Coevolution and Alternative Hypotheses on Insect/Plant Interactions

Coevolution and Alternative Hypotheses on Insect/Plant InteractionsAuthor(s): John N. ThompsonSource: Ecology, Vol. 69, No. 4 (Aug., 1988), pp. 893-895Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1941238 .

Accessed: 07/09/2014 00:07

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.

http://www.jstor.org

This content downloaded from 62.43.195.66 on Sun, 7 Sep 2014 00:07:50 AMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=esa

http://www.jstor.org/stable/1941238?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


August 1988 SPECIAL FEATURE-INSECT HOST RANGE 893

Ecology, 69(4), 1988, pp. 893-895 (c 1988 by the Ecological Society of America

COEVOLUTION AND ALTERNATIVE HYPOTHESES ON INSECT/PLANT INTERACTIONS

JOHN N. THOMPSON Departments of Botany and Zoology, Washington State University, Pullman, Washington 99164 USA

Ever since the appearance of Ehrlich and Raven's (1964) paper, secondary plant chemistry has enjoyed a sustained emphasis in the literature on the evolution of host range in phytophagous insects. During the past decade, however, other factors have jockeyed for at least place or show, if not the winning position, in the race for relative importance. These contenders include enemy-free space (Lawton and McNeill 1979, Price et al. 1980, 1986, Strong et al. 1984), herbivore lifestyles (e.g., parasitic vs. grazing lifestyles [Price 1980, Thompson 1982, 1983]), and the ecology of host plants (Wiklund 1981, Rowell-Rahier 1984, Strong et al. 1984, Rowell 1985). It has only been in recent years that thorough field studies have been designed to ask how some of these factors compare in their relative importance in determining particular cases of host associa- tion (e.g., Smiley 1978, 1985, Atsatt 1981, Courtney 1981, Rausher 1981, Pierce and Elgar 1985). No studies have examined all these factors together. In some cases the fit between adult oviposition preference and performance of offspring (e.g., growth rates, pupal masses) is quite good, whereas in other cases it is poor, calling for alternative hypotheses (review in Thompson 1988).

CHEMICAL COEVOLUTION

Bernays and Graham (1988) argue that chemical coevolution has been overemphasized in our search for factors determining the evolution of narrow host range. This is undoubtedly true in the sense that other pro- posed factors are not usually studied critically relative to plant chemistry as influences on the evolution of interactions between insects and plants. Recent papers have, in fact, questioned the adequacy of particular versions of chemical coevolution to explain the "clas- sic" cases in which insect radiation has been related to plant chemistry: butterflies on Passifloraceae (Smiley 1985) and lepidopterans on Umbelliferae (Thompson 1986).

Chemical coevolution seems to be a slippery con- cept. There are several ways in which coevolution between species is currently thought to occur (Thompson 1982, 1986), and chemical coevolution between insects and plants has been used by different researchers to apply to different models of coevolution. These models

range from gene-for-gene coevolution to the Ehrlich- Raven hypothesis of chemical escape and species radiation in plants followed by chemical breakthrough and species radiation in insects. In fact, there is no single, current paradigm on the relationship between plant chemistry and insect attack, much less chemical coevolution. Instead, there are several overlapping hypotheses on how plant chemistry affects insect/plant interactions based upon noxious compounds (e.g., Ehr- lich and Raven 1964, Feeny 1976, Rhoades and Cates 1976, Coley et al. 1985) or nutritional compounds important for insect development (e.g., Scriber and Slan- sky 1981). Most specific arguments for chemical coevolution between plants and insects are based upon the role of noxious chemical compounds alone, and these appear to be the kinds of compounds of most concern to Bernays and Graham.

As Bernays and Graham indicate, there is too much lability in many insect/plant interactions to expect that potentially noxious plant compounds are always the primary determinant of narrow host range or that one- to-one chemical coevolution involving these compounds is the norm. In their effort to de-emphasize plant chemistry, however, I think that they create an artificial link between chemical coevolution and narrow host range. They argue that because species-specific coevolution may be uncommon, plant chemistry is probably not the major determinant of narrow host range. This confuses the issue: the influence of plant chemistry upon host range does not depend upon chemical coevolution.

Specifically, Bernays and Graham argue that variation in host use by phytophagous insects and shifts onto introduced plant species imply that insect/plant associations change more often than would be expected if most associations were the product of long-term coevolution. Such lability has been amply demonstrated in a variety of insect taxa (Strong et al. 1984). But it cannot be used, as they use it, for an argument against the importance of plant chemistry as a major factor determining host range. Insects must cope with plant compounds whether or not they coevolve with their host plants, and plant chemistry is one of the axes of selection that will influence host range. Its potential importance in host use is not eliminated in the absence



894 SPECIAL FEATURE-INSECT HOST RANGE Ecology, Vol. 69, No. 4

of an ongoing coevolutionary arms race between plants and insects. Bernays and Graham go on to make sub- sidiary arguments on arms races and harmless deter- rents, but these again are arguments against one-to-one coevolution rather than the importance of plant chemistry.

Their other major argument against chemical coevolution is that insects are generally rare on plants and therefore seldom exert much selection on their hosts. This argument equates commonness of an interaction with intensity of selection. What matters for selection, however, is not commonness per se of an interaction but rather whether attack differs among plant genotypes. As studies in population genetics have shown, even small selection coefficients can have large effects over long periods of time. But again, even if insects did not exert major selection pressures on plant chemistry, it would not eliminate noxious plant compounds as a potentially major determinant of narrow host range. After all, ocean fish are limited to certain salinities and water depths even though they do not coevolve with salt and water pressure. Similarly, lack of selection by insects on plant chemistry does not necessarily imply lack of importance of plant chemistry to host range in insects.

ALTERNATIVE HYPOTHESES

Bernays and Graham go further and argue that generalist predators rather than plant compounds may be "the (italics mine) dominant factor in the evolution of host range." To reach this conclusion, they quickly dismiss several alternative hypotheses before settling on predators, although they acknowledge that physical sites of attachment of insects to plants may be important. They dismiss parasitoids in a sentence by stating simply that these enemies have relatively narrow host ranges themselves and are probably more important in causing host switches or broadening host ranges. It is not at all clear, however, why this is a more likely outcome than a narrowing of host range. They also dismiss the effect of relative host abundances, calling this a prerequisite rather than a cause of narrow host range. But why? Any ecologist that has watched an adult female insect searching for host plants can understand the time constraints that affect ovipositing females (e.g., Singer 1983). Finally, they do not con- sider two other potentially major influences on host range: mode of herbivory (e.g., parasitic insects that complete development on a single plant vs. "grazers" that move between two or more plants during their immature stages (Thompson 1982, 1983), and genetic constraints affecting the relationship between adult preference and larval performance on various hosts (Futuyma and Peterson 1985, Thompson 1988).

By dismissing or ignoring other current hypotheses,

Bernays and Graham gloss too quickly over the rich- ness of the partially overlapping alternatives that we need to explore in order to understand how host range is molded within and between insect populations. The dethroning of plant secondary chemistry has, in fact, become possible because we now have this variety of alternative hypotheses. But dethroning does not mean elimination. Each of these hypotheses needs careful consideration along with plant chemistry (both noxious and nutritional) as we search for patterns in insect/ plant interactions. Rather than argue now for a dominant influence of any one factor, we currently need at least three kinds of studies designed to delineate evolutionary constraints and selection pressures on host range:

1) Detailed field studies showing the ecological determinants of host choice, movement among plants, and survivorship on the range of potential hosts are needed to differentiate among the influences of plant chemistry, enemy-free space (whether from parasitoids or predators), relative plant abundance, competition, and mode of herbivory. Increasingly, studies are designed to test among at least three or more of these influences.

2) Genetic analyses of host preference and larval performance are needed to answer these questions: What is the genetic basis of host preference and specificity? How much genetic variation in host choice oc- curs within populations? (We currently have less than half a dozen studies showing genetic variation in oviposition preference and specificity within natural populations.) How is adult preference for hosts related ge- netically to larval performance on hosts? Questions on the selection pressures influencing host range must come to grips with the problem of how adult choice and larval performance are linked evolutionarily and how such links may place constraints on the evolution of host range (Futuyma and Peterson 1985, Thomas et al. 1987, Thompson 1988).

3) Physiological and biochemical studies of how chemical cues affect host choice and how insects cope with noxious plant compounds are needed to understand how adaptation to one group of chemical compounds expands or constrains the ability of insects to cope with other compounds (e.g., Feeny et al. 1983, Berenbaum et al. 1986, Lindroth et al. 1988).

These are not new topics or questions, but the focus of the questions is getting sharper and the alternative hypotheses are getting clearer. Interactions between insects and plants are perhaps the most diverse associations between taxa in terrestrial communities. Spec- ificity in these interactions is unlikely to have one major cause. The problem now is not to try to designate one factor as the major determinant of host range. Rather it is to understand how the factors interact under dif-



August 1988 SPECIAL FEATURE-INSECT HOST RANGE 895

ferent ecological conditions in the selection pressures and constraints they exert on phytophagous insects.

ACKNOWLEDGMENTS

I thank D. R. Strong for very helpful comments on the manuscript. This work was support by USDA competitive grant 84(86)-CRCR-1-1395.

LITERATURE CITED

Atsatt, P. R. 1981. Ant-dependent food plant selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia (Berlin) 48:60-63.

Berenbaum, M. R., A. R. Zangerl, and J. K. Nitao. 1986. Constraints on chemical coevolution: wild parsnip and the parsnip webworm. Evolution 40:1215-1228.

Bernays, E., and M. Graham. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69: 886-892.

Coley, P. D., J. P. Bryant, and F. S. Chapin, III. 1985. Re- source availability and plant antiherbivore defense. Science 22:895-899.

Courtney, S. P. 1981. Coevolution of pierid butterflies and their cruciferous food plants. III. Anthocharis cardamines (L.) survival, development and oviposition on different hostplants. Oecologia (Berlin) 51:91-96.

Ehrlich, P. R, and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.

Feeny, P. 1976. Plant apparency and chemical defense. Re- cent Advances in Phytochemistry 10: 1-40.

Feeny, P., L. Rosenberry, and M. Carter. 1983. Chemical aspects of oviposition behavior in butterflies. Pages 27-75 in S. Ahmad, editor. Herbivorous insects: host-seeking behavior and mechanisms. Academic Press, New York, New York, USA.

Futuyma, D. J., and S. C. Peterson. 1985. Genetic variation in the use of resources by insects. Annual Review of Ento- mology 30:217-238.

Lawton, J. H., and S. McNeill. 1979. Between the devil and the deep blue sea: on the problem of being a herbivore. Symposia of the British Ecological Society 20:223-244.

Lindroth, R. L., J. M. Scriber, and M. T. S. Hsia. 1988. Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814-822.

Pierce, N. E., and M. A. Elgar. 1985. The influence of ants on host plant selection by Jalmenus evagoras, a myrme- cophilus butterfly. Behavioral Ecology and Sociobiology 16: 209-222.

Price, P. W. 1980. Evolutionarybiologyofparasites. Prince- ton University Press, Princeton, New Jersey, USA.

Price, P. W., C. E. Bouton, P. Gross, B. A. McPheron, J. N. Thompson, and A. E. Weis. 1980. Interactions among three trophic levels: influence of plants on interactions be-

tween insect herbivores and natural enemies. Annual Re- view of Ecology and Systematics 11:41-65.

Price, P. W, M. Westoby, B. Rice, P. R. Atsatt, R. S. Fritz, J. N. Thompson, and K. Mobly. 1986. Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics 17:487-505.

Rausher, M. D. 1981. Host plant selection by Battus phile- nor butterflies: the roles of predation, nutrition, and plant chemistry. Ecological Monographs 51:1-20.

Rhoades, D. F., and R. G. Cates. 1976. Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry 10:168-213.

Rowell, C. H. F. 1985. The feeding biology of a species-rich genus of rainforest grasshoppers (Rhachicreagra, Orthop- terea, Acrididae). II. Foodplant preference and its relation to speciation. Oecologia (Berlin) 68:99-104.

Rowell-Rahier, M. 1984. The food plant preferences of Phratora vitellinae (Coleoptera: Chrysomelidae). A. Field observations. Oecologia (Berlin) 64:369-374.

Scriber, J. M., and F. Slansky. 1981. The nutritional ecology of immature insects. Annual Review of Entomology 26: 183-211.

Singer, M. C. 1983. Determinants of multiple host use by a phytophagous insect population. Evolution 37:389-403.

Smiley, J. T. 1978. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passi- flora. Science 201:745-747.

1985. Are chemical barriers necessary for evolution of butterfly-plant associations. Oecologia (Berlin) 65:580- 583.

Strong, D. R., J. H. Lawton, and R. Southwood. 1984. In- sects on plants: community patterns and mechanisms. Blackwell Scientific, Oxford, England.

Thomas, C. D., D. Ng, M. C. Singer, J. L. B. Mallet, C. Parmesan, and H. L. Billington. 1987. Incorporation of a European weed into the diet of a North American herbivore. Evolution 41:892-901.

Thompson, J. N. 1982. Interaction and coevolution. John Wiley and Sons, New York, New York, USA.

1983. Selection pressures on phytophagous insects on small host plants. Oikos 40:438-444.

1986. Patterns in coevolution. Pages 119-143 in A. R. Stone and D. L. Hawksworth, editors. Patterns in coevolution. Clarendon, Oxford, England.

1988. Evolutionary ecology of the relationship between oviposition preference and immature performance in phytophagous insects. Entomologia Experimentalis et Applicata, in press.

Wiklund, C. 1981. Generalist vs. specialist oviposition be- haviour in Papilio machaon (Lepidoptera) and functional aspects on the hierarchy of oviposition preferences. Oikos 36: 163-170.



Documents

Coevolution and Alternative Hypotheses on Insect/Plant Interactions