Evolution of Feeding Behavior in Insect Herbivores
Success seen as different ways to eat without being eaten Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 Elizabeth A. Bernays
nsect herbivores are extraordi In this article, I provide examples narily diverse and abundant. Ap An unparalleled of different approaches to under I proximately a quarter of the di standing the evolution of feeding versity of all eukaryote species can diversity of feeding behavior in insect herbivores. After be accounted for by insects that feed setting the scene by discussing the on tissues of green plants, excluding habits is influenced by historical setting and the diversity of those that feed on nectar and pollen. feeding modes that have evolved, I Some insect herbivores feed on di the diversity of plants describe the biology of feeding be verse plant species from unrelated havior, demonstrating the needs and plant families and may be consid and their chemistry, constraints faced by herbivores and ered food generalists. Many more the different solutions to the prob have restricted diets; they feed only and by natural enemies lem of obtaining a suitable diet. I on species within one plant family, of the herbivores also address the multiple roles of on a group of related plants, or even plant secondary metabolites and how on just one plant species. Most are they may interact with other ecologi also restricted to feeding on particu herbivores, as illustrated in the fossil cal factors to select for specialized lar plant parts, such as leaves, roots, record, provides some information feeding behavior. In cases for wh ich or reproductive organs; smaller in on how herbivore diets have evolved. the ecological functions of particu sects may be restricted to feeding on In addition, phylogenetic approaches lar behavioral traits can be estab particular tissues, such as phloem, to the patterns of herbivory that are lished, it is assumed that the func parenchyma, or developing seeds. seen today, together with studies of tions provide insights into the forces Ecologically, the significance of in geographie variation in host affilia responsible for the evolution and sect herbivores is profound. First, they tions of herbivores, provide insights maintenance of those traits. can dramatically reduce plant fitness, into how changes in affiliation might either directly or indirectly (i.e., by have evolved. Although these studies History of insect herbivores reducing plant competitive ability). are important in our overall under Second, they support an almost equal standing of the evolution of feeding Four hundred million years ago, number of species of invertebrate behavior, they do not substitute for plants evolved terrestrial forms. Dur predators and parasitoids. Third, the study of behavior itself. Not only ing the following 40 million years, they provide a major food source for is it difficult and time consuming to dense vegetation occurred on land a large proportion of birds and liz examine behavior, but also behavior together with terrestrial arthropods, ards and for some small mammals. leaves no fossils and is relatively la including the first insects. By the This diversity of insect herbivores bile in evolutionary time. Moreover, Carboniferous period, 300 million reflects a diversity in diet and feed the interplay between behavior and years ago, all of the major insect ing behavior. The history of insect evolution is bidirectional. Natural orders that feed on plants had selection operates on behavior, but evolved, with the probable excep behavioral changes made by an indi tion of the Lepidoptera (Figure 1). Elizabeth A. Bernays (e-mail: schistos@ag. vidual alter the suite of selective By this time, insects had already par arizona.edu) is Regent's Professor Emeri tus at the University of Arizona in the forces that then operate. For example, titioned the available food resources, Departments of Entomology and of Ecol learning to avoid one noxious food and a number of highly specialized ogy and Evolutionary Biology, University or habitat may lead to selection fa insect feeding types had evolved, in of Arizona, Tueson, AZ 85721. © 1998 voring behavioral patterns that had cluding spore feeders, sap suckers, American Institute of Biological Sciences. not previously been useful. and gall makers (Labandeira and
January 1998 35 mya Phillips 1996). Feeding on re- CENOZOIC Additional evidence that productive tissue of early QUATERNARY polyphagy may be ancestral pteridophytes (ferns) was one comes from the finding that niche that was probably sub TERTIARY it is more common among divided among several extinct Grasses the Orthoptera than among orders. Phloem feeding may MESOZOIC Radia~~~ig!:;::::,~ceous insect orders that evolved 100 also have evolved during the CRETACEOUS later (Figure 1). However, the Angiosperm radiation Carboniferous period, when evolutionary pattern of diet suitable vascular tissue be- breadth is probably not so came available. Typical chew JURASSIC simple. Over the last 100 ing insects, feeding externally, million years, herbivory has also had a niche, with the 200 Flowers evolved probably 50 or more evolution of laminate leaf tis TRIASSIC times independently in sev- sues. Thus, some basic tissue PALEOZ=07:IC::----I eral different ancient lin Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 specificity in diets evolved Gymnospermsdominale eages. The current patterns PERMIAN early as the insect orders ra of host use that vary among diated, probably in an envi- taxa may, thus, have been 300 ronment in which plants were CARBONIFEROUS Laminate leaves & phloem governed by various ecologi abundant, underutilized, and pteridophytesdominate cal factors that provided dif not diverse. Seeds ferent selection pressures at The feeding apparatus of Trees these different times. DEVONIAN insects evolved from the ap Tenninal spore structures Contrary to what is stated 400 pendages of three primitive Plants on land in much of the literature, head segments. Among cur SILURIAN there is evidence that early rent insect groups, homolo- herbivores from several dif gous structures can be identi Figure 1. Simplified phylogenie history of the inseets, showing ferent orders had relatively fied even when the adaptive the origin of major orders of herbivorous inseets and some specialized diets. For ex changes have been extreme. assoeiated biotie ehanges. After Labandeira and Phillips 1996. ample, several more primi Paired biting structures may tive groups of grasshoppers be present, or one or more te nd to be rather specialized, pairs of mouthparts may be elon nificantly more diverse than their whereas more derived grasshopper gated to produce different kinds of nonherbivorous sister groups (e.g., groups such as the Acrididae, which piercing and sucking, or lapping, Mitteret al. 1991). This finding pro later radiated extensively, contain organs. Such adaptations in the feed vides important evidence for the role high proportions of generalists (H. ing apparatus of insects presumably of plants in promoting diversifica F. Rowell, unpublished data, Uni evolved as potential food items in tion, which could have occurred by versity of Basel, Switzerland). In the creased in variety; the maximum di stepwise coevolutionary arms races, Order Lepidoptera, a few clades have versity of insect mouthpart types was as discussed by Ehrlich and Raven unusually high proportions of gen apparently established weil before (1964) and, subsequently, by many eralists, with the most conspicuous the appearance of angiosperms 200 others. This diversification could also being the large derived superfamilies million years ago. Numbers of insect have been a result of insects "track Geometroidea and N octuoidea families have been high since that ing" plant phylogenies, with minor (Nielsenand Common 1991). Within time; some groups disappeared, chemical changes in plants allowing lepidopteran families and subfami whereas in three herbivorous or evolving populations of insects to lies, there is also evidence that ders-the Coleoptera (beetles), the change and speciate, perhaps long polyphagy is often derived. Similarly, Lepidoptera (moths and butterflies), after the chemical changes occurred. in the Order Hemiptera, aphids are and the Diptera (flies)-family num The evident success of insect her thought to have evolved as special bers have more than doubled in the bivory is somewhat surprising, be ists on an extinct group of gymno last 100 million years (Labandeira cause the low protein levels of the sperms and then to have transferred and Sepkoski 1993). Proliferation of nonreproductive tissues of most to conifers and to the angiosperm genera and species in these groups plants make them poor food re family Hamamelidae, and thereafter also appears to have been extraordi sources (Southwood 1978). Conse to have further radiated and evolved narily high, and it is, therefore, quently, many biologists have sug polyphagous habits (Eastop 1978). among these groups that the expla gested that evolution to herbivory In particular, the most species rich nations for the numerical abundance proceeded via mixed feeding on re groups of aphids appear to be those of herbivorous insect should be productive parts or spores, dead tis that evolved different life forms and found. sues of plants and animals, and fungi. that were able to feed on plants in Although the extreme diversity of This progression implies that omnivory many more families than their ances insect herbivores has long been ac preceded generalized herbivory and tors without such alternative life knowledged, recent phylogenetic that the evolution of specialization forms (Moran 1988). Similarly, al studies of insect lineages confirm that on specific plant taxa was a later though bees feed primarily on pollen herbivorous insect groups are Slg- accomplishment (Dethier 1954). and were not among the earliest Hy-
36 BiaScience Val. 48 Na. 1 menoptera, recent studies indicate a) Saturniids b) Sphingids mechanism and many of the de that in at least two major groups tails of feeding behavior, such as of them, polyphagy is derived. The the orientation of the elongated limited ability of bees to use di mouthparts within the plant, verse plants is, indeed, considered which tissues are sampled, and to be an evolutionary constraint how often food is sampled. Spe (e.g., Muller 1996). eies specialized to feed on phloem Although the original patterns or xylem use fine tubes that are of feeding behavior of herbivo formed from particular mouth rous insect groups cannot yet be parts, called stylets, for food in evaluated with certainty, many stud take. An individual "plugs into" ies of diverse herbivorous insects c) the food, and feeding then be thus indicate that the evolution of comes its dominant activity. 0.6 xX diet breadth has not been just a N x Within a particular phloem-feed E pattern of increasing specialization. E- x ing group, such as the aphids, Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 :; x Cl x. Over evolutionary time, diet breadth 0.4 x x differences in details of stylet mor .s x (I) in insects has both increased and N X phology appear to be related at ·in x decreased. (]) x (3 x least partly to leaf anatomy and t: 0.2 x
38 BiaScience Val. 48 No. 1 throughout life, and the feeding pat Figure 4. Patterns of Specialist Intermediate Generalist terns of larval and adult forms are use of plant secondary cn usually similar. Furthermore, because metabolites as cues by ~ herbivorous insects. .0 the grasshoppers and their kin are ttl behaviorally flexible and mobile, they Specialists are repelled Q5 can adapt to the limited changes in or deterred by most of E needs by altering their behavior and :~:r~ct~~~r~~~m~~~~~~ ic eating a different mixture of plants ,-----:~--~~- Une of no effect by a few that charac- 8 or plant parts. At optimal tempera terize the host plants. m tures and on high-quality food, they Generalists are both "E spend 5-10% of their time feeding. deterred by a large ~ This figure is similar during each of number of chemieals .9 the larval stages, during the periods and stimulated to feed ~ when they are actively feeding. By by a large number of ~ contrast, holometabolous insects them, especially when .~ Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 those species, such as beetles, flies, they are in low con- (ß moths, and butterflies, that undergo centration. Every kind of intermediate situa a complete metamorphosis and have tion probably exists. a pupal stage-tend to have larvae Numbers of compounds that grow fast and must feed more than similar-sized larvae of he mime Roles of plant If the herbivore belongs to a clade of tabolous insects. The adults either feed secondary metabolites species specialized on plants with on something completely different, different chemistries, its responsive such as nectar, or feed much less, The vast numbers of diverse second ness to host chemicals may have unless they are egg-producing females. ary metabolites in plants profoundly evolved by a simple change in sensi A multitude of different foraging affect the behavior of herbivorous tivity of the taste receptor system or strategies and feeding behaviors have insects and, thus, the evolution of the brain to one or a few chemicals. evolved among the insect herbivores. that behavior. These compounds may If the herbivore is a specialist that Different plant structures and differ be either repellent or deterrent. In ad has evolved relatively recently from ent patterns of plant availability and dition, the deleterious post-ingestive polyphagous ancestors, the chemi distribution require different forag effects of some of them enable insects cal requirement is more likely to have ing strategies. Moreover, the ever to tearn to reject a plant (Bernays evolved after the establishment of present risk of predation also con and Lee 1988). Many other plant the narrow host range, perhaps as an strains feeding behavior (Stamp and secondary metabolites serve as rela aid to rapid host finding or recogni Casey 1993). Indeed, for an insect tively unspecific attractants or feed tion (Bernays and Wcislo 1994). herbivore, the key problem is to eat ing stimulants, although more com Specialists are behaviorally more without being eaten. Perhaps in the monly one or more particular readily repelled or deterred by chemi holometabolous groups, the dangers secondary metabolites in a plant spe cals they do not normally encounter, of feeding are partly offset by their cies serve as specific attractants or such as most plant secondary me relatively rapid development. Early stimulants for feeding by insects tabolites. However, it is difficult to instars of these rapidly developing adapted to that plant. They also serve separate cause from effect in the evo insects require especially high pro as cues by wh ich an insect learns to lution of this pattern. Sensitivity to tein foods, whereas in later instars recognize a particularly suitable host these chemicals could have evolved the balance changes toward more plant. Insects with different host secondarily, after restricted feeding carbohydrates. Thus, insect life his plant ranges appear to have differen behavior evolved, or i~ could have tory often involves behaviors that tial sensitivity to the potential posi been a cause of restricted host use change drastically in the middle of tive and negative effects of plant from the start. Many secondary me larvallife (Gaston et al. 1991). secondary metabolites (Figure 4). tabolites are not noxious if ingested, Because most insect herbivores are As mentioned above, the majority suggesting that in at least some cases, not generalists, they do not have the of insect herbivores feed on a re it is not physiologically necessary for option of changing the mix of foods stricted suite of plant species, often the insects to avoid them or the plants eaten. However, they can change only one. The choice of host plant in wh ich they occur (Bernays and their feeding strategies. For example, depends largely on the secondary Graham 1988). In some grass-feed several lepidopterans that feed on chemistry of the plant, although nu ing grasshoppers, for example, sen cereals start larvallife feeding on the trients can also playa part. Com sitivity to nonhost chemicals is ap youngest, or whorl, leaves, whose monly, the host range of extant her parently derived, having followed the protein levels are relatively high. bivore species is defined by the evolutionary acquisition of this spe Then, halfway through development, distribution of one or a few character cialized and rather bland diet. It may the larva emerges from the whorl, istic chemicals, such as glucosinolates be that becoming more or less spe migrates to the base of the culm, and (in the case of cabbage butterfly lar cialized involves individuals being initiates a tunnel. Here, it can feed on vae) and iridoid glycosides (in the deterred more or less by unusual tissues that are richer in carbohydrates. case of checkers pot butterfly larvae). chemicals, such as most plant sec- january 1998 39 ondary metabolites. If so, a speciation of the subpopula basic change in the sensitiv tion. These mechanisms may i ty of receptors for "deter be geographic, or they may rent" (i.e., bitter) compounds be changes in such factors as in the insect taste system the flight times of reproduc 2 2 could underlie major shifts in ing insects or the preferences diet breadth (Bernays and 3 3 for mating sites. Natural Chapman 1994). chemical variations among The relationship between plant populations are now the diversity of plants (and 4 4 known to be common; vari their secondary metabolites) ants readily emerge by ge and the diversity of herbivo netic drift, especially in small rous insect species has stimu populations (Rausher 1992). Plant species Insect species lated research and discussion In addition, insects show ge in recent decades. Ehrlich and Figure 5. A hypothetical case of parallel evolution of a group netic variation in relevant sen Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 Raven (1964) made the case of herbivores and a group of plants. Insect herbivory selects sory processes (Wieczorek for a stepwise coevolution for a new plant defense (a). The new genotype expands and 1976, Frey and Bush 1990), ary arms race, in which a new becomes a new species in the herbivore-free space. The insect so that rapid shifting of indi defense on the part of plants herbivore then adapts to the new defense at x, selecting once viduals or populations onto allows their radiation and again for a new plant defense (b). The reciprocal process may plant chemical variants can be repeated many times. For this stepwise "coevolution" to speciation, and the subse occur, several criteria must be met: the particular herbivore be envisaged. quent evolution of counter must influence fitness of the host, the new defense must Behavioral and phenotypic defenses by insects allows provide long enough protection from this herbivore to effect isolating mechanisms have insects, in turn, to undergo speciation events, and the herbivore must speciate along also been described within new colonization and specia plant species lines. An alternative scenario is that drift or herbivore species that enable tion events. Several lines of alternative selection pressures influence plant chemistry and popula tions using different evidence support this possi that the specialized herbivore population subsequently splits host plant species to diverge. bility. For example, Farrell et into populations (and species) with differing preferences for In one example, caterpillars a1. (1992) showed that in the related plant types, perhaps under the influence of factors of the foliage-feeding moth, plant taxa that produce la other than the putative plant defense. Alsophila pometaria, were tex, a substance that is gener- found to have genotypes with ally effective in preventing herbivory minor neural and behavioral changes, different host preferences. The pre by unadapted insects, more plant such as adopting a slightly different ferred host plant species of each moth species have evolved than in sister chemical host signal. genotype produces its new leaves at taxa of plants that do· not produce A simple hypothetical case of plant the time that caterpillars of that geno latex. This observation supports the and insect parallel evolution is shown type hatch. This scenario could, in idea that diversification is enhanced in Figure 5. A stepwise arms race turn, cause the genotypes to become in plants that are better defended process would involve a new defense temporally reproductively isolated against herbivory. arising in the plant as a result of (Futuyma et a1. 1984). Another ex Although plant chemistry is clearly selection pressure by the herbivores. ample of diverging host use among an important phylogenetic constraint The new genotype then expands in populations within a species is in the in insect herbivore host use, whether the period when herbivory is reduced apple maggot fly, Rhagoletis pomo the constraints relate mainly to the or absent. The insect herbivore even nella, which was restricted to haw presence of deterrents in nonhosts or tually adapts to the new defense, thorn 150 years ago. Ir has since the absence of specific stimulants in putting press ure on the new geno established a new host race on apples the hosts is generally not clear. How type, which ultimately pro duces an (Bush 1994), which was possible be ever, some evidence suggests that it other new defense, and the process cause of limited movement of flies is the positive function of chemicals continues. An alternative scenario between the different hosts. Later, that is important. For example, for parallel evolution of insects and several behavioral and physiological among swallowtail butterflies, spe plants is that a plant species pro factors became differentiated in the cies of Papilio have bridged host duces a chemical variant that has no two populations. For example, the families via common chemicals particular disadvantage and is not two host races have different emer (Feeny 1991). In addition, the re easily recognized by the individuals gence times (that match host fmit stricted diets of many herbivores seem of the specific herbivore population. availability) and show genetic differ to correlate with the distribution of However, variations among the her ences in host preferences (Bush 1994). certain chemicals or classes of chemi bivores in the sensory system confer The great capacity of even behav cals (e.g., Stadler 1992). These find on some members of the population iorally specialized insects to handle ings imply that where parallel clado an ability to identify the new plant potentially toxic compounds suggests genesis has occurred, herbivore genotype and, thus, to use it as they that behavioral mechanisms pre species constrained to feeding on a would the original plant genotype. dominate in initiating changes in host particular plant can evolve to feeding In either scenario, appropriate iso use. Because specialists use limited on a new host plant only through lating mechanisms are required for suites of chemical cues in host iden-
40 BioScience Vol. 48 No. 1 tification, yet are apparently able In some insect groups, there are or chemically similar plant species physiologically to handle nonhost patterns of expanding or narrowing (Thompson 1994). chemicals, it is likely that these small, diet breadth. The swallowtail but The studies of Papilio butterflies active organisms, which are highly terflies have been in existence for clearly indicate that diet breadth can vulnerable to predators yet have small nearly 50 million years, yet their narrow or broaden according to dif brains, must employ simple, easily diets are more or less restricted to ferent selection pressures. Butterfly identifiable cues in decision-making five angiosperm families that share host selection behavior and caterpil to remain both efficient and vigilant some secondary chemistry. Most of lar feeding ability both vary and are (Bernays and Wcislo 1994, Bernays the swallowtail species feed on a under separate genetic control, with 1996b). small number of plant species. In the an implied lability in host range, genus Papilio, the subject of many albeit with certain constraints. The meaning of diet breadth plant-insect studies, the original host Specialists predominate outside was the genus Citrus in the family the Orthoptera, and there is evidence Breadth of diet is a continuum. Her Rutaceae. Later, there were host that in many specialist lineages, spe bivores range from being extreme shifts and speciation on species of ciation and switches in host use oc Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 generalists to being restricted to a Apiaceae (Umbelliferae) that contain cur readily, but the species remain single plant species. Studies on her volatile and nonvolatile chemicals specialists. One example is that of bivores in different taxa are provid similar to those in citrus and that Yponomeuta moths, whose host use ing insights into variation at the spe stimulate oviposition (Feeny 1991). has diverged from a primitive use of cies, population, and individual Papilio glaucus (tiger swallowtail), plants in the family Celastraceae to levels-insights that are necessary to however, escaped from the chemical plants in totally unrelated families. understanding factors favoring the constraints as it expanded from its The original hosts, species of Euony different patterns of diet breadth. original tropical region. It can now mus, remain hosts for most extant At one end of the spectrum are feed on plants in 30 plant genera in Yponomeuta moth species, but in extreme generalists (at the species, 17 families in North America. The one European clade of 14 species, population, or individual level). glaucus clade has, in turn, given rise four have shifted to Rosaceae hosts, Among the generalist grasshoppers, to three species, each restricted to one to Salicaceae, and one to each individual tends to mix its foods, small subsets of the hosts used by P. Crassulaceae. All except one of this and some aposematic species, which glaucus. These changing patterns in European clade of moths are strictly advertise their chemical defenses, host use by a group of temperate monophagous on plants in four fami forage on as many as 20 different swallowtails reflect diverse biotic and lies that are unrelated taxonomically hosts in the course of a day. Other abiotic factors (Scriber et al. 1991). and phytochemically. The exception, grasshopper species that tend to be For example, so me evidence indi Yponomeuta padellus, consists of more cryptic on foliage switch foods cates that the tiger swallowtail had host races that specialize on differ just one to four times per day, de to expand its host range because the ent species of Rosaceae. This species pending on relative availability and climatic vagaries of the higher lati is an example of a situation in which nutrient complementarity (Chambers tudes meant that ancestral host types speciation events are in progress et al. 1996). Both types of grasshop were unpredictable. (Menken 1996). pers are generalists at all levels Species of Papilio in the machaon Another example of host switches species, population, and individual. species group have been studied in occurring in a specialist species is By contrast, in general ist species in tensively in the western United States, provided by Ophraella leaf beetles, other taxa of insect herbivores, dif where they use plants in the families wh ich have restricted diets that of ferent populations have relatively Rutaceae, Apiaceae, and Asteraceae ten comprise only one plant genus, restricted diets that are sometimes dif (Compositae), and appear to have and in which speciation events have ferent in different regions (Fox and made switches among the most abun occurred along with host shifts. Con Morrow 1981). Moreover, in many dant plant species with some chemi straints of some kind appear to species of generalist Lepidoptera and cal similarities. One member of the strictly limit the ability of these Hemiptera, an individual may be able group, Papilio zelicaon, shows ma beetles to use many plant species, to feed on different plant species but jor geographic variation in host pref with all species restricted to plants in typically feeds only on one and ap erence. It uses different species of the Asteraceae (Compositae). The pears not to gain from being able to umbellifers in different regions, and genus Ophraella diverged from its mix foods in the way that generalist one population has moved second si ster group less than 8 million years grasshoppers do (Bernays and arily onto citrus. A related and de ago, and the most primitive extant Minkenberg 1997). To a large ex rived species, Papilio oregonius, has species is restricted to one host. The tent, this restriction probably reflects shifted to the common composite, phylogeny of the beetle species is not the fact that in general, the adults are Artemisia dracunculus, which con congruent with that of its hosts. the mobile stages in Lepidoptera and tains chemicals typical of the Moreover, host shifts and speciation Hemiptera. Females of these groups Apiaceae. Such patterns strongly in events have occurred considerably later te nd to lay eggs on plants or plant dicate a potential for species to be than the diversification of the hosts parts that have been carefully chosen come specialists on the most abun (Futuyma and McCafferty 1990). as high-quality substrates for their dant usable host, while retaining In both Yponomeuta moths and relatively immobile young. variation in responsiveness to related Ophraella beetles, therefore, the january 1998 41 tradeoffs may exist. For example, insect feet are sometimes specially adapted to walk effectively on hairy Problems and solutions or waxy leaf surfaces, and such in sects are likely to be less agile on Feeding needs and food-related problems encountered by insect other surfaces (Southwood 1986). herbivores: The potential for morphological • Obtain basic nutrients tradeoffs have been somewhat ne • Obtain high-quality nutrients glected relative to physiological • Eat large amounts of food, especially if low in nitrogen tradeoffs in relation to digestion or • Mix food for nutritional balance detoxification abilities, but it is pos • A void toxicity sible that morphological tradeoffs actually dominate in promoting spe Behavioral solutions to solve food needs and problems in the face of cialization of host use. Physiological danger: tradeoffs have proved difficult to Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 • Decide quickly demonstrate, and some authors have • Use dear, simple cues argued that metabolie adaptability • Feed quickly may make such tradeoffs infrequent • Feed without stopping (Futuyma and Moreno 1988). There • Build shelter is no reason to suppose that physi • Hide feeding damage ological tradeoffs do not occur, how • Move and feed at night ever, and there is no doubt that long • Show behavioral crypsis term specialization on a particular food can restriet an insect's ability to Selectioo press ures 00 physiology and morphology: deal with a variety of plant toxins. • Efficient mouthparts In the evolution and maintenance • Tarsal morphology for attachment and agility of specialization, even when special • High sensitivity to specific host cue(s) food plants become scarce, behav • Attentiveness ioral factors may be more important • Cryptic form than morphology or digestive or • Efficient digestion and detoxification system pharmacological physiology. First, the rigidity of the sensory system and brain may simply prevent expanded host use in some dades of insects. newly acquired plant host may share tionary time, yet with the potential The only option for such insects is a one or more key features of the old to switch to new hosts within the jump to something that is fairly simi one, pro vi ding a bridge that enables plant taxon or to an unrelated plant lar in some critical way, and such some individuals to make the switch, having some presumed character, jumps may well be wh at has hap perhaps when the original host is in such as a plant secondary metabo pened where herbivore species have short supply or is invaded by preda lite, shared with the original host. apparently tracked speciation events tors. In contrast to these groups, the in plant dades. Again, constraints at phylogeny of Phyllobrotica beetles Selection for specialized diets this neural level may reflect the fact is almost exactly congruent with its that small animals, with small brains, hosts in the mint family (Lamiaceae; Specialized diets have often been need to have simple decision rules; Farrell and Mitter 1990). This con considered better options than gen after all, it is safer and more efficient to gruence suggests parallel diversifica eralized diets for insects that are not use dear cues to identify hosts than ti on of the insect and plant taxa, a short of resources, because of the to perceive all possible chemieals and prerequisite for the endless coevolu potential to become particularly try to make a complicated value judg tionary arms race in the strict sense adept at dealing with a specific food ment while remaining vigilant for of Ehrlich and Raven (Figure 5), al type. If so, specialization should re danger (Bernays 1996b). though it is also possible that the duce the ability to deal with alterna The need to avoid predators and beetles simply tracked the evolution tive food types. Morphological ad other natural enemies has an impact of the plants (Farrell et al. 1992). In aptations of mouthparts probably on behavior that is often underesti any case, it is striking that in both result in such tradeoffs with respect mated. However, the need for ex beetles, Ophraella and Phyllabrotica, to feeding on different plant types: treme vigilance constrains the wa y in as in Yponameuta, the shift to a new They allow for the most efficient which host cues are used and the host plant, either related or unre food handling by insects feeding on suite of cues that can be used effec lated, was accompanied by little or their specific food type but poor han tively. Feeding by insect herbivores no increase in diet breadth. None of dling of other food types. Such can increase the risk of predation by the beetles in these genera is polyp ha tradeoffs have even been demon up to 100-fold (Bernays 1996a), and gous. Thus, in so me groups, special strated within species (Carroll and ingestion time must be minimized to ists remain specialists over evolu- Boyd 1992). Other morphologie al reduce this danger. This requirement
42 BioScience Val. 48 Na. 1 must exert strong selection on mor determine the true constraints on tion in the soapberry bug: Natural history phological adaptations for rapid han diet breadth and to place the diverse with the history. Evolution 46: 1052- 1069. dling of food and on behavioral tech approaches to behavioral evolution Chambers P, Sword G, Angel JA, Behmer S, niques for avoiding detection. in a realistic context. Bernays EA. 1996. Foraging by generalist Predation can provide selection for grasshoppers: Two different strategies. Animal Behavior 52: 155-165. host plant choices that provide maxi Acknowledgments mum protection in terms of visual or Cornelius ML, Bernays EA. 1995. The effect of plant chemistry on the acceptability of chemical crypsis, mechanical oppor I wish to thank Reg Chapman for caterpillar prey to a predatory ant tunities for avoidance, or acquisi encouragement and constructive criti Iridomyrmex humilis. Journal of Insect tion of chemical traits that deter cism and the following colleagues who Behavior 8: 579-594. predators. All of these features are read earlier drafts of this article and Dethier VG. 1954. Evolution of feeding pref erences in phytophagous insects. Evolu most efficiently exploited by restrict helped to improve it: Judith Bron tion 8: 33-54. ing the diversity of plant hosts that stein, Laurie Henneman, Michael Dyer L. 1995. Tasty generalists and nasty are used; clearly, the most exact Singer, and Martha Weiss. specialists? Antipredator mechanisms in crypsis can be achieved by using a tropicallepidopteran larvae. Ecology 76: Downloaded from https://academic.oup.com/bioscience/article/48/1/35/322799 by guest on 30 September 2021 single substrate type. In addition, the 1483-1496. References cited Eastop VF. 1978. Evolution of aphid/plant use of physical features of a particular relationships. Pages 157-178 in van Em plant species can be maximized by Bernays EA. 1989. 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