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Evolution of Feeding Behavior in Insect Herbivores

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Evolution of Feeding Behavior in Insect Herbivores 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
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