Farrell, B. D., Mitter, C., Futuyma, D. J. 1992

8/14/2019 Farrell, B. D., Mitter, C., Futuyma, D. J. 1992

1/9

Diversification at theInsect-Plant Interface

nsights from by oge zeticsBrian D Farrell Charles Mitter and Douglas J Futuyma

AT and plants and their insect en-L mies together constitute morethan half of all known terres- The structure andtrial species an d a re food for most ofthe rest. The ir interaction is probab lyresponsible, directly and indirectly,for much of terrestrial diversity (Ehr-lich and R aven 196 4). Yet we areonly beginning to understand h ow thediversity of insect-plant assemblagesis determined.The phytophagous insects associ-ated with a particular plant taxonform an ecological unit convenientfor study, because an herbivore spe-cies typically attacks only a few re-lated plants. Considerable study (re-viewed in Strong et al. 19 83 ) hasyielded little evidence t ha t diversity insuch assemblages is limited by inter-specific interactions such as com peti-t ion (but see Jaenike 1990, Zwolfer198 8), once accorded a do minant rolein community structure (MacArthur19 72 ). Reflecting a broader shift fromequilibria1 to contingen t explan ationsin ecology (Ricklefs and Schluter in

Brian D. Farreil is a Sloan PostdoctoralFellow in the Section of Ecology andSystematics, Cornell University, Ithaca,NY 14853 and an assistant professor inthe Department of Environmental, Popu-lation, and Organismic Biology, Univer-sity of Colorado , Boulder, CO 80309.Charles Mitter is an associate professor inthe Department of Entomology, Univer-sity of M aryland, College Park, MD20742. Douglas J Futuyma is a professorin the Departm ent of Ecology and Evolu-tion, State University of New York, StonyBrook, NY 11794. 1992 AmericanIns titu te of Biological Sciences.

diversity of insect plantcommunities seemstrongly influenced by

a long historypress), there is a growing consensusthat phytophage community diversityretlects primarily a balance amongindependent rates of successful colo-nization of new hosts, speciation onthose hosts, and extinction. Theserates in turn will depend, in ways yetunclear, on the geographic and phy-Iogenetic history of the communityand its constituen t species.The o utstanding example of a histor-ical model of insect-plant communitiesis Ehrlich and Raven's (19 64 ) hypoth-esis of coevolLrtion, which has pro-foundly stimulated research on insect-plant interact ions . These authorspostulated an endless evolutionaryarms race whose elements are origin ofa new chemical defense in some-p lantlineage, which by reducing herbivoreattack allows those plan ts to increase inabund ance a nd eventually in diversity;and subsequent evolution of insectcounteradaptations to these defenses,permitting insect radiation in the adap-tive zone represented by the newly di-versified plant group. Current differ-ences in diversity and ecologicaldominance among insect and plantgroups are taken to represent differentstages in the historical sequen ce of es-

cape and radiation (Thom pson 1989)This concatenation of individual fit-ness, abundance, and macroevolution-ary success, although a cardinal themeof the modern evolutionary synthesis(Simpson 1953 ), is by n o means wellestablished, having faced vigorous re-cent opposition (e.g., Gould 1985).Although Ehrlich and Raven's ar-gument rested largely on taxonomicpatterns of pla nt secon dary chemistryand insect bost-plant use, m ost subse-quent work on coevolution has con-cerned irs possible ecological and ge-netlc mechanisms (Thom pson 198 9).Full und erstan ding of th e evoiution ofinsect;plant com mun ities, includingdefinitive tests of the escape-and-radiation model, require complemen-tary study of their long-term hisrory.Reflecting the current resurgence ofthe comparative approach in biologygenerally, spurred in turn' by advancesin phylogeny reconstruction and mo-lecular systematics, there is now agrowing literature on the phylogenet-ics of insect-plant associations. In thisarticle, we review several bro ad issuesemerging from these studies concern-ing the imprint of evolutionary his-tory on insect-plant com munities:

What aspects of insect host useare evolutionarily conservative?If the evolution of new prefer-ences occurs readily, the local dis-tribution of insects over plantspecies should adjust quickly tolocal host a bunda nce o r quality;if there are stron g genetic barriersto such evolution, local associa-tions should reflect instead theirlong-term historim

BioScience Vol. 42 No


2/9

How old are the associat ionsbetween particular extant insectand plant lineages, and to whatextent have such lineages diversi-fied in tandem? Long-continuedassociations provide the greatestopportunity for reciprocal evolu-tionary influence.Is there evidence for the escape-and-radiation steps of Ehrlich andRaven's scenario? Th at is, do phy-logenetic comparisons of extantspecies reveal escalating sequencesof plan t defenses and insec tcounter-adaptations? Do lineagesbearing these innovations showaccelerated diversification?T o what extent do the macro-evol u t i ona ry phenomena ou t -lined abo ve determine the currentdiversity and structure of insect-plant associations?Phylogenetic constraints onhost useThe evolutionary lability o f, trophichabits, which will determine the de-gree to which community structurecan be understood as s im ~ lvhe out -Acome of natu ral selection, is a recur-ring issue in ecology. Genetic varia-tion for host-use traits is common inphytophagous insects, and these her-bivores rapidly colonize at least someintroduced p lant species (Strong et al.1984 ). Although n ot al l such coloni-zations must entail genetic change,rapid colonization suggests that hostuse might evolve readily. However,genetic theory and experimental evi-dence are equally consistent with theexistence of strong barriers to suchevolution. which mav reauire simul-taneous change in several geneticallyi ndependent t r a i t s (Fu t uyma andMoreno 1988, Gould 1991, Jaenike1990) .Phylogenetic evidence can help re-solve the issue of evolutionary con-straint on host choice (Mitter andFarrell 19 91 ). Th e history of host usein an insect clade can be estimatedusing a cladogram (i.e., a phyloge-netic tree)-a bran chin g diag ram de-picting the sequence of divergence ofextant species from a c omm on ances-tor (e.g., Figures 6 7 an d 8)-derivedfrom other (e.g., morphological ormolecular) evidence. The preferencesof the common ancestors implied bythe phylogeny are taken to be those

January 1992

04 16 0 176 32 0 334 480 496 640 656 8requency of host family shift

Figure 1. Frequency distribution of shiftsin host family per speciation event in 25herbivorous insect groups. The largestcategory is that of insect clades for whichless than 17 of speciation events areassociated with host transfer betweenplant families. (Data from Mitter andFarrell 1991that w ould account fo r the habits ofthe extant species with the fewestevolutionary changes. If such histo-ries show that change in reference isLrare, or is restricted to hosts that arein some way mo st similar, it would bereasonable to infer tha t genetic barri-ers to adoption of new hosts haveconstrained th e evolution of diet.So far, few cladograms for phy-tophagous insects have been hro-duced (approximately two dozen),but they provide initial quantitativesuwort for the conventional wisdomar&ng entomo logists (but see Jermy1984) that related insect species userelated plants; change in host-plantfamily typical ly accompanies lessthan 1 7 % of insect speciation events(Figure ;Mitter an d Farrel l in 19 91).This stricture is probably a responseto similarity in plant chemistry, butexactly ho w a nd wh y plant chemistryplays such a cen tral role in insett dietevolution is still much debated (Ber-n a ys a n d G r a h a m 1 9 8 8 , J a en i k e1990, Moran 1988) .On e test, as yet little exploited, forthe genetic constraint suggested bysuch phylogenetic patterns considersthe pattern of genetic variation forpotential use of hosts that an insectspecies does n ot cu rrently attack. Tothe extent that genetic constraintshave guided the evolution of hostaffiliation, host shifts that have oc-curred in evolution should be re-- -fleeted in genetic variation within in-sect species tha t exemplify the feedinghabi t s i mmedi a t e l v be fore t hose.shifts, whereas genetic variation inthese same species should be less

abundant for hosts to which shifhave not subsequently occurred.For example, phylogenetic analysof the Aster acea e-fee ding leaf beetgenus Ophraella (Futuyma and McCafferty 1 99 0) reveals a cluster othree closely related species: two feeon ragweed (Ambrosia) and the thirfeeds on marsh elder (Iv a). The association with Iva has apparently beederived from the Ambrosia feedinhabi t . Futuyma and col labora topredicted and confirmed th at both othe species that retain the ancestraassociation with Ambrosia display genetically based propensity to feeon Iva when deprived of AmbrosiaOne of these species has also beescreened (via analysis of differenceamo ng families) f or g enetic variatioin feeding response to goldenro d (Soidago) and bonese t (Eupator iumplants that o nly distantly related species of Ophraella consume.The phylogeny estimate indicatet h a t E u p a t o r i u m h a s a p p a r e n t lnever been host to the Ambrosiafeeding lineage, an d S olidago has apparently been a host of the lineagonly in the distant past, if at all. ThAmbrosia-feeding species will nofeed, and can not survive, on Solidagoand it shows no evidence of genetivariation for the ability to do so-aresult that conforms to the geneticonstraint hypothesis. Neverthelessthis species does display genetic variation in feeding response to Eupatorium, in appar ent contradiction of thgenetic constraint hypothesis, although there is as yet no evidence thait can survive on this rilant.2Although cornparable studies arvirtually nonexistent, this initial evidence is largely consistent with thegenetic constraints hypothesis. Cornplementary evidence might also comfrom surveys of the apparent evolutionary sources of herbivore colonistcurre;tly adap ted to particu lar plantsConservatism in the assemblvof plant faunasPhylogenetic conservatism of host-plant choice could limit the diversityof herbivores on particular plan t species by restricting invasion of such'D. J. Futuyma, M. Keese, and S. Scheffer1992, unpublished manuscript.'See footnote 1.


3/9

I RhamnalesOther angiosperms MagnollalesRutaceaeAnacardiaceasarex~resln iolalesclades EuphorbialesUrticalesFabales kXSXlIsteridae

Number of milkweed herbivore groupsFigure 2 Frequency distribu tion of affiliations with other plan t orders among 50independent tax a containing herbivores of Asclepiadaceae/Apocynaceae. We countedthe num ber of milkweed-herbivore groups whose closest relatives feed on each of theplant groups listed. Most records- are from the subclass Asteridae or from otherlatex-canal-bearing groups. Asteridae are shown as lightly shaded bars, other latex/resin clades are heavily shaded, and other angiosperms are unshaded. Each plant orderor family for Anacardiaceae and Rutaceae) is presented on the vertical axis with namesfollowing Cronquist 1981).host-based insect communities to asmall subset of preadapted species.Explicit phylogenetic studies are lack-ing, but the operation of such evolu-tionary filters is suggested by broadtaxonomic patterns in some plantfaunas. For example, insects that at-tack the taxonom ic suberouo withint h e c ar ro t f am ily ~ m b i l i f e i a e )hatb e a r s a n g u l a r f u r a n o c o u m a r i n s ,h i g h ly u n u s u a l s e c o n d a r y c o m -pounds, have apparently evolved onlyin insect groups previously adapted tothe more widespread, probably moreprimi t ive , l inear furanocoumarinsBerenbaum 19 83).A broadly similar pattern emergesfor the c lade co m~ ris ed f the o lantfam ilies ~ s c l e ~ i a d i c e a end ~ ~ G c ~ n -aceae, which share a defense syn-drome of latex canals containingtoxic secondary compounds. The her-bivores of these plants are mostlyapos em atic i.e., appa rently advertise,via bright coloration, their toxicity ordistastefulness to predators), often se-ques t e r p l an t t ox ins fo r de fenseagainst qredators, and are both spe-cialized. an d co nservative in feedinghabits. Their nearest relatives nearlyalways feed either on other plantgroups with latex canals or on one ofjust ten families in the sa me subclass,Asteridae Figure 2 . This examplealso suggests colonization by a re-stricted set of preadapted lineages.3C. Mitter and B D. Farrell 1992 unpublishedmanuscript.

Age and persistence of insect-plant associationsIf insect hos t use were sufficientlyconservative, associations of particu-lar insect andmpla ntaxa might persistover extensive periods of geologicaltime. The contemporary distributionof insects over plant species mightthen reflect in pa rt th e relative ages ofthose species. Moreover, long-contin-ued associations, in which the inter-acting l ineages diversify together,should provide the greatest opportu-nity for coevolution sensu Ehrlich an dRaven. Conversely, if the particularassociations have evolved much morerecently, it is unlikely that any exten-sive coevolution has transpired e.g.,Miller page 5 this issue).At the scale of geological epochs,there is some eCidence that the fossilages of major insect herbivore cladescorrespond to those of their predom-inant host groups Zwolfer 1978);moreover, the basal d ivergenceswithin such insect groups are oftenroughly co ncordant w ith host phylog-eny. For example, the M esozoic fossilsof cerambpcid and scolytid beetles rep-resent primitive groups today and,presumably, then) mostly associatedwith conifers, whereas advanced,more recent m embers of these familiesmostly at tack the correspondinglyyounger flowering plants Linsley1961, Wood 1982). The older beetlegroups thus appear to have retainedhost preferences established before the

younger plant groups were available.Recent researc h is revealing similarpatterns at finer scales, underminingthe conventional wisdom t hat the in-sect fossil record is hopelessly incom-plete. For example, the ho st taxa usedby extant genera of chrysomeloid andcurculionoid beetles kn ow n also fromPaleocene-Eocene fossils are signifi-cantly older than those used by beetlegenera for which the oldest fossilsdate only to the Oligocene or Mi-ocene Figures 3 and 4; Farrell andMitter in press). Thus, the primitivechrysomelid genus Donacia is re-ported fr om the sa me Paleocene shalesas its present-day host NymphaeaCrow son 1 981) , a relatively primitiveangiosperm, whereas chrysomelid gen-era currently affiliated with compos-ites an d Conv olvulaceae e.g., Cassidaan d relatives) appear only in fossils ofOligocene and Mioce ne age Farrelland M itter in press). Th e older of theseassociations are, thus, likely to havepersisted for 55-65 million years seealso Hickey and Hodges 1975 , Opler1973 ). Ma ny coincident, apparentlyrelictual geographic distributions ofassociated insects and plants furthersuggest long-continued interactionsEastop 1973, Farrell and Mitter inpress, Humphries et al. 1986, Linsley1963, Mora n 19 89).Parallel diversificationMan y insect-plant associations, it ap-pears, have persisted for much of theTertiary or longer. Currently associ-ated insect and plant lineages may,therefore, have diversified to somedegree in concert, raising th e possibil-ity that their radiation reflects theirinteraction. One expectation undersuch parallel diversification is tha t thephylogenetic order of divergenceamong specific herbivores should cor-respond to that among their hosttaxa. Depending o n the details of theevolutionary process Mitter et al.1991 ), such concordance might rangefrom exact match und er truly simul-taneous speciation) to broad, imper-fect correlation e.g., under episodicplant escape and radiation, and sub-sequent insect recolonization).There have been few explicit stud-ies of parallel ins ect-p lant phylogene-sis; closer collaboration between in-sect and plant systematists is needed.Among 14 assemblages for which at

3 BioScience Vol. 42 No.


4/9


5/9

Phylogeny correspondenceFigure 5. Frequency distr ibut ion of corre-spondence (x-axis) between the phyloge-nies of 14 independent insect groups andthe phylogenies of their respective host-plant groups. The phylogeny correspon-dence is Colless' consensus index (seeFarrell and Mitter 1990) and ranges from0 (no correspondence) to 1 (complete cor-respondence). The phylogenies of mostgroups show some correspondence to hostrelationships, as they might if insects gen-erally either diversify in concert with theirhost plants or track host qualities corre-lated with plan t ~hvloerz nv. ddilional ev-idence (e.g, fro fbssil, biogeographic, ormolecular datings) is necessary to discrim-inate among these or other possible causesof this pattern. (Graph based on unpub-lished data from Mitte r and Farrell 1991.)though pairwise, reciprocal adapta-tion is known in a few instances (e.g.,between particular species of helico-niine butterflies and host Passiflora[Gilbert 19901 and may emerge inother intimate associations, such asthat of Phyllobrotica and Scutellaria.On the other hand, many sets ofrelated phytop hage species (genera o rhigher tax a) typically show conservedassociations with broader host taxa(e.g., plant genera or families). Thus,contemporary insect-plant interac-tions could well reflect the d i h s ecoevolution implicit in Ehrlich andRaven 's ( 19 64 ) essay (i.e., the evolu-tionary responses of a n insect or plan tgroup to a broad spectrum of re-source or enemy species).Phylogenies could provide supportfor the diffuse coevolution hypothesisby revealing evolutionary trends ofincreasingly effective adaptation forattack and defense ( though Vermeij[I9871 cautions tha t t he earlier s tagesof escalation may often be lost toextinction, preventing their study).For such progressions, there is littledefinitive evidence, which is likely torequire a conjunction of phylogeneticand experimental approaches.

Several systems ar e currently unders t u d y . F o r e x a m p l e , B e r e n b a u m(1983 ) has postula ted for Umbel-liferae and other plant groups an ev-olutionary sequence of increasinglytoxic and complex coumarin com-pounds, each reducing attack by ene-mies adapted to the antecedent de-fense. Asclepias milkweeds show anapparent phylogenetic progressiontoward more toxic and complex car-denolides, which, moreover, becomeincreasingly concen trated in the latex,where their effects against herbivoresshould be maximal (Nelson et al.198 1). Initial studies suggest tha t thehighly diverse, more advanced, toxicmilkweeds are free from the arctiidmoths and chrysomelid beetles thatattack chemically and phylogeneti-cally more primitive congeners. Asubset of Tetraopes beetles, which areone of the few herbivores of theseadvanced milkweeds, m ight represent

a recent breakthrough in an arms race(Farrell 1991, Farrell and Mitter inpress).Coevolution andadaptive radiationA second fundamental assertion ofEhr l ich and Raven ' s coevolut ionmodel is that improved defenses andcounteradaptations have led to in-creased diversification of the lineagesin which they arose. Phylogeneticanalysis is beginning t o provide morerigorous tests (e.g., via replicated sis-ter group comparisons; Mitter et al.1988) of such adaptive radiation hy-potheses than do the conventionalascription of evolutionary success towhatever features happen to distin-guish large groups (Farrell et al. 1991,Mitter e t al. 1 988 ). Thus, th e speciesdiversity of a lineage in which a newadaptation has arisen is contrasted

eetle Hoplasoma spp.

subgenusStachyslvorasubgenusPhyllobrotica:

P. quadrimaculate

P circumdata

P. sororiaP. physosteglae

\ P. llmbata

Clerodendrum*Physostegia

Stachys

Scutellaria:S. altissima

S. galericulata

S. integriifoliaS. arenicola

S. incana

S. drummondii

laterlfloraFigure 6 Phylogeny estim ate of Phyllobrotica leaf beetles compared with host Lamialesphylogeny synthesized from the published litera ture (Farrell and Mitter 1990). Beetletaxa are placed opposite their hosts (Phyllobrotica quadrimacufata and Phyllobroticadecora ta both attack Scutellaria galericulata, in the Palearctic and Nearctic, respective-ly), except fo r Phyllobrotica phytostegiae and its host Physostegia, which a re marked byasterisks. Cladogram correspondence is significant or nearly so under several random-ization models. The exceptional association of Phyllobrotica physostegiae with theperennial mint Physostegia probably represents recent colonization from an annual,xeric-adapted ancestral host in the same habitat.

38 BioScience Vol. 42 No.


6/9

most cogently to that of its sistergroup (Figure 7 , which by definitionhas had equal t ime for speciation andextinction and which should differ inthe fewest other characteristics (rela-tive to other more distantly relatedgroups). Replication of such sister-group comparisons is possible whenthe same trait has arisen (throughconvergence) multiple times indepen-dently, allowing statistical control fo rthe characters that might be con-founded with the trait of interest inany one com par ison.The sister-group approach has beenapplied to the evolution of plantsecretory canals bearing latex o r resin(Farrell et al. 1991), a syndrome tha thas evolved many times indepen-dently and for which there is strongevidence of a n antiherbivo re function(Dussourd a nd Eisner 198 7). Lin-eages characterized by such canals areconsistently more species-rich thantheir non-canal-bearing sister groups,strongly suggesting th at defense esca-lation can promote plant radiation(Farrell et al. 1991). Other conver-gen t , apparen t ly defense- re la ted ,plant tra its aw ait similar analysis.Recent inventories of tropical for-ests, in which canal bearers are aprominent element, suggest that spe-cies bearing these defenses have con-sistently elevated population sizes(Boom 198 6, Prance et al. 1976),4possibly in part because they areavoided by leaf-cutting ants (Stra-dling 19 78 ). This observation sup-ports the sti l l-controversial notiontha t popula tion size is both evolution-arily persistent (reviewed in Ricklefs19 89 ) an d linked, albeit by stil l-u n d es c r ib ed m ech an is m s , t o t h eadaptive superiority and evolutionarysuccess of lineages (Lidgard and Jac k-son 1989).The results from sister-group anal-ysis also support another of Ehrlichand Raven s broa d postulates, thatinsect diversification has been greatlyaccelerated by association with higherplants, which has evolved (from ear-lier predaceous o r saprophagous hab-its) in at least 5 0 independent insectlineages whose collective species di-versity a cco unts for m ore tha n half ofa ll i nsec ts ( M i t t e r e t a l . 198 8) .Whether the escape-and-radiat ion4B D. Farrell and C. Mitter, 1992,unpublishedmanuscript.

model (as opposed to the larger re-source base afforded to phytophages,compared with predators) accountsfor the spectacular success of phy-tophages is unk now n: there are as yetno phylogenetic studies of the manypossible examples of radiation aftercolonization of newly diversifiedplant groups (e.g., Berenbaum 1983).One al ternat ive explanat ion, thatrapid speciation is characteristic ofparasitic orga nisms in a broad er sense(Price 19 80 ), seems unlikely: th emany insect clades parasitizing ani-mals, rather than plants, show noevidence of elevated diversificationrates, compared with sister groupshaving other feeding habits.5Global p tterns in diversityInsect-plant coevolution, like othermacroevolutionary interactions, islikely to have a strong geographiccomponent (Darlington 19 57, Vermeij1987). Plants and insects can escapetheir predators or competitors eitherby evolving an a dap tation or by invad-ing a biota that initially lacks counter-measures to the adap tation s (i.e., plantdefenses or insect host use traits) theyalready have. For example, althoughsome introduced plants accumulateherbivores rapidly (Stron g et al. 19 84 ),others remain relatively herbivore-freefor periods ranging from decades tomillions of years. For instance, Eucalyptus was brought from Australia,where it has many insect enemies, toNorth America early in this century,but it still has few enemies in NorthAmerica. The thistle tribe Cardueae,host to a diverse, specialized fauna inits Palearaic center of origin, has fewinsect enemies in the New World, de-spite the proliferation of more than10 0 endemic C ardueae species since itsinvasion in the Miocene (Zwolfer1988). Whether such geographic es-cape repeatably promotes plant diver-sification (an d subsequ ent radiation ofcolonizing herbivores) has yet to betested.Elements of the escape-and-radia-tion model may help to explain thestriking latitudinal gra dients of plantand insect species diversity. The cur-rent extensive regions of temperateclimate date only to the global cool-B. M. Wiegmann, C. Mitter, and B. D. Farrell,1992 unpublished manuscript.

Figure 7 Hypo thetical example of onecomparison of the relative diversity be-tween sister groups. Clade A, marked byan advance in defense 2), s more diversethan its sister group, clade B, which re-tains the primitive defense 1).By defini-tion, sister groups (A and B) are the sameage (Hennig 1966); hus, this difference indiversity would reflect different rates ofdiversification.ing and d rying trend beginning in theearly T ertiary (Wolfe 197 8). Becauseplant families nearly all date back tobefore the Tertiary, most temperateplant groups are derived from ances-tors that lived in tropical environ-ments. Harsh climate has surely lim-ited invasion of or survival in Tertiarytemperate regions to those plantgroups able to evolve app ropria te ad-aptations. For example, the herba-ceous habit of the north temperaterepresentatives of many primitivelywoody, tropical lineages allows over-wintering underground (i.e., escape)during the most severe season (Wingand Tiffney 198 7).In turn, the recently evolved temper-ate flora may have a depauperate in-s e a fauna (compared with the tropics)because primitively tropical herbivoresmust develop analogous adaptations,such as diapause or migration, foroverwintering. These traits probablyarise only in pre ada pted lineages: tem-perate overwintering diapause, for

January 992


7/9

Temperatespecies

Tropicalspecies

illions of years agoFigure 8. Hypothetical example of a primitively tropical clade i.e., its earliest evolutionoccurred in South America and Central America [SA and CA, respectively]) withrecently evolved temperate representatives which occur only in North America [NA]).The tropical element has more species only because it is older: the rate of diversificationis higher in the temperate zone.example, has evolved only in insectgroups w hose tropical representativesshow some form of seasonal quies-cence Taub er et al. 1986) . Herbi-vores, whose host use seems so oftenevolutionarily conservative, face theadd itio nal obstacle of finding suitablehosts in the depauperate temperateflora. They might therefore be ex-pected to show even more pro-nounced latitudinal diversity gradi-ents than insects of more generalizedtrophic habits.The strikingly different latitudinal-diversity gradients in two dominant

beetle families, one herbivorous andone predaceous, provide some initialsup port for these conjectures Farrelland Erwin 1988, Farrell an d Mitter inpress). In forest canopy samples atTambopata, an ecologically diversesite in the Peruvian Amazon, speciesof rove beetles, the largest group ofpredators , are d is tr ibuted evenlyacross habitats of different floristiccomposition, with species diversityand abundance predictable from thetotal canopy foliage volume Farrelland Erwin 1988). In contrast, mostspecies of leaf beetles, the dominant

phytophagous group , are restricted ta single canopy type with diversityand abundance little related to foliavolume, as might be expected of specialized herbivores.Th e leaf beetles, which ar e far mordiverse at a single Peruvian localiti.e., 750 species) than in a muchlarger temperate area that was thoroughly sampled for both beetle families Indian a has 28 6 species of leabeetles), appear to present a muchsteeper latitudinal-diversity gradienChi-s quare 75.8; p < 0.001; d.f

1 han the rove beetles 30 2 and2 8 7 species, respectively, in Peru andIndiana). The hypothesis that steepelatitudinal diversity gradients in leabeetles reflect evolu tionary conservation of these host specializations isupported by the fossil record. Leafand rove beetles both appear to havearisen in the Jurassic Crow son1981 .However, tfie major diversification of leaf beetles, in contrast torove beetles, apparently occurredmuc h later, coincident with the generic-level diversification of their mostlytropical host groups, which have onlyinfrequently entered temperate florasAmong the leaf beetles and othetropical herbivore groups that doreach the temperate zone, radiationmay be promoted by special adaptation to the temperate flora, for example, by shift onto domi nant temperateplant groups Farrell and Mt t e r inpress, Mitter and Farrell in press)This hypothesis awaits rigorous testbut there are many suggestive examples. For instance, the temperatefauna of noctuid moths is dominatedby a huge, evolutionarily advancedcutworm clade, typically grounddwelling and polyphagous on herba-ceous plants, w hereas relatively prim-itive noctuids are primarily arboreafeeders, mostly host specific, andmo st diverse in tropical forests Holloway 1989).In recent decades, historical expla-nations f or latitudin al diversity gradi-ents have been overshadowed byequilibria1 theories based on inherentdifferences between temperate andtropical environments e.g., Janzen1967, Pianka 1978, Stevens 1989)Resolution of this debate has beenhampered by the lack of control forthe greatly differing ages of temperateand tropical climatic conditions. Onesolution is to restrict diversity com-

4 BioScience Vol 42 No


8/9

parison to sister groups, of equal ageby definition (Figures an d 8). Only afew temperateltropical sister-groupcomparisons can as yet be identifiedfor herbivorous insects, but in thesecomparisons there is no suggestion ofa trend toward faster diversificationin the tropics (Farrell and M itter inpress). This result is at least consistentwith the view of diversity gradients asreflecting the tro pical origins of mosthigher taxa (Stebbins 1974).A sobering implication of the his-torical view, long appreciated by ag-ricultural and forest entomologists(e.g., Burke et al. 1986, Krysan andM ~l le r 1986, Wood 1982), is thatmuch of the str uctu re an d diversity oftemperate insect-plant communitieswill be intelligible only as relicts of ( orrelease from the con straint o f) ancientbut fast-disappearing tropical associ-ations. In almost every respect, tropi-cal biotas are insufficiently known,but ignorance of tropical insect-plantinteractions is truly profound. Only avery small fraction of tropical insectspecies has been described, and for amajority of those that have been de-scribed, no ecological information-no t even a single host record--exists.Most of the questions we have raisedcannot be satisfactorily studied usingonly temperate zone species, becauseessential information on their closetropical relatives is lacking. Many ofthe major questions about organismaldiversity and evolution, of which thequestions about insect-plant relation-ships are a sm all sample, will requireboth conservation of tropical ecosys-tems and concerted systematic andecological study of their denizens.ConclusionsThere is substantial evidence thatmuch of the evolution of currentlyaffiliated insect an d p lant lineages hasoccurred over similar geological timeintervals, although cases of strictlyparallel diversification are rare. T hereis also increasing evidence tha t insectsare often conservative with respect tothe evolution of new host affiliations;hence, the structure and diversity ofi n s e c t -p l a n t c o m m u n i t i e s s ee mstrongly influenced by a long history.There is som e evidence that successiveescalations in plant defense have beenmatched by insect counteradaptationand that these counteradaptations, in

turn, have stimulated the diversifica-tion of insects and plants. Thus, theavailable evidence on the evolution ofinsect-plant communities, althoughstill sparse, is largely consistent withthe conclusions reached by Ehrlichand Raven (196 4).AcknowledgmentsWe thank man y colleagues for discus-sions and Lucinda McDade, ScottArmbruster, Rob Colwell, and JulieAnn Miller for comments on themanuscript. We acknowledge supportby the Alfred P. Sloan Foundation(B.D.F.), a grant from the M arylandAgr icu l tu ra l Exper imen t S ta t ion(MAES; C.M. and B.D.F.), USDAgrant 86-CRCR-1-2113 (C.M.), andNSF grant BSR 8817912 (D.J.F.).This article is, in part , scientific articleA-6242 and contribution 841 1from MAES.References citedBenson, W.W., K. S. Brow n, and L. E. Gilbert.1975. Coevolution of plants and h erbivores:passion flower butterflies. Evolution 29:659-680.Berenbaum, M. 198 3. Coumarins and caterpil-lars: a case for coevolution. Evolution 37:163-179.Bemays, E. A., and M. Grah am. 198 8. On theevolution of host specificity in phytophagousarthropods. Ecology 69: 886-892.Boom, B. M . 1986 . A forest inventory in Am-azonian Bolivia. Biotropica 18: 287-294.Brown, V. K. 19 90. Insect herbivory and its

effect on p lant su ccession. Pages 275-288 inJ. J. Burdon and S. R. Leather, eds. Pests,Pathogens and Plant Communities. Black-well Publ., Oxford.Burke, H. R., W. E. Clark, J. R. Cate, and P. A.Fryxel. 1 986. O rigin and dispersal of the bollweevil. Bull. Ent. Soc. Am. 32: 228-238.Cronquist, A. 1981 . A n Integrated System' ofClassification of Flowd ring Plants. C olumbiaUniversity Press, New York.Crowson, R. A. 19 81 .. The Biology of theColeoptera. AcademicPress, New York.Darlington, P. J. 1957. Zoogeography: TheGeographical Distribution of Animals. JohnWiley Sons, New York.Dussourd, D. E., and T. Eisner. 1987. Vein-cutting behavior: insect counterploy to the, latex defense of ,plants. Science 237: 898-901.Eastop, V. F. 1 973 . Diversity of the Sternor-rhyncha within major climatic zones. Pages71-88 in L. A Mou nd and N. Waloff, eds.Diversity of Insect F aunas. ,Blackwe ll Publ.,London.Ehrlich, P. R., and P. H. Raven. 1964. Butter-flies and plants: a study in coevolution. Ev-olution 18: 586 60 8.Farrell, B. D. 1991. Phylogenetic studies ofinsectiplant interactions: Tetraopes (Co-

leoptera: Ceramb ycidae) and Asclepias (As-clepiada ceae). Ph.D. dissertation , Universityof Maryland, College Park.Farrell, B. D. Dussourd, and C. Miner. 1991.Escalation of plant defense: do latexlresincanals spur plant diversification? Am. Nut.138: 881-900.Farrell, B. D., and T. L. Erwin. 1988. Leaf-beetle commun ity structure in an amazonianrainforest can opy. Pages 73-90 in P. Jolivet,E. Petitpierre, and T. J. Hsiao, eds. Biologyof Chrysomelidae. Kluwer, Dordrecht, TheNetherlands.Farrell, B. D., and C. Mitter. 1990 . Phylogen-esis of insectlplant interactions: have Phyllo-brotica leaf beetles (Chrysomelidae) and theLamiales diversified in parallel? Evolution44: 1389-1403.In press. Phylogenetic determinants ofinsectlplant community diversity. In R. Rick-lefs and D. Schluter, eds. Historical andGeographic Determinants of CommunityDiversity. University of Chicago Press, Chi-cago.Futuyma, D. J. and S. J. McCafferty. 1990.Phvlogenv and the evolution of host ~ l a n t.associations in the leaf beetle &nusOphraella (Coleoptera, Chrysomelidae). Ev-olution 44: 1885-1913.Futuyrna, P J., and G. Morepo. 1988. Theevolution of ecological special~z ation.Annu.Rev. Ecol. Syst. 19: 207-234.Gilbert, L. E. 1990. Biodiversity of a CentralAmerican Heliconrus community: pattern,process and problems. Pages 40 3 4 3 0 in P.W. Price, T. L. Lewinsohn, G. W. Fernandes,and W. W. Benson, eds. Plant-Animal lnter-uctions: Evolutionary Ecology in Tropicalan d Temperate Regions. John Wiley Sons,New York.Gould, F. 1 991. Arthropod behaviour and theefficacy of plant protectants. Annu. Rev.Entomol. 36: 305-330.Gould, S. J. 1985 . The para dox of the first tier:an agenda for paleobiology. Paleobiology

: 2-12.Hennig, W. 1966. Phylogenetic Systematics.University of Illinois Press, Urb ana.Hickey, L. J., and R. W. Hodges. 1975. Lepi-dopteran leaf mine from the early EoceneWind River formation of northwestern Wy-oming. Science 1 89: 71 8-720.Holloway, J. D. 1989. The Moths of Borneo.part 12 Noctuidae: Noctuinae, Heliothinae,Hadeninae, Acronictinae, Amphipyrinae,Agaristinae. Southdene, K uala Lurnpur.Humphries, C. J., J. M. Cox, and E. S. Nielsen.1986 . Nothofagus and its parasites: a cladis-tic approach to coevo lution. Pages 53-76 inA R. Stone and D. L. Hawksworth, eds.Coevolution and Systematics. ClarendonPress, Oxford, UK.Jablonski, D. 1987. Heritability at the specieslevel: analysis of geographic ranges of Cre-taceous mollusks. Science 238: 360-363.Jaenike, J. 1990. Host specialization in phy-tophagous insects. Annu. Rev. Ecol. Syst. 21:243-274.Janzen, D. H. 1967. Why mountain passes arehigher in the tropics. Am. Nut. 101: 233-249.Jermy, T. 1984. Evolution of insecthostplantrelationships. Am. Nut. 124: 609-630.Krysan, J. L., and T. A Miller, eds. 1986.Methods for the Study of Pest Diabrotica.Springer-Verlag, New York.


9/9

Lidgard, S., and J. B. C. Jackson. 1989.Growth in encrusting cheilostome bryozo-ans. I. Evolutionarv trends. Paleobioloav15: 255-282.Linsley, E. G. 1961. Cerambycidae of NorthAmerica. Part I. Univ. Calif. Publ. Entomol.18: 1-135.1963. Bering arc relationships in Ce-rambycidae and their hostplants. Pages 159-178 in J. L. Gressitt, ed. Pacific Basin Bioge-ography. Bishop Museum Press, Honolulu,HI.MacArthur, R. H. 1972. GaogmphLal Ecol-ogy. Harper and Row, New York.Miller, J. S. 1991. Host-plant associationsamon g prominent moths. BioScience 42: 50-57.Mitter, C., and B. D. Farrell. 1991. Macroev-olutionary aspects of insectlplant interac-tions. Pages 35-78 in E. Bernays, ed. Insect1

Plant Interactions, vol. 3. CRC Press, BocaRaton, EL.Mitter, C., B. D. Farrell, and D. J. Futuyma.1991. Phylogenetic studies of insecdplantinteractions: insights into the genesis of di-versity. Trends Ecol. Evol. 6: 290-293.Mitter, C., B. Farrell, and B. Wiegmann. 1988.The phylogenetic study of adaptive zones:has phytoph agy promoted insect diversifica-tion? Am. Nut. 132: 107-128.Mora n, N. A. 1988. The evolution of host-plant alternation in aphids: evidence for spe-cialization 3s a dead end, Am. Nut. 132:681-706.1989. A 48-million-year-old aphid-host plant association a nd co mplex life cycle:biogeographic evidence. Science 245: 173-175.Nelson, C. J. J. N. Seiber, and L. P. Brower.1981. Seasonal and intraplant variation of

BioScience is the mo nthly ma gazine fo r biologists in all fields. It in cludes articles o n research,policy, techniques, and education; news features on developments in biology; book reviews;announcements; meetings calendar; and professional opportunit ies. Published by the Arneri-can Institute of Biological Sciences, 730 11th Street, NW Washington, DC 20001-4521;2021628-1500. 1992 membership dues, including BioScience subscription: Individual45.00/year; Studen t %25.00/year. 1992 Institutiona l subscription rates: 99.50/year (domes-tic), 127.00/year (foreign ).

cardenolide content in the California milk-weed Asclepias eriocarpa, and implicationsfor plant defense. J. Chem. Ecol. 7: 981-1010.Opler, P. A. 1973. Fossil lepidopterous leaf-mines demonstrate the age of some insea-plant relationships. Science 179: 1321-1323.Pianka, E. R. 197 8. Evolutionary Ecology.Harper and Row, New York.Prance, G. T., W. A. Rodriguez, and M. F.DaSilva. 1976. Inventario florestal de umhectare de mata de terra firme km 30daestrada Manaus-ltacoatiara. Acta Ama-zonica 6: 9-35.Price, P. W. 1980. Evolutionay Biology ofParasites. Princeton University Press, Prince-ton, NJ.Ricklefs, R. E. 19 89. Speciation an d diversity:the integration of local and regional pro-cesses. Pages 599-624 in J. Endler and D.Otte, eds. Speciation and its Consequences.Sinauer, Su nderland, MA.Ricklefs, R. E., and D. L. Schluter. In press.Historical Determinants o Community Di-versity. University of Chica go Press, Chi-cago.Simpson, G. G. 1953. The Major Features ofEvolution. Columbia University Press, NewYork.Stebbins, G. L. 1974. Flowering Plants: Evoiu-tion Above the Species Level. Harvard Uni-versity Press, Cambridge, MA.Stevens, G. C. 1 989. The latitudinal gradient ingeographical range: how so many speciescoexist in the tropics. Am. Nut. 133: 240-256.Stradling, D. J. 197 8. The influence of size onforaging in the a nt, Att.2 cepha lotes, and theeffect of some plant defense mechanisms. J.Anim. Ecol. 47: 173-188.Strong, D. R., J. H. Lawton, and T. R. E.Southwood. 1984. Insects on P[ants. Har-vard University Press, Camb ridge, MA.Tauber, M. J., C. A. Tauber, and S. Masaki.1986. Seasonal Adaptations of Insects. Ox-ford University Press, New York.Thompson, J. N. 1989. Concepts of coevolu-tion. Trends Ecol. Evol. 4: 179-183.Vermeij, G. J. 198 7. Evolution an d Escalation:An Ecological H isto ry .of Life. PrincetonUniversity Press, Princeton, NJ.Win g, S. L., a nd B. H. Tihey. 1987. Interac-tions of angiosperms and herbivorous tetra-pods throug h time. Page s 203-224 in E. M.Friis, W. G. Chaloner, and P. R. Crane, eds.The Origins of Angiosperms and Their Bio-logical Consequences. Cambridge UniversityPress, New York.Wolfe, J. A. 1978. A paleobotanical interpre-tation of Tertiary climates in the NorthernHemisphere. Am. Sci. 66: 694703.

Wood,. S. L.. 1982. T he bark and ambrosiabeetles (Coleoptera: Scolytidae) of Northand Central America: a taxonomic mono-graph. Great Basin. Nut. 6: 1-685.Zwolfer, H. 1978. Mechanismen und Ergeb-nisse der Co-evolution von phytoph agen undentomophagen Insekten und hoheren Pflan-zen. Sonderbd. Naturwiss. Ver. Hambg. 2:7-5 0. 1988. Evo lutionary an d ecological re-lationships of the insect fauna of thistles.Annu. Rev Entomol. 33: 103-229.

BioScience Vol 42 No

Documents

Farrell, B. D., Mitter, C., Futuyma, D. J. 1992