenses of their di- of host shifts may be guided in part by ciation in phytophagous insects (17, 86). verse Brassicales hosts. In this Special limitations on genetic variation in insect Yet, among 145 pairs of presumptive Feature, Winkler et al. (92), in a new species that make some shifts more dif- sister species in 45 phylogenies, Winkler phylogenetic analysis, provide evidence ficult than others. Futuyma et al. (75, and Mitter (71) found divergence in that evolutionary shifts to chemically 76) could detect genetic variation in host association in only 48%. They different plant clades are associated feeding responses of four specialized noted that there need be no causal rela- with elevated diversification in leaf- species of Ophraella leaf beetles to tionship between host use and specia- mining flies.

Futuyma and Agrawal PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 ͉ 18057 Downloaded by guest on September 27, 2021 In contrast to the ‘‘bitrophic’’ view on of individual defense characters. A few sociations have arisen by ‘‘colonization’’ diversification proposed by Ehrlich and examples have been well documented. from one plant lineage to another, usu- Raven (4), Singer and Stireman (93) European populations of Barbarea vul- ally related and therefore chemically have recently advocated a ‘‘tritrophic garis (Brassicaceae) are polymorphic for similar. The radiation of insect clades niche concept.’’ In its simplest form, the resistance to a major flea beetle herbi- associated with specific plant clades idea is that factors allowing herbivores vore (Phyllotreta nemorum), and the bee- shows a degree of temporal correspon- to escape predation represent additional tle similarly shows a simply inherited dence. For example, Zwo¨lfer and Herbst niche axes of a species (in combination polymorphism for utilization of B. vul- (105) suggested, based on fossil and bio- with adaptations to host plant defenses). garis (95). Differences in furanocouma- geographic evidence, that the weevil Consequently, adaptive divergence and rin profiles among populations of genus Larinus is as old (Oligocene) as speciation in herbivores might be facili- human-introduced Pastinaca sativa (wild the thistle clade with which it is associ- tated by escape from their own enemies parsnip) are matched with the detoxifi- ated, and molecular clock estimates sug- and host plant characteristics. Although cation (cytochrome P450) profile of as- gest that the butterfly subfamily Pieri- the escape of herbivores from predation sociated populations of the specialist nae arose within Ϸ10 million years of and parasitism is clearly important for webworm Depressaria pastinacella (96), the origin of its hosts (72). How long insect community structure and host and the thickness of the exocarp in such clade-level associations, indicative shifts (reviewed in ref. 93), far less at- fruits of Camellia japonica varies clinally of phylogenetic conservatism, persist is tention has been paid to its impacts on in concert with the length of the ros- uncertain. Some higher taxa of insects diversification. Singer and Stireman sug- trum of the plant’s sole seed predator, are largely or entirely associated with gest that diversification will be pro- the weevil Curculio camelliae (97). The plant clades that date from the mid or moted when divergent selection imposed more difficult problem in such cases is early Tertiary, and others associate with by enemies of herbivores is strong (i.e., to show that variation in both parties conifers or monocots, which originated where attack rates are high), and where is a consequence of their interaction in the Early Cretaceous or before. It is ecological opportunity in tritrophic rather than another environmental vari- not certain that all of the insect clades niche space is particularly high (i.e., able. Ultimately, reciprocal transplants thus restricted are comparable in age to where competition is low). Their hy- and measures of selection on specific their host lineages, nor that there exists pothesis could be tested by comparing functional traits in both partners would a continuous age distribution of associa- diversification rates of insect herbivore provide convincing evidence. tions. The strength of any such associa- lineages with different feeding strate- Whatever the distribution of the adap- tion will appear to decay with time as gies, which apparently show differential tations of plants and herbivores to each lineages of the insect clade colonize and rates of enemy attack and competition other may be along the pairwise/diffuse proliferate on other plant clades, as in- (93). Additionally, the impact of adapta- spectrum, their evolution is clearly an sect lineages on the ancestral plant clade tions to enemies (antipredator behav- ongoing process. Related plants may be become extinct, and as plant lineages iors, sequestration of plant toxins, etc.) chemically similar, but they nonethe- have escaped from some of their erst- on diversification rates is essentially less differ in the identity and levels of while herbivores by evolving new de- unexplored. compounds that issue from similar bio- fenses, a point on which, as we noted synthetic pathways, as is clear from earlier, there is little evidence. It may Coevolution comparing the terpenoids of Bursera prove possible to glimpse some of these As we have noted, ‘‘coevolution’’ has (98), the cardenolides of Asclepias (44, dynamics from sufficiently detailed phy- several meanings (94). They include 99), and many other examples. In at logenies of both insects and plants. population-level processes of reciprocal least some cases, divergence is driven by adaptation of interacting species, which selection, as shown by DNA sequence Consequences of Macroevolution for may be relatively specific or pairwise patterns at the methylthioalkymalate Ecological Communities (two species, each adapting to a charac- synthase (MAM) locus in the glucosino- There is a growing appreciation among teristic of the other) or more diffuse late synthesis pathway in crucifers (100). ecologists that long-term evolutionary (multispecific), in which a species adapts Adaptive variation among the detoxify- history has a major role in explaining to the properties of a set of interactors, ing capacities of insects has also been the composition and structure of ecolog- and so has genetically correlated re- documented, for instance in the cyto- ical assemblages or communities, and sponses to several species (51, 52). At a chrome P450’s of Papilio butterflies phylogenetic approaches are indispens- macroevolutionary level, diversity in ad- (101). Many questions remain, however, able in achieving explanation (23, 24, aptations of plants to herbivores and about such variation. For example, do 106, 125). The diversity of herbivores vice versa could range from ongoing new chemical defenses confer advantage associated with plant species in a com- interactions between antagonist lineages, because they are more potent (betoken- munity [part of what Root (107) termed with relatively short time lags between ing escalation) or simply because they a ‘‘component community’’] is not solely reciprocal evolutionary changes, to the are new? Do new biochemical adapta- a consequence of adaptation of insects decoupled, sequential bursts of adaptations of plant or insect compromise ear- to that plant in that region, but is af- tion and diversification portrayed in lier or other adaptations? And finally, fected by the accessibility of that plant Ehrlich and Raven’s ‘‘escape-and- what is the relationship between popula- and its relatives, in both the focal region radiate’’ scenario (4). tion-level adaptations and macroevolu- and elsewhere, to lineages of insect her- Demonstrating reciprocal adaptation tionary processes? bivores whose diet has been shaped by a requires information on function and/or At the macroevolutionary level, we very long history, and by genetic con- selection on relevant characters. Al- have noted that except in special cases straints that contribute to phylogenetic though adaptations of specialized insects [specifically, the seed-predatory agaonid conservatism. For reasons that are still to their hosts have been thoroughly doc- wasp pollinators of Ficus (102)], phylog- almost entirely unexplored, but presum- umented, adaptations of plants to spe- enies of insects seldom match closely ably include constraints on genetic varia- cific herbivore species have been shown those of their host plants. The more tion, some insect clades seem entirely less frequently, partly because there is common pattern appears to be that of barred from feeding on some plant less information on the target specificity sequential evolution (103, 104): the as- clades. For instance, almost no butter-

18058 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904106106 Futuyma and Agrawal Downloaded by guest on September 27, 2021 flies feed on the very large family Rubi- Ecological and microevolutionary pat- Such factors as breadth of geographic aceae (108), and the Orchidaceae, one terns indicate that when closely related range, abundance, and structural archi- of the two largest plant families, is rela- plants coexist shared herbivores may tecture have been implicated by ecologi- tively devoid of associated insect herbi- impose important impacts on commu- cal studies (68, 121). A plant’s fauna has vores. Thus the distribution of herbivore nity structure and selection for defen- doubtless accreted over the course of diversity, and presumably the impact of sive strategies (113, 114). It is also to be time: some species of insects will accom- herbivory, across plant taxa may be expected, then, that as plant communi- pany its origin or its spread to a new highly imbalanced, in part for historical ties assemble over evolutionary time, region, some will use it on first encoun- reasons. herbivore impacts may impose selection ter or will adapt to it soon thereafter; Community ecology cannot be di- on divergence among closely related others will colonize and adapt to it vorced from historical biogeography. A plant species. Becerra (115) recently later, perhaps depending on chemical or regional flora has been assembled over tested this hypothesis by assessing the phylogenetic propinquity to their normal time by invasion from other areas, per- chemical similarity of coexisting and hosts. Just as it is possible, in principle, haps followed by within-region diversifi- noncoexisting Bursera spp. from the to determine the historical sequence in cation, and the composition of the her- Mexican dry forest, trees that are at- which lineages have invaded and diversi- bivore fauna, dominated by insects with tacked by a clade of specialist leaf bee- fied in a regional biota (122–124), so we phylogenetically conservative diets, will tles in the genus Blepharida. The pattern can envision the possibility of phyloge- likewise have a historical explanation. that emerges from this analysis is that as netically tracing the history of the bio- For example, Futuyma and Mitter (109) the spatial scale of communities de- ta’s component communities: the as- analyzed the 90 genera of leaf beetles creases (from regional to local), and as semblages of animals associated with the plant–herbivore relationships be- (Chrysomelidae) recorded from New species of plants. Of course, the phylo- come increasing tight (i.e., toward York. Excluding those with very polyph- genetic history of insect herbivores monophagy) coexisting Bursera tend to agous species or poorly recorded diets, themselves may contribute to commu- be more chemically dissimilar than 56 genera occur also in a distinct bio- nity patterns. In a coevolutionary per- would be expected by chance. Kursar et geographic region (western North Amer- spective, both the history and traits of al. (35) report a similar pattern in the ica, tropical America, or Europe). In both plant and insect lineages have almost all of the genera, species in New genus Inga in their contribution to this Special Feature. Although it is difficult contributed to their joint diversifica- York feed on at least one plant family tion and current associations. that is also used as a host by congeneric to determine whether this pattern arose from herbivore-mediated divergent se- species in a different region. This pat- Speculation and Future Directions lection or an ecological filter preventing tern was highly nonrandom, and equally the local establishment of chemically Here, we outline four major conclusions strong among genera shared with all similar species, these studies make ex- based on the current trends in the liter- three biogeographic regions. Whether a plicit the links between phylogeny, de- ature and speculate on future directions. genus spread to New York from else- fense variation, and the assembly of where or vice versa, it is clear that dis- Y Current investigations confirm phylo- plant communities. persing insect species retain their ances- genetic patterns in plant defense and Similarly, when a plant is first intro- insect host use. Evidence of adapta- tral host preferences and presumably are duced to a region by human transport, it integrated into a regional biota or not, tion is often detected by departures will be colonized soonest by polypha- from phylogenetically correlated simi- depending on the plant species they gous herbivores and specialists that are encounter. larity, such as patterns of conver- adapted to closely related or chemically gence. Exceptional shifts in defensive Not surprisingly, then, the structure of similar plants. The fauna of introduced strategy and insect host use will likely the food web, of the plant/herbivore in- plants, including ‘‘invasive’’ species, be extremely informative, especially if terface, has a strong phylogenetic signal. largely supports this conjecture (116, studied in a phylogenetic context in- In a crude effort that preceded the de- 117). A contribution to this Special Fea- volving replicated divergences. velopment of molecular phylogenies, ture by Pearse and Hipp (118) takes Y Plant and insect traits cannot be Futuyma and Gould (110), using phen- analyses of the insect communities on etic analysis, found that the similarity of nonnative plants to the next level by ex- treated as unitary. Some traits may insect communities on tree species in a amining the relative importance of phy- form coadapted strategies (e.g., se- deciduous forest was somewhat corre- logenetic distance (from native species) questration of plant toxins and apose- lated with the plants’ taxonomic rela- and specific plant traits for the abun- matic coloration in specialist herbi- tionship. Weiblen et al. (111) reported dance of insects on North American vores). Thus, although tradeoffs on a massive study in which associations oaks. In the same vein, introduced spe- clearly must constrain evolution, of 524 species of herbivores that were cialist insects, if they persist in a new tradeoffs may be difficult to detect recorded from more than 62 plant spe- community, generally attack native between two arbitrarily selected traits cies in a New Guinea rain forest were plants related to their normal hosts and they likely occur at the level of analyzed with reference to plant phylog- (119, 120). For this reason, herbivores the overall strategies used by plants eny. The faunal similarity of pairs of that are candidates for biological control and insects. The prevalence of such plants was negatively correlated with are screened for their responses to com- patterns and their effects on trait co- their phylogenetic distance, measured by mercially important plants that are re- evolution are poorly known, although molecular branch length. This correla- lated to the herbivore’s natural hosts, we have a few examples of incremen- tion explained an astonishingly high and sometimes (too rarely?) are tested tal and directional change during di- 25% of the variance in faunal similarity. on related native wild plants as well. versification, the consecutive addition In a similar analysis, Ødegaard et al. The phylogenetic, or ‘‘deep histori- of novel strategies, and the replace- (112) explained an even higher propor- cal,’’ perspective is a relatively recent ment of old strategies by new ones. tion (35%) of the variance in faunal addition to an old question: what deter- Y Phylogenetic methods to assess the similarity of beetles on Panamanian mines variation among plant species in role of traits in diversification range plant species by phylogenetic distance. the diversity of their herbivore fauna? from elegant sister clade compari-

Futuyma and Agrawal PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 ͉ 18059 Downloaded by guest on September 27, 2021 sons to computationally intensive community interactions. Conversely, effects of ecological complexity are estimates of how traits correlate with community–ecological complexity af- little explored and difficult to untan- speciation and extinction rates. fects all aspects of the macroevolution gle, yet are surely important. These methods need further elabora- of plants and insects. Whether we tion, and their application to plant consider the impact of which plant ACKNOWLEDGMENTS. We thank Amy Hastings, and insect diversification is in its in- species coexist in a community, the Marc Johnson, Mike Singer (Wesleyan University), fancy. Little is known about the role intensity of predation and parasitism Jennifer Thaler, and Dan Rabosky for comments of plant and herbivore traits in diver- of herbivores, or the extent of speci- and assistance with this article. A.A.A. is sup- sification, much less their role in co- ficity of plant defense traits on diverse ported by National Science Foundation Grant DEB 0447550. This PNAS Special Feature on Plant evolution. insects, we can expect community in- and Insect Biodiversity grew out of a symposium Y Knowledge of phylogenetic history is teractions to modify classic coevolu- held at the 2008 International Society for Chemi- proving to be critical in understanding tionary predictions. The evolutionary cal Ecology meeting organized by A.A.A.

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