Geographic Mosaic Theory Of Coevolution Research Articles

How specialists can be generalists: resolving the “parasite paradox” and implications for emerging infectious disease

The parasite paradox arises from the dual observations that parasites (broadly construed, including phy- tophagous insects) are resource specialists with restricted host ranges, and yet shifts onto relatively unrelated hosts are common in the phylogenetic diversification of parasite lineages and directly observable in ecological time. We synthe- size the emerging solution to this paradox: phenotypic flexibility and phylogenetic conservatism in traits related to resource use, grouped under the term ecological fitting, provide substantial opportunities for rapid host switching in changing environments, in the absence of the evolution of novel host-utilization capabilities. We discuss mechanisms behind ecological fitting, its implications for defining specialists and generalists, and briefly review empirical examples of host shifts in the context of ecological fitting. We conclude that host shifts via ecological fitting provide the fuel for the expansion phase of the recently proposed oscillation hypothesis of host range and speciation, and, more generally, the generation of novel combinations of interacting species within the geographic mosaic theory of coevolution. Finally, we conclude that taxon pulses, driven by climate change and large-scale ecological perturbation are drivers of biotic mixing and resultant ecological fitting, which leads to increased rates of rapid host switching, including the agents of Emerging Infectious Disease.

When Is Correlation Coevolution?

Studying the correlation between traits of interacting species has long been a popular approach for identifying putative cases of coevolution. More recently, such approaches have been used as a means to evaluate support for the geographic mosaic theory of coevolution. Here we examine the utility of these approaches, using mathematical and computational models to predict the correlation that evolves between traits of interacting species for a broad range of interaction types. Our results reveal that coevolution is neither a necessary nor a sufficient condition for the evolution of spatially correlated traits between two species. Specifically, our results show that coevolutionary selection fails to consistently generate statistically significant correlations and, conversely, that non-coevolutionary processes can readily cause statistically significant correlations to evolve. In addition, our results demonstrate that studies of trait correlations per se cannot be used as evidence either for or against a geographic mosaic process. Taken together, our results suggest that understanding the coevolutionary process in natural populations will require detailed mechanistic studies conducted in multiple populations or the use of more sophisticated statistical approaches that better use information contained in existing data sets.

Role of coevolution in generating biological diversity: spatially divergent selection trajectories

The Geographic Mosaic Theory of Coevolution predicts that divergent coevolutionary selection produces genetic differentiation across populations. The 29 studies reviewed here support this hypothesis as they all report spatially diverged selection trajectories which have generated variable outcomes in the interaction traits among populations. This holds for both mutualistic interactions such as those between host plants and their root symbionts, or plants and their pollinators, as well as for antagonistic interactions such as plants and their pathogens or herbivores. Most often, it is the strength of selection that varies across landscapes. Variation may be generated by both the physical environment (namely temperature), and the local community--competitors, parasites, and alternative hosts--that intensify or dilute selection locally for a wide range of species interactions. At its extreme, selection trajectories may be reversed with an antagonistic interaction being commensalistic in some populations and mutualistic in yet others, depending on the local community context. Selection trajectories were found to diverge among continents, but also more locally among neighbouring populations and even within a single population. This result highlights the importance of coevolutionary selection generating biological diversity with far-reaching implications for both biodiversity conservation as well as applied biology.

Local adaptation and maladaptation to pollinators in a generalist geographic mosaic

The Geographic Mosaic Theory of Coevolution predicts the occurrence of mosaics of interaction-mediated local adaptations and maladaptations. Empirical support to this prediction has come mostly from specialist interactions. In contrast, local adaptation is considered highly unlikely in generalist interactions. In this study, we experimentally test local adaptation in a generalist plant-pollinator geographic mosaic, by means of a transplant experiment in which plants coming from two evolutionary hotspots and two coldspots were offered to pollinators at the same four localities. Plants produced in the hotspots attracted more pollinators in all populations, whereas coldspot plants attracted fewer pollinators in all populations. Differences in adaptation were not related to genetic similarity between populations, suggesting that it was mainly due to spatial variation in previous selective regimes. Our experiment provides the first strong support for a spatially structured pattern of adaptation and maladaptation generated by a generalist free-living mutualism.

A geographic selection mosaic in a generalized plant–pollinator–herbivore system

The concept of Selection Mosaic is central to the Geographic Mosaic Theory of Coevolution. Most information on coevolving interactions, however, comes from specialized organisms. In contrast, an accurate understanding of the effect of geographically varying evolutionary dynamics on the evolution of generalist organisms is lacking, although these kinds of organisms are the most frequent in nature. In flowering plants, pollinators and herbivores are important selective agents. In this study we investigate whether a geographic selection mosaic for floral traits in a generalist plant,Erysimum mediohispanicum(Brassicaceae), can be mediated by the interplay of mutualistic and antagonistic interacting organisms. In eight populations we quantified the selection exerted by these organisms on several plant traits. We found significant spatial variation in pollinator assemblage. In different populations, the main pollinators belonged to different functional groups (beeflies, large bees, small bees, and beetles). Damage by ungulates also varied among populations. Consequently, we found that different populations were under different selective regimes, and the traits affected by selection depended on the local interaction intensity with pollinators and mammal herbivores. Some traits, such as flower number and stalk height, were selected similarly in most populations. Other traits, such as corolla diameter and tube length, were selected only in some populations. Finally, we found divergent selection for some traits, such as corolla tube width and corolla shape, which were selected in contrasting directions in different localities. This spatial variation in selective scenarios results in populations with strong selective regimes (hot spots) intermingled with populations with weak selective regimes (cold spots). Four important outcomes emerge from theE. mediohispanicumselection mosaic. (1) Interactions with generalist organisms may produce strong selection. (2) Spatial changes in main pollinators result in divergent selection across populations. (3) Geographic mosaics depend on a balance between mutualistic and antagonistic selection. (4) Selection mosaics operate at fairly small spatial scales. These findings will surely contribute to expanding the conceptual framework of the Geographic Mosaic Theory of Coevolution.

Locally adapted social parasite affects density, social structure, and life history of its ant hosts

Selection and adaptation are important processes in the coevolution between parasites and their hosts. The slave-making ant Protomognathus americanus, an obligate ant social parasite, has previously been shown to evolve morphological, behavioral, and chemical adaptations in the coevolutionary arms race with its Temnothorax hosts. Yet empirical studies have given variable results on the strength of the selection pressure this parasite exerts on its host populations. In this study, we directly investigated the pressure exerted by P. americanus and the reactions of the main host species, T. longispinosus, in two ant communities by manipulating parasite density in the field over several years. In addition, a cross-fostering design with the exchange of parasites between host populations allowed us to investigate local adaptation of parasite or host. We demonstrate a severe impact of the social parasite on the two host populations in West Virginia and New York, but also variation in host reactions between sites, as expected by the geographic mosaic theory of coevolution. Host density decreased at the West Virginia site with the presence of local slave-makers, whereas at the ecologically favorable New York site, density was unaffected. Nevertheless, social organization, colony size, and investment patterns of these host colonies at this site changed in response to our parasite manipulation. The release of P. americanus colonies led to a reduction in the number of resident queens and workers, an increase in intranest relatedness, and lower productivity, but also a higher investment in reproductives. In West Virginia, colony demography did not change, but raiding activity by New York slave-makers caused different investment patterns of host colonies. In addition, the cross-fostering element revealed local adaptation of the parasite P. americanus: slave-making colonies fared better in their sympatric host population, as they contained more slave-making ant workers and slaves at the end of our 27-month experiment.

Within-population genetic variability in mycorrhizal interactions

The geographic mosaic theory of coevolution hypothesizes that natural selection on species interactions varies among ecosystems, partly because the genes involved in species interactions differ in their fitness effects among environments. This selection mosaic may be expressed, at the extreme, as ecological outcomes ranging from mutualism to parasitism among environments. In a recent laboratory experiment on the interaction between a plant, bishop pine (Pinus muricata), and a root-symbiotic ectomycorrhizal fungus, Rhizopogon occidentalis, we demonstrated the potential for selection mosaics in that interaction, and the existence of substantial within-population genetic variation for symbiotic compatibility in the interaction. Here, we present the results from a second experiment on the interaction between the same ectomycorrhizal fungus and a different plant, shore pine (Pinus contorta var. contorta), designed to test for the presence of genetic variation for symbiotic compatibility in another similar system, and also to test whether such variation might be generated in part by adaptation of fungal lineages to individual trees. In this experiment, we found no genetic variation among plant lineages for compatibility with the fungal symbiont, and no evidence for adaptation of fungal lineages to individual plants, but the two fungal genotypes differed greatly in their compatibility with the plant hosts. Specifically, one of the two fungal genotypes not only colonized host plants less intensively than the other, but also had a negative effect on plant growth. Altogether, these results suggest the potential for ongoing natural selection on the ectomycorrhizal fungus, R. occidentalis, for different levels of symbiotic compatibility with particular pine hosts, but the mechanisms generating and maintaining genetic variation for symbiotic compatibility remain unclear. Such results will aid in efforts to develop realistic models of how plants and their symbionts coevolve over broad geographic ranges in which they co-occur.

Understanding the limits to generalizability of experimental evolutionary models

Given the difficulty of testing evolutionary and ecological theory in situ, in vitro model systems are attractive alternatives; however, can we appraise whether an experimental result is particular to the in vitro model, and, if so, characterize the systems likely to behave differently and understand why? Here we examine these issues using the relationship between phenotypic diversity and resource input in the T7-Escherichia coli co-evolving system as a case history. We establish a mathematical model of this interaction, framed as one instance of a super-class of host-parasite co-evolutionary models, and show that it captures experimental results. By tuning this model, we then ask how diversity as a function of resource input could behave for alternative co-evolving partners (for example, E. coli with lambda bacteriophages). In contrast to populations lacking bacteriophages, variation in diversity with differences in resources is always found for co-evolving populations, supporting the geographic mosaic theory of co-evolution. The form of this variation is not, however, universal. Details of infectivity are pivotal: in T7-E. coli with a modified gene-for-gene interaction, diversity is low at high resource input, whereas, for matching-allele interactions, maximal diversity is found at high resource input. A combination of in vitro systems and appropriately configured mathematical models is an effective means to isolate results particular to the in vitro system, to characterize systems likely to behave differently and to understand the biology underpinning those alternatives.

Natural history of Arabidopsis thaliana and oomycete symbioses

Molecular ecology of plant–microbe interactions has immediate significance for filling a gap in knowledge between the laboratory discipline of molecular biology and the largely theoretical discipline of evolutionary ecology. Somewhere in between lies conservation biology, aimed at protection of habitats and the diversity of species housed within them. A seemingly insignificant wildflower called Arabidopsis thaliana has an important contribution to make in this endeavour. It has already transformed botanical research with deepening understanding of molecular processes within the species and across the Plant Kingdom; and has begun to revolutionize plant breeding by providing an invaluable catalogue of gene sequences that can be used to design the most precise molecular markers attainable for marker-assisted selection of valued traits. This review describes how A. thaliana and two of its natural biotrophic parasites could be seminal as a model for exploring the biogeography and molecular ecology of plant–microbe interactions, and specifically, for testing hypotheses proposed from the geographic mosaic theory of co-evolution.

Increasing productivity accelerates host–parasite coevolution

Host-parasite coevolution is believed to influence a range of evolutionary and ecological processes, including population dynamics, evolution of diversity, sexual reproduction and parasite virulence. The impact of coevolution on these processes will depend on its rate, which is likely to be affected by the energy flowing through an ecosystem, or productivity. We addressed how productivity affected rates of coevolution during a coevolutionary arms race between experimental populations of bacteria and their parasitic viruses (phages). As hypothesized, the rate of coevolution between bacterial resistance and phage infectivity increased with increased productivity. This relationship can in part be explained by reduced competitiveness of resistant bacteria in low compared with high productivity environments, leading to weaker selection for resistance in the former. The data further suggest that variation in productivity can generate variation in selection for resistance across landscapes, a result that is crucial to the geographic mosaic theory of coevolution.

GEOGRAPHIC VARIATION IN THE EVOLUTION AND COEVOLUTION OF A TRITROPHIC INTERACTION

The geographic mosaic theory of coevolution predicts that geographic variation in species interactions will lead to differing selective pressures on interacting species, producing geographic variation in the traits of interacting species (Thompson 2005). We supported this hypothesis in a study of the geographic variation in the interactions among Eurosta solidaginis and its natural enemies. Eurosta solidaginis is a fly (Diptera: Tephritidae) that induces galls on subspecies of tall goldenrod, Solidago altissima altissima and S. a. gilvocanescens. We measured selection on E. solidaginis gall size and shape in the prairie and forest biomes in Minnesota and North Dakota over an 11-year period. Galls were larger and more spherical in the prairie than in the forest. We supported the hypothesis that the divergence in gall morphology in the two biomes is due to different selection regimes exerted by natural enemies of E. solidaginis. Each natural enemy exerted similar selection on gall diameter in both biomes, but differences in the frequency of natural enemy attack created strong differences in overall selection between the prairie and forest. Bird predation increased with gall diameter, creating selection for smaller-diameter galls. A parasitic wasp, Eurytoma gigantea, and Mordellistena convicta, an inquiline beetle, both caused higher E. solidaginis mortality in smaller galls, exerting selection for increased gall diameter. In the forest there was stabilizing selection on gall diameter due to a combination of bird predation on larvae in large galls, and M. convicta- and E. gigantea-induced mortality on larvae in small galls. In the prairie there was directional selection for larger galls due to M. convicta and E. gigantea mortality on larvae in small galls. Mordellistena convicta-induced mortality was consistently higher in the prairie than in the forest, whereas there was no significant difference in E. gigantea-induced mortality between biomes. Bird predation was nonexistent in the prairie so the selection against large galls found in the forest was absent. We supported the hypothesis that natural enemies of E. solidaginis exerted selection for spherical galls in both biomes. In the prairie M. convicta exerts stabilizing selection to maintain spherical galls. In the forest there was directional selection for more spherical galls. Eurytoma gigantea exerted selection on gall shape in the forest in a complex manner that varied among years. We also supported the hypothesis that E. gigantea is coevolving with E. solidaginis. The parasitoid had significantly longer ovipositors in the prairie than in the forest, indicating the possibility that it has evolved in response to selection to reach larvae in the larger-diameter prairie galls.

Dos and don'ts of testing the geographic mosaic theory of coevolution

The geographic mosaic theory of coevolution is stimulating much new research on interspecific interactions. We provide a guide to the fundamental components of the theory, its processes and main predictions. Our primary objectives are to clarify misconceptions regarding the geographic mosaic theory of coevolution and to describe how empiricists can test the theory rigorously. In particular, we explain why confirming the three main predicted empirical patterns (spatial variation in traits mediating interactions among species, trait mismatching among interacting species and few species-level coevolved traits) does not provide unequivocal support for the theory. We suggest that strong empirical tests of the geographic mosaic theory of coevolution should focus on its underlying processes: coevolutionary hot and cold spots, selection mosaics and trait remixing. We describe these processes and discuss potential ways each can be tested.

Neotyphodium infection and hybridisation as a function of environmental variation

Neotyphodium is an asexual, vertically transmitted, obligate fungal endosymbiont infecting cool-season grasses such as Arizona fescue. The relationship between Neotyphodium and several native grass hosts ranges from antagonistic to mutualistic. One theory that may explain how Neotyphodium infection is maintained despite inconsistent mutualistic benefit to the host is the bounded hybrid superiority hypothesis. This hypothesis argues that hybrids are more fit than non-hybrids in response to some environmental stresses. Neotyphodium infects hosts in both hybrid and non-hybrid forms. We tested the possibility of hybrid superiority in depauperate habitats (low soil water and nitrate) by quantifying the types and frequency of host infections (uninfected, hybrid-infected and non-hybrid-infected), and the quality of resources available between three host populations. A second theory, the geographic mosaic theory of coevolution, may also explain different symbiotic outcomes at the population level in response to variation in abiotic and biotic population characters. We provide cursory support for both hypotheses. Keywords: geographic mosaic theory of coevolution, hybrid, Festuca, Neotyphodium, symbiosis, mutualism, bounded hybrid superiority

PARASITE LOCAL ADAPTATION IN A GEOGRAPHIC MOSAIC

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.

PARASITE LOCAL ADAPTATION IN A GEOGRAPHIC MOSAIC

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.

Temporally persistent patterns of incidence and abundance in a pollinator guild at annual and decadal scales: the bees of Larrea tridentata

A recent alternative model to conventional coevolution, the geographic mosaic theory of coevolution, posits that reciprocal selection is episodic and local, rather than persistent and spatially extensive. However, little empirical evidence addresses this model's tenets, in particular the temporal stability of local plant–pollinator interactions. We evaluated this tenet using the richly diverse guild of bees at creosote bush (Larrea tridentata), a generalist plant that hosts many specialist bees. We systematically resampled over 2–5 years at 11 sites across the south-western USA. Incidence and abundance also were compared for survey sites sampled 20 ± 2 years earlier. Average Morisita-Horn faunal similarities of local bee guilds was 87% for sequential years and 36% after 20 years. Similarities in taxonomic composition of resampled local bee guilds could be statistically represented as a random assemblage drawn from the regional source pool of 54–68 bee species that could be expected at Larrea, weighted by regional abundance. At every site, only the minority of abundant bee species was typically persistent in local guilds, even after > 20 years. Most bee species in the Larrea guild were chronically uncommon, geographically sporadic and temporally unpredictable, attributes that render them numerically inconsequential as pollinators in their local guild. Persistence among abundant bee species in local pollinator assemblages satisfies one condition by which reciprocal selection could act locally. The well-being of these more abundant core species, and not bee diversity per se, may better characterize the health of such plant–pollinator associations. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 319–329.

Adaptation varies through space and time in a coevolving host-parasitoid interaction.

One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.

Coevolution across landscapes: a spatially explicit model of parasitoid-host coevolution

The geographic mosaic theory of coevolution suggests that population spatial structure may have a strong impact on coevolutionary dynamics. Therefore, coevolution must be studied across geographic scales, not just in single populations. To examine the impact of movement rate on coevolutionary dynamics, we developed a spatially explicit model of host–parasitoid coevolution. We described space as a coupled-map lattice and assumed that resistance (defined as the ability of a host to encapsulate a parasitoid egg) and virulence (defined as the successful parasitization of a host) traits were graded and costly. The model explicitly detailed population and evolutionary dynamics. When holding all parameters constant and varying only the movement rate of the host and parasitoid, profoundly different dynamics were observed. We found that fluctuations in the mean levels of resistance and virulence in the global population were greatest when the movement rate of the host and parasitoid was high. In addition, we found that the variation in resistance and virulence levels among neighboring patches was greatest when the movement rates of the host and parasitoid was low. However, as the distance among patches increased, so did the variation in resistance and virulence levels regardless of movement rate. These generalizations did not hold when spatial patterns in the distribution of resistance and virulence traits, such as spirals, were observed. Finally, we found that the evolution of resistance and virulence caused the abundance of hosts to increase and the abundance of parasitoids to decrease. As a result, the spatial distribution of hosts and parasitoids was influenced.

Coevolution in temporally variable environments.

Many potentially mutualistic interactions are conditional, with selection that varies between mutualism and antagonism over space and time. We develop a genetic model of temporally variable coevolution that incorporates stochastic fluctuations between mutualism and antagonism. We use this model to determine conditions necessary for the coevolution of matching traits between a host and a conditional mutualist. Using an analytical approximation, we show that matching traits will coevolve when the geometric mean interaction is mutualistic. When this condition does not hold, polymorphism and trait mismatching are maintained, and coevolutionary cycles may result. Numerical simulations verify this prediction and suggest that it remains robust in the presence of temporal autocorrelation. These results are compared with those from spatial models with unrestricted movement. The comparisons demonstrate that gene flow is unnecessary for generating empirical patterns predicted by the geographic mosaic theory of coevolution.

PHENOTYPE MATCHING IN WILD PARSNIP AND PARSNIP WEBWORMS: CAUSES AND CONSEQUENCES

According to the geographic mosaic theory of coevolution, selection intensity in interactions varies across a landscape, forming a selection mosaic; interaction traits match at coevolutionary hotspots where selection is reciprocal and mismatch at coldspots where reciprocity is not a factor. Chemical traits play an important role in the interaction between wild parsnip (Pastinaca sativa) and the parsnip webworm (Depressaria pastinacella). Furanocoumarins, produced as plant defenses, are detoxified by the webworms by cytochrome P450 monooxygenases; significant additive genetic variation exists for both furanocoumarin production in the plant and detoxification in the insect, making these traits available for selection. To test the hypothesis that differences in selection intensity affect the distribution of coevolutionary hotspots and coldspots in this interaction, we examined 20 populations of webworms and wild parsnips in Illinois and Wisconsin that varied in size, extent of infestation, proximity to woods (and potential vertebrate predators), and proximity to a chemically distinct alternate host plant, Heracleum lanatum (cow parsnip). Twelve of 20 populations displayed phenotype matching between plant defense and insect detoxification profiles. Of the eight mismatched populations, a logistic regression model related matching probability to two predictors: the presence of the alternate host and average content of xanthotoxin (one of the five furanocoumarins produced by P. sativa). The odds of mismatching were significantly increased by the presence of the alternate host (odds ratio = 15.4) and by increased xanthotoxin content (odds ratio = 6.053). Parsnips growing near cow parsnip displayed chemical phenotypes that were chemically intermediate between cow parsnip and parsnips growing in isolation. Rapid phenotype matching in this system is likely due in part to differential mortality every season; larvae transferred to a plant 30 m or more from the plant on which they developed tended to experience increased mortality over larvae transferred to another umbel on the same plant on which they had developed, and plant populations that mismatched in 2001 displayed a change in chemical phenotype distribution from the previous year. Trait mixing through gene flow is also a likely factor in determining mismatch frequency. Populations from which webworms were eradicated the previous year were all recolonized; in three of seven of these populations, infestation rates exceeded 90%. Our findings, consistent with the geographic mosaic theory, suggest that the presence of a chemically distinct alternate host plant can affect selection intensity in such a way as to reduce the likelihood of reciprocity in the coevolutionary interaction between wild parsnip and the parsnip webworm.