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Variation in Interspecific Interactions Author(s): John N. Thompson Source: Annual Review of Ecology and Systematics, Vol. 19 (1988), pp. 65-87 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/2097148 . Accessed: 01/09/2014 10:52 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 of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology and Systematics. http://www.jstor.org This content downloaded from 213.103.193.105 on Mon, 1 Sep 2014 10:52:24 AM All use subject to JSTOR Terms and Conditions

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Page 1: Variation in Interspecific Interactions

Variation in Interspecific InteractionsAuthor(s): John N. ThompsonSource: Annual Review of Ecology and Systematics, Vol. 19 (1988), pp. 65-87Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097148 .

Accessed: 01/09/2014 10:52

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].

.

Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review ofEcology and Systematics.

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Page 2: Variation in Interspecific Interactions

Ann. Rev. Ecol. Syst. 1988. 19:65-87 Copyright ? 1988 by Annual Reviews Inc. All rights reserved

VARIATION IN INTERSPECIFIC INTERACTIONS

John N. Thompson

Departments of Botany and Zoology, Washington State University, Pullman, Wash- ington 99164

INTRODUCTION

The study of evolving interactions between species has progressed from descriptions of adaptations and counteradaptations to a search for patterns and constraints affecting the evolution of interactions and the conditions favoring coevolution. This search for patterns and constraints requires a populational approach to species interactions. It is not enough to understand in a typologi- cal way that one species has a particular trait, another species has a particular counter-trait, and that the interaction of the two species can be described in general terms as antagonism, commensalism, or mutualism. Individuals vary in their expression of traits, populations vary in their structure, and, as a consequence, interactions vary in their outcomes.

Just as variation in traits in populations is the raw material for the evolution of species, variation in outcome is the raw material for the evolution of interactions. Nonetheless, only in recent years has the analysis of variation in the outcome of interactions become a focus of evolutionary research. A glance through the major evolution journals from two decades ago would show few papers confronting the problem of how interspecific interactions can vary in outcome and how this variation can affect the evolution of interactions (e.g. 38, 93, 111). Not until the mid 1970s did any text in ecology include chapters on the evolution of species interactions (e.g. 108, 120, 124). And not until the appearance of Futuyma's book in 1979 (46) did any major textbook in evolution include a chapter on coevolution or the evolution of interactions. The first book devoted to issues on coevolution of animals and plants did not appear until 1975 (53), and the first books devoted to the general problem of coevolution did not appear until 1982 and 1983 (49, 98, 149).

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In this paper I review the kinds of analyses that provide the raw material for understanding how interspecific interactions evolve under different ecological conditions. The review focuses on variation in the outcome of interactions at the level of the individual, rather than the effects of interactions on the dynamics of populations. In writing the review, I generally avoided covering the same ground as two previous reviews that focused on the ways in which two-species interactions are affected by interactions with a third trophic level (112) or parasites (113). The studies I consider here are divided broadly into two kinds: (a) those showing distributions of outcome within populations (distributed outcomes) because of variation in age or size of individuals, density, size, and subdivision of populations, or distribution of genotypes; and (b) those showing variation in outcome across environmental gradients (interaction norms). These terms, and their use in the study of evolving interactions, are developed below.

TYPOLOGICAL VERSUS POPULATIONAL APPROACHES

The traditional classifications of interactions as (-,-), (+,-), (+,O), etc mask the kinds of information needed to understand the evolution of in- teractions. These classifications lump together interactions that can differ fundamentally in the mechanisms that produce the outcomes; both predator/ prey interactions and Batesian mimicry, for example, are classified as (+ ,-) interactions (1). Moreover, this typological approach to thinking about in- teractions ignores the variation in outcome that is central to the study of evolving interactions.

For example, ground-foraging beetles attack Lomatium dissectum seeds after the seeds are dispersed by wind. These beetles, however, do not kill all the seeds they attack. Lomatium seeds are flat and have a prominent wing. Both in the field and in the laboratory, the beetles consistently eat only the wings of seeds from some L. dissectium plants within a population, whereas they consistently chew past the wings and into the endosperm and embryo of seeds from other plants within the population. Consequently, the interaction varies from predation to commensalism within a population, with subgroups of plants consistently experiencing different outcomes (150). No simple typological label can accurately describe the interaction. An understanding of the ecological dynamics of the interaction and the potential effect of the beetles on plant genotypes (if the differences in seeds are genetically de- termined) requires an understanding of the distribution of outcomes. The mean outcome provides little information, for the outcome differs among the subgroups within the plant population.

A second problem with typological descriptions arises in mutualistic in-

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teractions. Few if any mutualistic interactions impose no costs on the interact- ing species. Many mutualisms probably derive evolutionarily from antagonis- tic interactions (149), and the antagonistic components of the interactions often remain as costs of the mutualism, as in the ovules killed by larvae of pollinating fig wasps (71) and yucca moths (2). Within a population, the cost/benefit ratio is likely to vary, and it is precisely this variation that provides the information important to understanding how slight shifts in life histories, age, sizes, morphologies, and physiologies can affect interactions. To describe simply the mean outcome of an interaction or to describe the benefits without an analysis of the costs is to lose the information fundamental for studying the evolution of the interaction.

A third problem in typological descriptions occurs in interactions that involve several components of life histories. Some species may be mutualistic for some aspects of their life histories while being antagonistic for others. By forming Mullerian mimicry complexes, adult Heliconius butterflies are mutualistic for avoidance of enemies, but compete for adult nectar sources. Consequently, as Templeton & Gilbert (146) argued, it is misleading to describe these interactions as having some net outcome and meaningless to argue that one of these kinds of interactions can outweigh the other. Both kinds of interaction occur within these populations, and they must both be considered in evaluating the evolution of these interactions. Coevolution of the mutualistic traits can affect coevolution of the competitive traits, and vice versa.

A fourth problem is that all populations have age or size structure, which can affect the outcomes of interactions. Therefore, an analysis of the mean outcome of an interaction on a random sample of individuals masks the variation in outcome that can depend upon age or size. Furthermore, a random sample probably provides a mean estimate that most closely applies to young or small individuals, since they will be the largest group in any random sample of a stable or growing population.

Finally, both the mean and the distribution of outcomes in an interaction can vary among environments. Some mycorrhizal associations, for example, can be mostly mutualistic on infertile soil but antagonistic on more fertile soil, depressing the growth rate of the host plant (18). Therefore, the outcomes of interactions may be environment-specific. The study of plasticity in outcomes is as important to understanding the evolution of interactions as the study of plasticity in morphology, physiology, and life histories is to an understanding of the evolution of species.

The first four of these problems with typological descriptions of in- teractions concern disttibutions of outcomes within populations, and the fifth relates to variation in the distributions among environments or across gra- dients. The study of the evolution of interactions will increasingly demand

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analyses of the distributions of outcomes both within and among environ- ments. This is hardly a new idea. Nonetheless, the analysis of the distribu- tions of outcomes-rather than simply a mean outcome or a mean cost/benefit analysis-has not yet become a standard part of studies on the evolution of interactions.

DISTRIBUTED OUTCOMES

Many, perhaps most, interactions between populations vary with age, size, or genotype of the interacting individuals. Roughgarden & Diamond (126) argued that population models of species interactions will need to be im- proved by subdividing populations into groups within which the interactions are on average similar. They referred to such models as distributed in- teractions.

We can think of distributed interactions as having two components: distrib- uted probabilities and distributed outcomes. Individuals differing in age, size, or genotype may differ in their probabilities of encountering another species, and mathematical models of distributed probabilities of encounter based upon age (101) or size (156) are beginning to appear. Similarly, outcomes can vary among ages, sizes, and genotypes, and the following sections focus on these distributed outcomes.

Age-Dependent Outcomes Ontogenetic changes in susceptibility to diseases are common in animals (3, 40, 145) and plants (23). Some viral infections such as viral hepatitis and poliomyelitis in humans may sometimes produce no symptoms or only mild symptoms if infection occurs in early childhood but may produce more symptomatic and even severe disease if infection first occurs at a later age (41, 91). Maternal antibodies apparently confer protection against some diseases such as measles and parainfluenza viruses in infants up to 4-6 months of age, after which the incidence of these diseases increases (15, 56).

In plants, the effects of herbivory or survivorship can vary with plant age. In two grasses, Bromus tectorum (an annual) and Agropyron spicatum (a perennial), the probability of dying after being grazed by microtines decreases with age at initial grazing (115). Herbivory on a young plant is an act of predation, killing the plant immediately, whereas herbivory on a larger plant often results only in reduced growth and reproduction. Consequently, the timing of the interaction relative to plant age can affect the extent to which selection on these populations is primarily "viability selection" or "fecundity selection." Such differences in selection could affect the kinds of defenses that evolve within plant populations (149).

Age structure may also influence the evolution of mutualism. In environ-

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ments in which lifespans of hosts are short, some potential mutualisms may be preempted. Under these conditions, host lifespans may not permit sufficient time for development of the symbiont or sufficient time for the symbiont to have an effect on host growth or reproduction. At the other extreme, if host lifespans are already long, it may require a large input on the part of any symbiont to have a significant effect on the host. Hence, some kinds of symbiotic mutualism may be most likely to develop in populations in which hosts have intermediate lifespans that can be readily affected by a small input by a symbiont (123, 125) in environments with intermediate disturbance regimes (149, 152).

Relative age structures and generation times of hosts and parasites may affect the distribution of outcomes and potentially the evolution of reduced virulence in parasites. Analyses of the evolution of reduced or intermediate virulence in parasites living in hosts with much longer generation times have invoked interdemic selection (80, 176), rapid rates of evolution within in- dividual hosts (138), mode of transmission (42), and/or maximum transmissi- bility of parasites at intermediate levels of virulence (4, 87, 89). How the evolution of pathogenicity varies among populations differing in age structure if susceptibility is age-dependent has not yet been thoroughly explored in models.

Size-Dependent Outcomes In many taxa, size is as important as age as an influence on the demography of a population (e.g. 127a) and on interactions with other species. Outcomes of competition can depend upon size in a variety of taxa (19, 96, 103, 131). Similarly, the outcomes of trophic interactions can depend upon size, as in the effects of phytophagous insects on plant reproduction (68, 85), and the likelihood of successful predation on particular prey sizes by gastropods (73) and fish (174). Nonetheless, only recently have there been attempts to devel- op mathematical theory for species interactions in size-structured populations (156, 174). Shifts in the distributions of sizes and growth rates within a population can affect both the probability that an individual with a given growth rate will ever encounter some other species during its lifetime (156) and the population outcomes of interspecific interactions (174).

Differences in outcome that depend upon size can result in a population in which individuals of different sizes interact with different species. Within the population of Darwin's Medium Ground Finch (Geospiza fortis) on Daphne Major in the Galapagos, individuals differ in bill size and their ability to crack large seeds (114). Only the finches with relatively large bills are able to crack seeds of Opuntia echois and Tribulus cistoides. The smaller birds can crack only the smaller, softer seeds produced by some other plant species. Con- sequently, the birds in this population vary in the proportion of large seeds

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they incorporate in their diets, and large-seeded plants are susceptible to predation from only a subgroup of this avian population.

Species chosen as prey can also vary ontogenetically, when individuals grow in size as they get older. In reviewing the literature on ontogenetic shifts in species interactions, Werner & Gilliam (174) referred to these size-related differences in species interactions (and habitat use) accompanying age as the "ontogenetic niche." Hence, the distribution of outcomes of some interactions will depend upon current size distributions and growth rates of individuals within the interacting populations. Successful predation by naticid drilling gastropods on their bivalve prey varies with prey size, and Kitchell et al (74) argued that coevolution of these predator/prey interactions has been governed by this size-dependent variation in outcome.

The relationship between size and outcome in interactions is reciprocal: the distribution of sizes affects the outcomes of interactions, and interactions affect the distribution of sizes. Studies of competition have analyzed and displayed distributions of outcome in size more often than studies of any other kind of interaction. One of the common consequences of competition between plant species is an increased skewness of inequality in the distribution of plant sizes (63, 172). Decreased inequality is also possible if competition is sym- metric; that is, if competition affects all individuals equally so that no one species or one group of individuals has a competitive edge (163, 173). Asymmetric outcomes of competition, however, appear to be much more common than symmetric outcomes in both plants and animals (10, 76, 149), so an increase in inequality is probably the more common outcome in interspecific interactions. In experiments on plant competition this increased inequality seems often to take the form of a highly skewed distribution in which a few plants grow to a large size, usurping light and other resources from surrounding plants. The effect of competition on skewness or inequality of plant sizes has, in fact, been the basis of recently proposed measures of plant competition: the jackknifed skewness coefficient (63) and the bootstrap- ped Gini coefficient (172).

The outcomes of interactions between ants and trees that produce ex- trafloral nectaries may also vary with plant size. These interactions may be mutualistic primarily when trees are saplings (100, 132, 159) and may become less mutualistic as trees become too large for ants to patrol the entire plant effectively. In Prunus serotina, for example, the number of buds per tree increases approximately exponentially with trunk circumference (159). Tilman (159) estimated that if a colony of ants with 20,000 workers could forage on a small sapling at a rate of 100 ants/1000 buds, then that rate would drop to 8 ants/G000 buds on a tree larger than 30 cm in circumference. At the other extreme, small plants may not produce enough reward to attract many ants. O'Dowd (100) found that doubling the leaf area of juvenile Ochroma

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pyramidale more than doubled the number of ants visiting the foliar nectaries at any one time.

GENOTYPES AND DISTRIBUTIONS OF OUTCOMES

Multiple outcomes of interspecific interactions can be maintained within populations through genetic polymorphisms arising from a variety of mech- anisms, including frequency-dependent selection or heterozygote advantage (124, 139). Mathematical models of gene-for-gene interactions between spe- cies indicate that frequency-dependent selection can result in stable poly- morphisms within populations (77, 89). If the parasites also regulate the density of host populations, polymorphism may still result, unless the host develops resistance without a cost, or parasite virulence becomes very low without loss in transmissibility (88). Differential outcomes of interactions based upon different combinations of parasite and host genotypes could, in fact, be a major factor maintaining polymorphisms within populations (22, 27). Variation in outcome dependent upon the particular combination of parasite and host genotypes has been shown repeatedly (e.g. 60, 84, 94, 121, 134, 177) and is the basis of models of gene-for-gene interactions (6, 23, 33, 136).

Other polymorphisms in traits affecting outcomes of interactions may be maintained through conflicting selection pressures. The coexistence of cyanogenic and acyanogenic plants within populations of Lotus corniculatus along the coast of Anglesey in Britain may result partly from selective grazing on acyanogenic plants balanced by a lower salt tolerance of cyanogenic plants (28). Variation within plant populations in characters that can affect the probability and extent of herbivory has been observed in a variety of other plant species (13, 26, 36). These variations in outcome highlight the need to study and report distributions of outcome rather than just the average outcome of interactions between two or more populations.

In interactions between plants and pathogens, the extent of infection within individual plants is an important component of the outcome of an interaction. High levels of infection can result in lower growth rates, survivorship, or reproduction than in plants with low levels of infection (107). Although studies in phytopathology often divide plants into only two categories (resis- tant, susceptible) and pathogens into two complementary categories (virulent, avirulent), intermediate levels of susceptibility or virulence can occur. These distributions, however, are seldom reported.

Only recently have studies of interactions between plants and pathogens begun reporting distributions of both susceptibility and virulence in natural populations of plants and pathogens (24, 34, 99). Burdon et al (24, 99) analyzed variation in interactions between wild oats (Avena spp.) and Pucci-

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nia rusts in Australia. The results showed that both the mean and the distribu- tion of susceptibility to Puccinia differed greatly among Avena populations. Northern populations exhibited broad, symmetrical distributions, whereas southern populations exhibited narrow, skewed, or bimodal distributions. Similarly the distributions of virulence in the rusts varied among populations, ranging from almost normal distributions to more bimodal distributions. Burdon et al attributed the differences among populations in distributions of susceptibility to differences in the selection pressures placed upon the plant populations by the pathogens (99). In the more seasonal southern populations, the interactions between plants and pathogens are more ephemeral and in- termittent than in the warmer, northern populations, and the accumulation of multiple resistance alleles is less common in the southern populations.

The outcomes of interactions between plants and pathogens can vary broadly even on a much more local scale. Parker (106) found that populations of an annual legume Amphicarpaea bracteata separated by as little as 1 km differed in susceptibility to a particular strain of a fungal pathogen Syn- chytrium decipiens. Moreover, there was significant variation among families in susceptibility to the pathogen along a transect of only 160 m. The distribu- tion of outcomes along the transect was bimodal. In natural populations the distributions of disease severity should be expected to change over time both within and between generations, if survivorship depends upon disease sever- ity. Yet other interactions vary within populations because of differences among individuals in genotype or the microenvironment in which the interac- tion takes places. Coleopteran seed parasites of Lomatium grayi affect not only the seeds they attack but also the masses of surrounding unattacked seeds on the same plant. The extent to which seed parasitism affects unattacked seeds, however, differs among plants within a population (39).

POPULATION SIZE, DENSITY, SUBDIVISION, AND OUTCOMES

The outcomes and selection pressures on interactions can vary with the numbers of individuals within populations and their spatial and social subdivi- sion, and the result can be interactions that vary between antagonism and mutualism. Studies of phenological overlap in flowering plants have indicated that plants relying upon the same pollinators may potentially compete for those pollinators or suffer reduced seed set due to interspecific pollen transfer when the plants occur in moderate or high densities (e.g. 5, 25). But at low densities, the flowers of any one species may be too rare to attract pollinators. Several low-density species flowering at the same time, however, may attract pollinators, thereby increasing pollination success over what would occur if the species differed in flowering time. Hence, pollinator-mediated in-

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teractions between plants may vary from facilitation to competition as density changes from low to high, and selection for convergence or divergence of flowering phenology may vary accordingly (43, 44, 116, 130, 157, 158). How such variation in outcome affects the evolution of an interaction will depend upon the relative frequency of the different outcomes.

Mutualisms between ants and plants may depend upon a minimum threshold of ant density necessary to patrol plant surfaces effectively. The effect of ants on plant growth or reproduction is in some cases positively correlated with ant density or activity, and produces a range of outcomes (75, 129). Consequently, the outcomes of these interactions can potentially vary within populations not only with plant size, but also with the distance of a plant from an ant colony and the size of the colony visiting surrounding plants. As Beattie (9) noted, studies of the outcomes of ant/plant interactions will vary in their conclusions as variables such as ant density, herbivore density, and reward density vary. Such variation in outcome again argues for reporting distributions of outcomes together with means.

Some other interactions can persist only above a minimum threshold population size. Measles does not persist in human populations on islands with less than 500,000 people (14). Individuals acquire lifetime immunity after contracting the disease once. Consequently, after an initial epidemic, there are too few individuals lacking immunity on small islands to maintain the parasite population. The effect of population size on disease persistence within populations should be expected to vary among diseases depending upon the length of time of immunity after infection, the length of the latency period of the disease, the social and genetic structure of the population, and the age distribution of those susceptible.

Some hypotheses on the evolution of avirulence in interactions between parasites and hosts rely directly on the differing success of parasite genotypes under different densities. Levin & Lenski (77) argued that when host density is low, the evolution of temperate phage may be favored over virulent phage, for the probability of finding a new host would be low. Moreover, they argued that at high host densities, coevolution between bacteria and viruses would generally be antagonistic, whereas at low densities coevolution might tend not only just toward commensalism but also toward mutualism. Similarly, Gill & Mock (54) suggested that low host densities in red-spotted newt populations may favor apathogenicity in the trypanosomes that attack these populations. These newts reproduce in temporary ponds that historically may have been produced by beavers. Gill & Mock predicted a time sequence in mean outcome of these interactions within a pond: selection initially favors apathogenic trypanosome genotypes, but as a pond ages and newt populations become higher, selection on the trypanosomes favors pathogenic genotypes. In modelling the low density hypothesis for the evolution of temperate phageY

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Stewart & Levin (143) found that constant low density alone would not favor temperance. With constant low density set by a constant level of resource, the equilibrium density of the bacterial population does not vary, and the con- ditions for invasion by temperate or virulent phage do not differ. But with fluctuating densities, including extended periods too low to support virulent phage, temperate phage are favored over time as virulent phage fluctuate to ever lower levels as the bacterial host population fluctuates.

Selection on hosts in other interactions, such as those involving pollination or protection of a host, may vary with density in other ways. If the probability of encounter between two species is low, then selection for commensalistic or mutualistic genotypes may be ineffective. As the probability of encounter increases to the point of becoming inevitable within the lifetime of an individual host, then selection may favor host genotypes that decrease the antagonistic effect of the other species or increase the mutualistic effect (123, 125, 149, 152). Hence, selection for specific mutualistic coevolution between a plant and pollinator population would be effective only if the probability was consistently high that the plants would be visited by that pollinator species and the plants were sufficiently abundant to be consistently available to the pollinator.

The relative densities of interacting species also have the potential to influence both the direction of evolution in an interaction and the likelihood of coevolution. Gilbert (52) suggested that coevolution in Mullerian mimicry between two or more distasteful species is most likely when the populations are approximately equal in size but fluctuate in relative abundances over time. If one species is consistently less abundant than the other, simple convergence in color pattern of the less abundant on the more abundant species is probably more likely than coevolution. In Batesian mimicry (distasteful model, edible mimic converging on the model), coevolution is probably most likely when the edible mimic is at least occasionally more abundant than the model. High relative abundance of the edible mimic could exert selection on the model to diverge in color pattern, for the predators would be encountering a high proportion of edible prey with the current aposematic pattern.

PATCH DYNAMICS OF INTERACTIONS AND THEIR OUTCOMES

In the process of succession within patches, populations change in age and size distributions, densities, relative abundances, and relative proportions of genotypes (7, 31, 58, 104, 110, 140, 147, 151, 170). Moreover, populations may over time alter their local environment by changing such resources as light, nutrients, and water (66, 169). These changes in populations and resources can, in turn, affect the outcomes of interactions. Consequently,

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there can be a patch dynamics of interactions as there is a patch dynamics of species distributions, abundances, and compositions (149, 151). Walker & Chapin (171) found that, in primary succession on an Alaskan floodplain, alder (Alnus tenuifolia) can both facilitate the establishment of other plants because of its nitrogen-fixing ability and compete with other species through shading of seedlings. Hence, succession along the floodplain apparently results from an interaction of these conflicting outcomes of facilitation and competition, life history differences, and stochastic processes.

The extent to which disturbance and succession within habitat patches affect interactions depends, of course, upon the mobilities and biologies of the species and changes over time in species composition within patches. Fein- singer et al (45) found little variation between natural-disturbance patches of different sizes in interactions between highly mobile hummingbirds and flowers. They argued that the scale of natural disturbance in the Costa Rican cloud forest where they studied these interactions was too small relative to the normal movement patterns of the hummingbirds to have any effect.

Changes induced in hosts by interactions can also influence the outcomes of subsequent interactions, thereby changing the overall distribution of outcomes within a patch or population over time. Herbivory on plants can induce the production of secondary compounds (127), produce juvenilization in tissues with concomitant changes in secondary compounds (20), and potentially rearrange the carbon/nutrient balance (20, 162). These changes can affect the palatability of plant tissues, the amount of plant tissue eaten, and the growth rates of herbivores (21, 62). Such changes have been hypothesized to affect fluctuations in the sizes of some insect populations (61, 118).

CORRELATED OUTCOMES

Few populations interact with only one other species. Selection on an interac- tion between two species can in turn affect how these species interact with yet other species. The result can be positive or negative correlations of outcomes of interactions between a population and several other species. The distribu- tions of outcome in an interaction can therefore result from constraints and selection arising from other interactions affecting a population. Analyses of what can be called correlated outcomes are still few. There are no analyses showing how the? distribution of outcomes in a two-species interaction is affected by interactions with other species.

Studies of performance (survivorship, growth, reproduction) in phyto- phagous insects have shown from the insect's perspective the variety of possible correlated outcomes that can result from insect attack on two plant species. One of the most commonly suggested hypotheses for the evolution of restricted host use in insects is that adaptation to one plant species will come

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at the expense of the ability to do well feeding on other plant species; actual results range from this effect to a variety of much more diverse effects (e.g. 48, 51, 95, 117). For example, parthenogenetic genotypes of the moth Alsophila pometaria differ in whether the moths feed on oak or maple foliage. Futuyma et al (51) found that these host-specific genotypes did not differ in any simple way that would suggest better physiological adaptation of the genotypes to their normal host. The maple-feeding genotype achieved higher weights on both maple and oak than did the oak-feeding genotype. Further- more, compared to the maple-feeding genotype, the oak-feeding genotype performed more poorly on oak than on maple. In an experiment designed to study rates of adaptation to different host plants, Gould (57) found that selection on a subdivided population of two-spotted spider mites (Tetranychus urticae) produced cross-adaptation to other hosts. After 21 months, the subpopulation fed on a combination of lima beans and cucumbers had higher survivorship on two novel hosts (tobacco and potato) than did the population that had been maintained on lima beans alone. That is, selection on the outcome of the interaction between the mites and the beans and cucumbers affected indirectly the outcome of interaction between the mites and tobacco and potatoes. In tortoise beetles (Deloyala guttata), which vary among pop- ulations in use of Ipomaea species, Rausher (117) found no evidence of negative genetic correlations in performance on different hosts. In other species, the patterns of performance on different hosts may vary among genotypes within a population (168).

For the most part the genetics of performance and preference in phytophagous insects are still mostly unknown (47, 50, 155). Progress in our understanding of the evolution of interactions will demand rigorous analyses of the genetics of these correlations. Such analyses are particularly important for interactions between insects and plants, which are probably the most abundant and diverse interspecific interactions in both natural and managed terrestrial communities.

INDIRECT OUTCOMES

The outcomes of interactions between any two species can also be affected indirectly by additional interactions with other species within communities. Interactions between herbivores and plants can be shaped by predators or parasites of the herbivores (112), and the outcomes of a variety of competitive and other interactions can be influenced by parasites that attack one or more of the species (113). Indirect mutualisms or other populational effects that become apparent only when three or more species are studied simultaneously have now been indicated and modelled for a variety of other interactions as

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well (78, 128, 164, 165). The results show that the outcomes of two-species interactions can vary broadly as additional species are added or removed from an interaction. In addition, the results emphasize that evolutionary studies of relationships between species will need to be based upon broader evolutionary units of interaction: groups of interacting species through which any two- species interaction is shaped in evolutionary time (113, 149).

INTERACTION NORMS

The means and distributions of outcomes in interactions can vary among environments as changes occur in the phenotypic expression of genotypes or the effectiveness of traits involved in interactions. The range in expression of a genotype among environments is sometimes called a reaction norm (59, 141, 168). Similarly, the range of outcomes of interactions among environ- ments due to variation in the expression of genes or variation in the effective- ness of particular traits can be called an interaction norm; that is, the reaction norm of species interactions (152, 153). Analyses of interaction norms are needed to understand how different environmental conditions can affect selection on interactions, how interactions are restricted geographically, and how differences in outcome among populations can affect divergence of populations (154).

Differences in outcome among environments can potentially be great enough to shift the mean outcome along the continuum of antagonism, commensalism, and mutualism. Some of these differences could occur di- rectly through variation in the expression of genes. The gene-for-gene interac-- tion between barley and Ustilago hordei fungi can vary with the environment. In the interaction between V2V2: R2R2 genes, the parasite is usually aviru- lent. But in a test comparing responses in California and British Columbia for the barley variety Excelsior, the interaction of these genes resulted in no pathogenicity in California but low levels of pathogenicity in British Colum- bia (37).

In some interactions, outcomes are clearly mutualistic only in environments in which a small input to host nutrition by a symbiont can have a large effect on host survivorship or reproduction. Hence, some plants benefit from mycor- rhizae in nutrient-poor soils but grow better without mycorrhizae in fertile soils (69). Ant-fed plants, in which ants live and dump their debris in absorptive chambers witfin host plants, are restricted mostly to ephiphytes in relatively dry tropical canopies where nutrient flow through the canopy is low (55, 67, 70, 148, 149). Reef-building corals, which are common in tropical waters in areas of low productivity, seem to depend upon the endosymbiotic dinoflagellates that they harbor mostly within the cells of their oral endoderm

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(97). Nutrient-poor marine environments are, in fact, rich in a variety of mutualistic symbioses often involving unicellular algae (64, 79, 86, 97, 167, 175, 178).

Other interactions vary in more complex ways along gradients, cautioning against any simple conclusion on how an interaction affects fitness at different points along the gradient. In the grass species Agryoyron smithii the effect of mycorrhizae varies with soil phosphorus. At low phosphorus levels mycor- rhizal plants produce 35% more biomass than do nonmycorrhizal plants; at high phosphorus levels there is no difference in biomass production. At all phosphorus levels, however, mycorrhizal plants are shorter but have more tillers (92). Which of these effects of mycorrhizal association is more impor- tant for lifetime fitness cannot be readily assessed without concomitant de- mographic studies.

Interactions between symbionts and hosts that differ significantly among environments may even provide a basis for symbiont-induced speciation in hosts (154). Differential coadaptation of hosts and symbionts along environ- mental gradients or among habitats may potentially cause rapid divergence of host populations. Such divergence could be especially pronounced if the interaction norms resulted in the symbionts and hosts being mutualistic in some environments but antagonistic in other environments, for different sets of alleles and loci may then be under selection in the different populations.

Ideally, studies of interactions along gradients or between habitats would analyze variation in outcome for both (or all) species simultaneously. In practice most studies, except for many on competition, analyze the outcome for only one of the species. Competitive outcomes between animals vary between environments both in laboratory experiments (e.g. 12, 105) and in natural populations (e.g. 29). The outcomes of plant competition vary along gradients of soil moisture (109, 119), nutrients and light (16, 160, 161), and CO2 concentration (8). These results emphasize how the distribution of outcomes and, potentially, selection on competitive interactions can vary among environments. Most studies of reversals in competitive outcome along gradients, however, have not been done in natural communities, and rarely have field experiments on competition been repeated in different environ- ments (30).

Similarly, very few studies analyze variation in outcome among environ- ments for both species in interactions between parasites, grazers, or predators and their hosts or prey. Most studies analyze variation in outcome in only one of the species, and few actually report how the distributions in outcome vary among environments. Much more commonly reported is variation in mean outcome among environments for one of the species, as exemplified by studies of interactions between herbivores and plants. Growth rates of phytophagous insects have been shown to vary with light intensities, water

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and nitrogen content in plant parts, and levels of secondary compounds (133, 137, 144). When fed on Rudbeckia laciniata under high and low light intensities and high and low water levels, clones of Uroleucon rudbeckiae aphids differed in mean survivorship or fecundity among treatments due to water treatment, aphid clone, the interaction of aphid clone and light intensi- ty, and uncontrolled phenotypic differences among individual host plants (135). Fed on plants sprayed with N fertilizer, Cyrtobagus sp. beetles showed higher rates of population increase than did beetles grown on unsprayed plots (122). In feeding trials on Melanoplus bivittatus grasshoppers, nymphal survival and development rate varied with the mix of plant species in the diet and the temperature at which the trials were run (81). Environmental gradients also affect interactions between plants and mammalian herbivores. Secondary chemistry and palatability to snowshoe hares vary with soil fertility and shade in Alaska paper birch (Betula resinifera) but not in green alder (Alnus crispa) (21).

Effects of herbivory on plant growth, survivorship, and reproduction also vary among environments (e.g. 35). Growth and reproduction in tansy rag- wort (Senecio jacobaea) following defoliation by cinnabar moths (Tyria jacobaeae) was positively, although weakly, correlated with levels of irriga- tion in field plots (32). This study displayed the distribution of outcomes for each watering treatment, and the displayed results potentially indicate changes among treatments in the skewness, kurtosis, and modality of the distributions.

Outcomes of interactions between plants and pathogens can be influenced by temperature, light, moisture levels, and nutrition (23). For example, some genes for stem and leaf rust resistance in wheat vary in their effectiveness with temperature. Wheat plants with the Srl5 gene are resistant to some races of Puccinia graminis tritici at 15?C, show increased infection at 20?C, and exhibit a fully susceptible response at 26?C (23). Even different forms of nutrients can influence disease severity in plants. Ammonium and nitrate nitrogen often have opposite effects on disease levels (65). Few of these studies, however, report the distributions. In interactions between wild barley and powdery mildew in Israel, the distributions of disease severity differ between plants grown in sun or shade (34). In some extreme cases, the distribution of disease severity in shaded plants is skewed heavily to the right whereas in plants grown in the sun the distribution is skewed to the left.

EVOLUTIONARY CHANGES IN MODES OF INTERACTION

The distributions of outcomes within and among populations can provide evidence for the ways in which new modes of interaction evolve, including

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the evolution of sublethal grazing interactions from predator/prey in- teractions. Interactions between predators and prey are not always either strictly successful or unsuccessful from either the predator or prey viewpoint. There can be variation in the amount of damage that a predator inflicts on a prey individual that gets away and variation in the parts of a prey individual that a predator can capture or eat (the reward per captured prey). Variation within populations in failure rates at capturing prey and variation in the levels of sublethal damage on prey both provide opportunities for understanding how different combinations of traits affect the outcomes of interactions (166). In some cases sublethal damage to a prey individual may provide no nutrition to the predator, as in unsuccessful drilling or shell-breaking by marine predators (166) or beak damage by birds on butterfly wings (72). But in other cases sublethal damage may provide the predator with some nutrition, such as loss of leaf tissue to herbivores or loss of a tail to vertebrate predators in some lizards.

Some interactions that result in sublethal damage to the victim but provide some nutrition to the attacker may in fact be evolutionary consequences of selection on prey with modular structure to minimize the negative effects of inevitable interactions with predators (149). In modular organisms such as plants, some body parts can be lost without the individual dying. Grasses and large herbivorous mammals have been undergoing diffuse coevolution for millions of years (142). The current outcomes of interactions between grasses and large, hooved mammals vary geographically, depending upon the morphology of the plants (83). In North America, grasses in the Great Plains have a long evolutionary history of interactions with large, hooved mammals. The major grasses in these communities have morphological traits, including rhizomatous growth, well-adapted to such grazing. In contrast, grasses in the northern Intermountain West were never subjected to the large herds of grazing mammals common east of the Rockies. These caespitose grasses were readily killed when large, grazing mammals (cows) were placed in these steppe communities (83). Hence, the interaction between grasses and large, grazing mammals in North America varies from predation on individual plants to "grazing," in which plants lose leaves but generally are not killed by the interaction. Similar differences in response to herbivory by large hooved mammals occur among grasslands on other continents as well (82).

The conflicting results and viewpoints on the effects of herbivory on plant growth and reproduction together highlight the need for analyses of the distributions of outcome (11, 90, 102). Few studies of herbivory display the distributed outcomes for plant growth or seed production, report whether the distributions become skewed or change in kurtosis relative to control plants without herbivory, or partition the results by plant age or size. Moreover, few

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studies of herbivory are conducted under several environmental conditions to see how the results vary among environments. Yet these results are as important as the means in understanding the effects of herbivory on individual plants, plant populations, and selection. In the absence of reported distribu- tions of outcome, it is not possible to know whether the increased means in flower and fruit production with herbivory result from increases in (a) all plants, (b) a majority of plants with a normal distribution around the mean, (c) a small number of plants that do very well with herbivory thereby producing a highly skewed distribution, or (d) one or several subgroups of plants, produc- ing a bimodal or multimodal distribution of outcomes.

FINAL REMARKS

Evolutionary history is the record of diversification in species and the in- teractions that link their life histories. The interactions partly shape the evolution of species and are partly shaped themselves as species change. The result is the ever-changing mix of species and interactions called biological communities. Consequently, the two most general problems for evolutionary theory are to understand how populations and species evolve, and to un- derstand how interactions are molded, changed, or diversified under different ecological and genetic conditions.

Just as the study of the evolution of species requires that we understand the origins and partitioning of variation among individuals, the study of the evolution of interspecific interactions requires that we understand the origins and partitioning of variation in outcomes of interactions between species. The study of distributed outcomes, correlated outcomes, the patch dynamics of interactions, and interaction norms can show how different aspects of popula- tion structure and environmental conditions affect interactions. Achieving realistic evolutionary models of species interactions will demand detailed studies of these distributions of outcome. Analyses of distributions as well as mean outcomes are becoming more common, but they are not yet a standard part of studies of species interactions. The study of the patterns of variation in the outcomes of interactions provides a route toward understanding both selection and constraints on evolving interactions.

ACKNOWLEDGMENTS

I am grateful to Jeremy Burdon, Peter Feinsinger, Douglas Futuyma, Olle Pellmyr, Peter Price, and Wayne Wehling for very helpful comments on the manuscript. This work was supported by USDA Competitive Grant (Biologi- cal Stress) 84(86)-CRCR-1-1395 and NSF grant BSR 8705394.

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