Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects

Entomol. exp. appl. 47: 3-14, 1988 �9 Kluwer Academic Publishers, Dordrecht - Printed in the Netherlands 3

Mini-review

Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects

John N. Thompson Departments of Botany and Zoology,

Accepted: November 10, 1987

Washington State University, Pullman, WA 99164, USA

Key words: Growth, host selection, oviposition preference, Papilio, life history covariance

Abstract

The relationship between oviposition preference and growth, survival, and reproduction of offspring is the crux of the problem in the evolution of host associations between phytophagous insects and plants. Observed relationships between oviposition preference and performance of offspring range from good to poor. At least four hypotheses have been suggested to explain observed use of particular host plants that may not result in the fastest growth rates or greatest pupal masses: time, patch dynamics, parasite versus grazer lifestyles, and enemy-free space. Our current understanding of these relationships, however, is hampered by an almost complete lack of data on how preference and performance are related genetically. These data are needed to understand the origins of covariance between preference and performance and constraints on the evolution of host associations.

Introduction

The relationship between preference of ovipositing females for certain plant species and growth, survival, and reproduction of offspring on those plants (hereafter, performance) has been a central problem in the theory of insect/plant interactions. This preference/performance problem has played an important role in studies and debates over the evolution of host specificity (e.g., Wiklund, 1975; Bush & Diehl, 1982; Futuyma & Peterson, 1985; Thompson, 1986a), selection for enemy-free space (e.g., Lawton & McNeill, 1979; Price et al., 1980; Atsatt, 1981a, b), and host shifts in allopatric and sympatric insect populations (e.g., Bush, 1975a, b; Futuyma & Mayer, 1980; Jaenike, 1980, 1981; Wood & Guttman, 1983; Rausher, 1984b). The relationship between these adult and immature characteristics influences how shifts onto new hosts occur and, therefore, how insect species come to be distributed among plant species over evolutionary time.

Consequently, the relationship between oviposition preference and offspring performance is the crux of the problem of the evolutionary ecology of host association in insect/plant interactions. Nonetheless, our current understanding of the preference/performance problem is very preliminary, pieced together from studies of geographic variation in host use, a few studies of phenotypic or genetic variation within populations in preference or performance, and even fewer studies on selection to modify these characters. The results of these few studies, however, suggest hypotheses on how the relationship between preference and performance can vary under different ecological conditions and selection pressures.

In this paper I consider the following questions on the relationship between oviposition preference and the performance of immature insects on their hostplants: (1) What is the range of the observed phenotypic relationships between preference and performance; (2) How are these characters related genetically; and (3) What are

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the causes of variable relationships between preference and performance? The discussion is restricted to preference and performance of insects on different plant species, although these questions also apply to the use of plant parts and habitats.

Preference, specificity, and performance

The words preference, specificity, and performance have a number of meanings in the literature on insect/plant interactions (reviews in Miller & Strickler, 1984; Singer, 1986). The uses of these words depend somewhat on the questions asked and behavioral assays used. Here I will use oviposition preference as the hierarchical order- ing of plant species by ovipositing females. In a choice trial in which plants of equal mass of several species are offered simultaneously, preference would be expressed as the proportion of eggs laid on each of the plant species (e.g., Stanton, 1979; Wiklund, 1975; Thompson, 1986b). Preference cannot be determined in the field from a simple count of the proportion of eggs found on various plant species, since such counts can be the result of oviposition by more than one female and not all plants will be of equal abundance and availability (Stanton, 1982; ~hman, 1985). Specificity in simultaneous trials can be defined as the number of plant species on which females oviposit. That is, given a preference hierarchy, does an individual female in a simultaneous choice trial restrict her oviposition to the most preferred plant species, or to the top two species, or to the top three? Using sequential trials in which plant species are offered one at a time, Singer (1982) uses specificity as the length of time over which a female refuses all hosts except one.

Performance is used here as a composite term for survival at all immature stages (egg, larval, pupal), larval growth rate, efficiency as indicated by nutritional indices (Waldbauer, 1968; Scriber & Slansky, 1981), pupal mass, and resultant adult fecundity and longevity. The problem in assessing performance is that the components are not always positively correlated, so different criteria of performance could give different results in evaluating the relationship between oviposition preference and performance of offspring. Liriomyza sativae larvae grown on cowpea (Vigna unguiculata) show a genetic correlation between development time and pupal mass, but no such correlation is evident when the larvae are reared on tomato (Via, 1984a, b). In Deloyala guttata beetles larval survival and pupal mass are positively correlated across hosts but development time is not (Rausher, 1984a).

Performance may not even be correlated among larval instars within a population. In Papilio cresphontes, growth in the final instar on different hosts does not always follow the same pattern as growth in the penultimate instar (Scriber, 1983). So partial analyses of performance (e.g., growth from first instar to some arbitrary age prior to pupation) are of little use, except perhaps to show genetic differences between populations that are expressed at particular developmental stages.

An additional complication is that the causes of good or poor performance on a plant species in natural or managed communities need not result directly from interactions between an insect and a plant. Consistently poor performance on a particular plant species could result from interactions with competitors or enemies at other trophic levels (Price et al., 1980), interactions with mutualists (Atsatt, 1981a, b), or abiotic differences (e.g., temperature, sunlight) in the microhabitats in which the plant species grow. Consequently, analyses of performance made in a laboratory need to be supplemented by similar analyses done in the field in the presence of potential competitors, predators, parasitoids, and mutualists.

Observed relationships between preference and performance

Almost all conceivable relationships between oviposition preference and various components of performance of offspring on different plant species have been observed, except the extreme in which females always oviposit on a host that is fatal to the immatures. Observed relationships range from good correspondence between adult

preference and some components of larval performance (e.g., Singer, 1972, 1983; Rausher, 1982) to poor correspondence (e.g., Courtney, 1981, 1982). In some cases poor correspondence between preference and performance may result from oviposition onto introduced host plants (e.g., Chew, 1977; Legg et al., 1986) or relative rarity of the preferred host (e.g., Williams, 1983).

Part of the problem is to understand how local patterns of preference and performance fit within broader geographic patterns. Swallowtail butterflies in the genus Papilio are proving to be useful taxa for studying geographic patterns in preference and performance and the expression of preference within populations. Papilio machaon, the Old World Swallowtail, has a circumboreal distribution and varies in the plant species that are used as hosts. In Fennoscandia, P. machaon has been found on 21 plant species in the Umbelliferae and Rutaceae but varies between populations in which species and how many species are used as hosts (Wiklund, 1974, 1982). Larvae are capable of surviving and growing on a broader range of plant species than are used by ovipositing females (Wiklund, 1973, 1975). In North America, P. machaon is considered either one species or a small group of closely related species or subspecies. In Alaska and Canada females oviposit on Artemisia arctica in the Compositae and perhaps on some Umbelliferae. Farther south, in the Intermountain West of the United States, the populations are generally called P. oregonius and they oviposit exclusively on Artemisia dracunculus (Thompson, 1988).

These populations in the Intermountain West occur sympatrically or parapatrically with several other species in the P machaon group, all of which feed upon umbelliferous species. When P. oregonius females are offered A. dracunculus and several umbelliferous species that are the common hosts of the other local species in the P. machaon group, they invariably oviposit almost exclusively on their normal host (Thompson, 1988). Nonetheless, preliminary trials indicate that larval growth on some umbelliferous hosts is high, and in some cases development may be as fast as on the normal host (Thompson, unpublished data).

Similarly, Papilio zelicaon varies geographically in its use of plant species. In eastern Washington and north- eastern Oregon, populations oviposit and feed primarily on Lomatium grayi and Cymopterus terebinthinus (Thompson, 1988). In western Washington, however, some populations now oviposit and feed exclusively on fennel (Foeniculum vulgare), which was introduced 100 to 200 years ago. Along the Pacific coast of Washington at least one population oviposits and feeds exclusively on Angelica lucida. Farther south, some populations have shifted onto oranges (Citrus sinensis) or, again, onto fennel (Emmel & Shields, 1978; Masuda, 1981). De- spite these shifts in patterns of host use, some populations so far tested still include individuals that prefer L. grayi and C. terebinthinus over their local hosts when these plants are offered in simultaneous choice trails (Thompson, unpublished data).

Although the relationships between preference and performance are still incompletely known, the tests com- pleted so far in Sweden and North America on these Papilio species suggest several patterns. First, there is a hierarchical arrangement of preference in these species (Wiklund, 1975, 1981; Thompson, 1988), and progress has recently been made in identifying the plant compounds used as oviposition cues in one of the species in this group, Papilio polyxenes (Feeny et al., 1983). Second, within a species the preferred hostplants may not always vary geographically, but the actual hosts used may vary. As Wiklund (1981) showed for P. machaon, if the most preferred hosts are not available, then females use hosts lower down the hierarchy. Third, larval survival and growth rates on host species correspond partially but not completely with oviposition preference, and the discrepancy is of two kinds: females oviposit on some hosts that are relatively poor for larval survival, and females do not oviposit on some hosts that are adequate for larval survival. Finally, in the species tested so far, the range of hostplants acceptable for larval growth is generally broader than the range of hosts used locally by ovipositing females.

As in Papilio, populations of the checkerspot butterflies show geographic variation in use of plant species (Singer, 1971, 1972; Ehrlich et al., 1975; Bowers, 1986). Populations of both Euphydryas editha and E. chalcedona differ in survival and growth of larvae on the various potential host species (Rausher, 1982; Bowers, 1986). There is also phenotypic variability in oviposition preference within populations, and the genetic basis of differ-

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ences in preference are now being analyzed (Thomas et al., 1987; Singer, pers. comm.). Using sequential trials in which plants were presented one at a time to females caught in the field, Singer (1983) showed that females differed within populations in how they ranked plant species.

Genetic covariance in preference and performance

As has been emphasized repeatedly in the literature of the past decade, our understanding of the relationship between oviposition preference and performance of offspring is hampered by an almost complete lack of understanding of how preference and performance are determined and related genetically (Wiklund, 1975; Futuyma & Mayer, 1980; Bush & Diehl, 1982; Gould, 1983; Jaenike & Grimaldi, 1983; Scriber, 1983; Rausher, 1984a; Futuyma & Peterson, 1985). Variation among individuals in host selection or performance on different hosts has been demonstrated within and between populations (e.g., Fox & Morrow, 1981; Tabashnik et al., 1981; Wik- lund, 1981; Tavormina, 1982; Papaj & Rausher, 1983; Singer, 1983; Stanton & Cook, 1983). Some differences between populations have been shown to be genetically determined (e.g., Hsiao, 1978; Tabashnik, ~ 1983; Thind & Muggleton, 1981; Rausher, 1982; Scriber, 1982; Bowers, 1986; Thomas et al., 1987). Nonetheless, only a few studies have demonstrated a genetic basis for within-population variation in oviposition preference (e.g., Jaenike & Grimialde, 1983; Thompson, 1988) or performance (e.g., Gallun et al., 1961; Gould, 1979; Pathak & Heinrichs, 1982; Tabashnik, 1983; Rausher, 1984a; Hare & Kennedy, 1986). Moreover, nearly nothing is known about how these aspects of host use covary genetically (Via, 1986).

Consequently, the wide variety of hypotheses that have been suggested on how loci for preference and performance may be linked, how they might covary, and how they contribute to host shifts remain mostly untested. Some verbal and mathematical models of preference and performance assume that these characters are inherit- ed on separate loci. Bush (1975a, b) has argued that shifts onto new hosts, especially sympatic shifts, may involve separate loci affecting host recognition and offspring survival. More recently, Bush and Diehl (1982) suggested that different patterns of linage between oviposition preference and larval survival genes may influence the evolution of monophagy, oligophagy, and polyphagy. Based upon this work with Papilio machaon, Wiklund (1975) concluded that oviposition preference and larval performance are controlled by separate loci, and that over evolutionary time the range of plants suitable for larval growth should come to be wider than the range of plants on which an average female oviposits.

Analyses of divergent populations have shown that preference and performance can vary either together (e.g., Tavormina, 1982) or independently (e.g., Thomas et al., 1987). Some populations of Coliasphi lodice in western United States have shifted completely from native legumes to alfalfa in areas where alfalfa is now abundant. Populations that feed upon native legumes do not differ from alfalfa-feeding populations in oviposition preference but do differ in larval performance. Alfalfa-feeding populations now do better on alfalfa than on native legumes, whereas populations that feed on native legumes do better on those hosts than on alfalfa (Tabashnik, 1983). In contrast, selection experiments on Callosobruchus maculatus, designed to alter oviposition preference and performance on two legumes, showed after 11 generations of selection no evolution of performance (Wasserman & Futuyma, 1981). But the experiments did result in changes in the number of eggs that females laid on the different legume species. The analyses, however, were made at the population level (that is, number of eggs laid by groups of females), so it is difficult to determine how the evolution of the components of this complex result is partitioned among individuals within populations. For the special case in which the larval stages disperse and choose the host plants, Futuyma et al. (1984) showed divergence in larval preference but not larval performance on difference hosts.

If genetic covariance does occur between preference and performance, it could result either from linkage disequilibrium between alleles at the loci affecting these characters or from pleiotropy (Lande, 1980; Futuyma & Peterson, 1985; Via, 1986). These effects have not been separated in models of the relationship between prefer-

ence and performance, and the effects are currently difficult to distinguish experimentally since so little is known about the genetics of these characters.

The other problem in analyzing the genetics of these characters is that most published studies have been designed to ask how these two components of host use are related at the population level rather than at the individual level. That is, studies have generally been designed to ask whether most eggs within the population are found on plant species on which offspring generally do best; the studies do not ask how oviposition preference in an individual female is related to performance of her offspring on the host she chose as compared with other hosts (e.g., Knerer & Atwood, 1973; Courtney, 1981; Rausher, 1982). These population-level studies have been important in testing whether factors other than larval growth rates and pupal masses can contribute to selection for oviposition preference (e.g., Smiley, 1978; Price et al., 1980; Atsatt, 1981a, b; Courtney, 1981; Rausher, 1981; Singer, 1983, 1984; Williams, 1983). As Via (1986) recently emphasized, however, the evolutionary problem is now to understand how different genes for preference and performance are distributed among individuals, not as population averages.

Via found, in an analysis of several populations of Liriomyza sativae (insects collected from different fields with different crop species), that females preferred to oviposit on the hosts on which they achieved highest pupal masses. This relationship was apparent only at the level of individuals. Analyses based upon population averages showed neither preference for nor better growth on one of the plant species. Via was unable, however, to extend her analysis to test how larvae of host-specific females performed on different plant species because females insert their eggs into the plant tissues such that they can not be readily moved between plants. Also, since the analyses combined fields she could not determine whether the variation in preference and performance occurred within fields or between fields. Nonetheless, this kind of direct study of genetic covariance of these characters is crucially needed for a variety of phytophagous insect taxa with different life histories and feeding modes, especially if it can be combined with transplants of eggs between plants.

Another needed approach to understanding the genetics of preference and performance is through localiza- tion of genes for these characters onto particular chromosomes. Analyses of the Papilio machaon group over the past several years have indicated that significant genetic control of oviposition preference in these species is located on one chromosone but is modified by one or more genes on other chromosomes (Thompson, unpublished). This is the first insect taxon for which genes for oviposition preference have been localized to a particular chromosome, and-it provides the opportunity to now ask if performance genes are localized on the same chromosome.

Selection pressures on preference/performance relationships

Some aspects of the relationship between preference and performance may be a simple consequence of how these characters are related genetically. Only detailed breeding studies and quantitative genetic studies will pro- vide these answers. A strong relationship, however, between preference and performance may be decreased or prevented by the ecological conditions affecting populations. At least four general hypotheses on selection pressures have been proposed to explain existing patterns of preference and performance, including poor relationship between preference and some components of offspring performance. Several of these factors could easily act simultaneously to shape host use by an insect species.

The time hypothesis. When novel plant species are offered to insects or are newly added to a community, females may sometimes lay eggs on these plants even though the plants are relatively unsuitable or even fatal to larvae or nymphs (Wiklund, 1975; Chew, 1977; Legg et al., 1986). Selection may take many generations either to reduce the tendency of females to oviposit on these plant species or to increase the ability of larvae to survive and grow on them. Pier& napi females in the Rocky Mountains of Colorado oviposit on seven crucifer species,

including two introduced species that have glucosinolate profiles similar to the indigenous hosts but are fatal to larvae, Chorispora tenella and Thlaspi arvense (Chew, 1977; Rodman & Chew, 1980). These two plant species have probably now been in these communities for several decades or more. Consequently, some cases of poor correspondence of oviposition preference and larval performance may reflect simply the lack of time to modify preference or performance. Such instances should become more common as we continue to dismantle natural communities and replace them with a mixture of introduced species.

Furthermore, the rate of evolution may differ between preference and performance. Futuyma (1983) argued that preference for a new host may evolve before performance if an insect population is presented with a relatively abundant novel host. One population of Euphydryas editha in California has evolved in preference toward a plant species introduced about 100 years ago, Plantago lanceolata, but larval performance has not changed from other populations (Thomas et al., 1987).

Patch dynamics hypothesis. Geographic variation in host use sometimes follows geographic variation in the relative abundance of potential hosts (e.g., Wiklund, 1981; Rowell-Rahier, 1984a, b). These patterns may be due to genetic differences in preference between populations or simply to the relative availability of plant species. In coastal California, Euphydryas chalcedona butterflies prefer to oviposit on and grow better on Scrophularia california than on the more abundant and persistent shrub, Diplacus aurantiacus (Williams, 1983; Williams et al., 1983). Nonetheless, D. aurantiacus is the more commonly used host, because ovipositing females encounter it much more often than the preferred host.

Relative abundances of many plants, however, are often not static, and neither is the structure of the plant populations. Landscapes are a mosaic of patches differing in age since the last major disturbance (e.g., fire). Hence, the structure of plant populations is also a continually changing mosaic. As plant communities change in species composition and populations change in age structure and size structure, the interactions with insects also change. The probability of encounter with particular plant species may increase or decrease, and the mechanics and outcomes of interactions may change. Plants of different ages or sizes differ in the parts available (e.g., flowers), the mix and concentrations of secondary compounds, and the physical properties of tissues. The result is a 'patch dynamics of interactions' that both follows and may influence the patch dynamics of species (Thompson, 1982, 1985).

As a consequence of patch dynamics, a plant species that is best for larval development at one stage in local succession of a plant community may be rare or less suitable for larval growth or survivorship at other stages in local succession. Under these conditions natural selection may not consistently favor use of any one particular plant species, which could preempt directional selection for a strong relationship between preference and performance (Thompson, 1986b). In fact, preference and performance tests in some insects can vary in outcome depending upon the ages, sizes, and reproductive states of plants, and the nutrient conditions in which the plants were grown. Changes in water availability and nutrient mixes in soils can potentially alter the suitability of plants for insect growth (Scriber, 1984; White, 1984), and ovipositing females of some insect species can differentiate among plants that have been subject to different fertilization regimes (Myers, 1985).

The variations in plant population structure and community composition could result in poor correspondence between preference and performance with respect to the current relative abundances of plant species. Adult preferences that vary with previous adult exposure to host species (Jaenike, 1982; Prokopy et al., 1982; Papaj, 1986) could potentially even be an evolutionary result of natural selection in environments in which host availability varies among insect generations.

Theparasite/grazer hypothesis. There are some essential differences between phytophagous insects that routine- ly complete development on a single plant individual (parasites) and those that must move between two or more plant individuals during the course of larval development (grazers) (Thompson, 1982). If an individual plant is sometimes too small for a larva to complete development, then selection could favor either pupation

at a small size or grazer-like behavior (Thompson, 1983a). Grazer-like behavior is found in insects that feed on small plants in grasslands, steppes, deserts, tundras, and forest understories. It is also found in insects with high mobility that allows easy movement between plants (e.g., some grasshopper species), and in insects that feed on large plants but experience irruption in their populations (e.g., gypsy moths, Lymantria dispar). If selection favors grazer-like behavior, it may also favor the ability of larvae to grow on several plant species. The converse may also be true: the ability of larvae to survive on several plant species available in a community may make the evolution of grazer-like behavior more likely.

Whatever the evolutionary origin of the use of two or more plant individuals during the course of larval or nymphal development, such movements could affect selection on preference and performance. Natural selection could favor oviposition on the plant species that is best for egg survivorship and development of early instars, although survivorship and development in later instars is better on other plant species. During the later instars, the larvae may move to those other plant species. Or, females may show no preference among several plant species if there is no host that is always best for early larval development and if the combination of plant species available to larvae is unpredictable as they move between plants. At the extreme, adult females of some insect species with grazing larvae may not even lay eggs on the larval host plant. Some butterflies that use herbaceous hosts and overwinter as eggs, and some satyrids that feed on abundant grasses, lay their eggs near but not on a host plant and larvae must search for the host (Wiklund, 1984). Of 12 satyrid species studied by Wiklund (1984) in Sweden, only 3 always deposit their eggs on the plant individuals fed upon by larvae after eclosion.

There are three additional complications that come with a grazing habit, especially in insect species that can move often between plants during development such as some grasshoppers. First, preferences for plant species can be expressed both in adults and immatures, unlike insec.ts that finish development on a single plant. Hence, there is the potential for selection on preference to act differently in adults and immatures. Grazing insects do show preference in immature stages, and these preferences may vary genetically with the relative abundance of plant species. Grasshoppers in the genus Rhachicreagra differ in the plant species they choose in 2-way choice tests, and these differences partly correspond to the relative abundance of plant species found in their native habitats (Rowell, 1985).

Second, in insect species that are phytophagous (excluding nectarivorous) as both immatures and adults, the relationship between oviposition preference and immature performance could be complicated by adult feeding preference and performance on different hosts. Since components of performance are not always correlated among instars, immature and adult performance on different hosts may not always be correlated. Consequent- ly, the relationship between oviposition preference and immature performance may differ between, for example, Lepidoptera, in which adult food differs from larval food, and Orthoptera and some Coleoptera, in which adult and larval food may not differ.

Third, natural selection on grazing insects could favor mixed-species diets, which would make nonsense of performance results based upon single-species diets. Diet-mixing in which individuals actively choose two or more plant species while foraging has been observed in a variety of herbivorous animal taxa (review in Thomp- son, 1982) and the effects on growth and survival can be large. For example, when Melanoplus bivittatus grasshoppers were fed only on Descurainia sophia from first instar to adult at a rearing temperature of 21 ~ only 40% of individuals survived. When fed on Thlaspi arvense, none survived past the fourth instar. But when nymphs were fed on a mixed diet of these two crucifer species, 90% survived. Increases in survivorship were also observed in other mixed-species/single-species comparisons (MacFarlane & Thorsteinson, 1980).

Therefore, there may be less of a hierarchy in oviposition preference in some grazer-like insects than in related species that finish development on a single plant individual and there may be less of a strong genetic link between preference and performance on single plant species than in parasitic species. Both the unpredictability of which plant species will be encountered as larvae or nymphs move between plants and the potential for selection for mixed-species diets may decrease selection for a strong preference hierarchy during oviposition.

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Selection for mixed diets may also extend to the use of different plant parts. Plant parts can differ in nutritional quality, secondary compounds, physical characteristics, protection from an insect's enemies, and availability to an insect's mutualists (e.g., Price et al., 1980; Berenbaum, 1981; Thompson, 1983b, c). The selective use of plant parts presents questions additional to those usually considered in studies on the use of plant species by insects. As in other animals, selection may favor a mixed diet in insects that can take advantage of foods that differ nutritionally (Thompson, 1982, 1983a). An insect that mines leaves or bores into stems or seeds may not be able to choose among plant parts, but a caterpillar that can easily move between flower parts and leaves could make such choices. Preliminary studies of corn earworm larvae (Heliothis zea), for example, have shown that these larvae can select an optimal nutrient mix when offered artificial diets (Waldbauer et al., 1984). Conse- quently, performance tests on plant species must be based upon an understanding of the pattern of use of plant parts by the insects, and analyses of preference and performance on plant parts require an understanding of whether diet-mixing of plant parts is a normal feeding tactic in that species.

Enemy-freespace hypothesis. Performance on plant species may be influenced as much by enemies - including predators, parasitoids, and competitors - as by plant characteristics. Consequently, the ranking of performance based upon survivorship and growth in the absence of an insect's enemies can differ from the ranking in the presence of enemies. Natural selection for use of host plants may therefore be based partly on 'enemy-free space' (Lawton & McNeill, 1979; Price et al., 1980, 1986). For example, many lycaenid butterfly larvae are tended by ants that may protect the larvae from enemies. Ovipositing females of Ogyris amaryllis oviposit on the nutritionally inferior host Amyema maidenff with ants rather then on the nutritionally superior A. preisii without ants (Atsatt, 1981a). Similar choice of hostplants based upon presence of ants has been shown for other lycaenid species (Pierce & Elgar, 1985) and avoidance of hosts because of risk from parasitism or predation has been suggested for other insect species (e.g., Singer, 1971, 1972; Smiley, 1978; Price et al., 1980). Gilbert (1979) refers to this as 'ecological monophagy' to separate it from cases of monophagy due to nutritional differences between plant species.

Concluding remarks

All these hypotheses on selection pressures affecting preference and performance suggest that evaluations for particular species must ultimately be made in the field. Laboratory studies can show the relationship between preference and performance relative to nutrition of immatures. But evaluation of the patch dynamics hypothesis and the enemy-free space hypothesis require analyses in natural populations. Furthermore, analyses of free- ranging insects are necessary for evaluation of parasite as compared to grazer lifestyles and use of mixed diets. No study has evaluated all four hypotheses for a single insect species. The availability of these multiple hypotheses should allow for more efficient experimental designs on these problems in the next decade. And new studies will undoubtedly suggest additional hypotheses.

The ecological and physiological work on preference and performance must also go hand-in-hand with studies of genetics in order to understand the evolution of insect/plant interactions. The genetic relationships between preference and performance may place evolutionary constraints on how these characteristics can covary. Moreover, genetic studies are needed to determine whether the use of several host plants within insect populations is due to genetic polymorphism or to a similar pattern of use of several hosts by all individuals (Fox & Morrow, 1981; Futuyma & Peterson, 1985).

Once genetic strains that differ in preference or performance can be established either within or between populations, work on the ecological and physiological questions can proceed much more efficiently. An understanding of the basic genetics will allow more efficient evaluations of reaction norms, that is the range of phenotypic expression of genotypes across environments. In the case ofMelanoplus bivittatus, individuals fed mixed-

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species diets generally had higher survivorship than individuals fed single-species diets, but the effect of mixed- diets on survivorship differed with the temperature at which the experiments were run (MacFarlane & Thor- steinson, 1980). As insect and plant genotypes are expressed differently in different physical or biotic environments, natural selection could differ in how it acts on interactions. These 'interaction norms', the reaction norms of species interactions, are the raw material for the evolution of interactions (Thompson, 1986a) and can indicate how genetics, ecology, and physiology of preference and performance are related in causing divergence in insect/plant interactions in different environments.

Acknowledgments

I thank the editors for asking me to write this review, and I am grateful to Stephen P. Courtney, L. M. Schoon- hoven, Michael C. Singer, Christer Wiklund, and two anonymous reviews for discussion or helpful comments on the manuscript. This work was supported by USDA grant 84(86)-CRCR-1-1395 and NSF grant BSR8705394.

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Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects