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.     

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.     

Coevolution and maladaptation

Many of the most commonly cited examples of exquisite adaptationare of coevolved symbioses. As we learn more about the coevolutionaryprocess, however, it is becoming increasingly evident that coevolutionmay also keep populations moderately maladapted much of thetime. As a result, coevolving populations may only rarely occupyadaptive peaks, because the selective landscape is under continualchange through reciprocal selection on the species themselves.These shifting patterns of coadaptation are further shaped bythe geographic structure of most species. Selection mosaicsacross landscapes and coevolutionary hotspots can favor differentevolutionary trajectories in different populations. The combinedaction of gene flow, random genetic drift, and local extinctionof populations may then continually remold these local patterns,creating a geographic mosaic in the degrees of maladaptationfound within local interactions. Recent mathematical modelsof the geographic mosaic of coevolution suggest that complexmosaics of maladaptation are a likely consequence of spatiallystructured species interactions. These models indicate thatthe spatial structure of maladaptation may depend upon the typeof coevolutionary interaction, the underlying selection mosaic,and patterns of gene flow across landscapes. By maintaininglocal polymorphisms and driving the divergence of populations,coevolution may produce spatial patterns of maladaptation thatare a source of ongoing innovation and diversification in speciesinteractions.     

Coevolutionary clines across selection mosaics

Abstract. Much of the dynamics of coevolution may be driven by the interplay between geographic variation in reciprocal selection (selection mosaics) and the homogenizing action of gene flow. We develop a genetic model of geographically structured coevolution in which gene flow links coevolving communities that may differ in both the direction and magnitude of reciprocal selection. The results show that geographically structured coevolution may lead to allele-frequency clines within both interacting species when fitnesses are spatially uniform or spatially heterogeneous. Furthermore, the results show that the behavior and shape of clines differ dramatically among different types of coevolutionary interaction. Antagonistic interactions produce dynamic clines that change shape rapidly through time, producing shifting patterns of local adaptation and maladaptation. Unlike antagonistic interactions, mutualisms generate stable equilibrium patterns that lead to fixed spatial patterns of adaptation. Interactions that vary between mutualism and antagonism produce both equilibrium and dynamic clines. Furthermore, the results demonstrate that these interactions may allow mutualisms to persist throughout the geographic range of an interaction, despite pockets of locally antagonistic selection. In all cases, the coevolved spatial patterns of allele frequencies are sensitive to the relative contributions of gene flow, selection, and overall habitat size, indicating that the appropriate scale for studies of geographically structured coevolution depends on the relative contributions of each of these factors.     

Gene flow and geographically structured coevolution

Many of the dynamic properties of coevolution may occur at the level of interacting populations, with local adaptation acting as a force of diversification, as migration between populations homogenizes these isolated interactions. This interplay between local adaptation and migration may be particularly important in structuring interactions that vary from mutualism to antagonism across the range of an interacting set of species, such as those between some plants and their insect herbivores, mammals and trypanosome parasites, and bacteria and plasmids that confer antibiotic resistance. Here we present a simple geographically structured genetic model of a coevolutionary interaction that varies between mutualism and antagonism among communities linked by migration. Inclusion of geographic structure with gene flow alters the outcomes of local interactions and allows the maintenance of allelic polymorphism across all communities under a range of selection intensities and rates of migration. Furthermore, inclusion of geographic structure with gene flow allows fixed mutualisms to be evolutionarily stable within both communities, even when selection on the interaction is antagonistic within one community. Moreover, the model demonstrates that the inclusion of geographic structure with gene flow may lead to considerable local maladaptation and trait mismatching as predicted by the geographic mosaic theory of coevolution.     

Genetic dimension of the coevolution of virulence-resistance in Drosophila -- parasitoid wasp relationships

Variations observed in parasite virulence and host resistance may be the outcome of coevolutionary processes. Recent theoretical developments have led to a 'geographic mosaic theory' of coevolution according to which there are some localities where reciprocal selection occurs (hot spots) and others where it is strongly reduced (cold spots). Studies of host-parasitoid systems back this up, revealing a geographical variation of traits subjected to antagonistic selection governed by variations in the strength of the ecological interactions. A more detailed analysis of the genetic basis of these geographic variations in a model system -- the interaction between Drosophila melanogaster and its specific parasitoid Leptopilina boulardi -- suggests that cold spots and hot spots are also driven by the amount of genetic variation available for the trait considered. Our approach, based on isolating reference strains, has been found to predict the result of sympatric interactions and it will be helpful in identifying the selective forces responsible for the coevolution. In this model, host resistance to a standardised reference strain is a weak predictor of the outcome of interactions in the field, and the main parameter accounting for the geographic variations is the number of host species available, with less parasitoid virulence towards D. melanogaster being found in areas displaying a more diversified host community.     

The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts

The "geographic mosaic" approach to understanding coevolution is predicated on the existence of variable selection across the landscape of an interaction between species. A range of ecological factors, from differences in resource availability to differences in community composition, can generate such a mosaic of selection among populations, and thereby differences in the strength of coevolution. The result is a mixture of hotspots, where reciprocal selection is strong, and coldspots, where reciprocal selection is weak or absent, throughout the ranges of species. Population subdivision further provides the opportunity for nonadaptive forces, including gene flow, drift, and metapopulation dynamics, to influence the coevolutionary interaction between species. Some predicted results of this geographic mosaic of coevolution include maladapted or mismatched phenotypes, maintenance of high levels of polymorphism, and prevention of stable equilibrium trait combinations. To evaluate the potential for the geographic mosaic to influence predator-prey coevolution, we investigated the geographic pattern of genetically determined TTX resistance in the garter snake Thamnophis sirtalis over much of the range of its ecological interaction with toxic newts of genus Taricha. We assayed TTX resistance in over 2900 garter snakes representing 333 families from 40 populations throughout western North America. Our results provide dramatic evidence that geographic structure is an important component in coevolutionary interactions between predators and prey. Resistance levels vary substantially (over three orders of magnitude) among populations and over short distances. The spatial array of variation is consistent with two areas of intense evolutionary response by predators ("hotspots") surrounded by clines of decreasing resistance. Some general predictions of the geographic mosaic process are supported, including clinal variation in phenotypes, polymorphism in some populations, and divergent outcomes of the interaction between predator and prey. Conversely, our data provide little support for one of the major predictions, mismatched values of interacting traits. Two lines of evidence suggest selection is paramount in determining population variation in resistance. First, phylogenetic information indicates that two hotspots of TTX resistance have evolved independently. Second, in the one region that TTX levels in prey have been quantified, resistance and toxicity levels match almost perfectly over a wide phenotypic and geographic range. However, these results do not preclude the role the nonadaptive forces in generating the overall geographic mosaic of TTX resistance. Much work remains to fill in the geographic pattern of variation among prey populations and, just as importantly, to explore the variation in the ecology of the interaction that occurs within populations.     

Metapopulation structure of a seed-predator weevil and its host plant in arms race coevolution

Although the importance of gene flow in the geographic structuring of host-parasite interactions has been well discussed, little is known about how dispersal drives the spatial dynamics of other types of coevolutionary interactions in nature. We evaluated the roles of gene flow in the geographically structured processes of a predator-prey arms race involving a seed-predatory weevil with a long mouthpart and its host camellia plant with a thick fruit coat. Molecular genetic analyses showed that both weevil and camellia populations were structured at a spatial scale of several kilometers. Importantly, the spatial pattern of the migration of weevils, but not that of camellias, imposed significant effects on the geographic configuration of the levels of coevolutionary escalation. This result suggests that even if migration is limited in one species (camellia), local coevolution with the other species that migrates between neighboring localities (weevil) can reduce the interpopulation difference in the local adaptive optima of the former species. Thus, gene flow of a species potentially homogenizes the local biological environments provided by the species and thereby promotes the evolutionary convergence of its coevolving counterparts. Consequently, by focusing on coevolutionary interactions in natural communities, "indirect" effects of gene flow on the adaptive divergence of organisms could be identified.     

Evolutionary diversification through hybridization in a wild host-pathogen interaction

Coevolutionary outcomes between interacting species are predicted to vary across landscapes, as environmental conditions, gene flow, and the strength of selection vary among populations. Using a combination of molecular, experimental, and field approaches, we describe how broad-scale patterns of environmental heterogeneity, genetic divergence, and regional adaptation have the potential to influence coevolutionary processes in the Linum marginale-Melampsora lini plant-pathogen interaction. We show that two genetically and geographically divergent pathogen lineages dominate interactions with the host across Australia, and demonstrate a hybrid origin for one of the lineages. We further demonstrate that the geographic divergence of the two lineages of M. lini in Australia is related to variation among lineages in virulence, life-history characteristics, and response to environmental conditions. When correlated with data describing regional patterns of variation in host resistance diversity and mating system these observations highlight the potential for gene flow and geographic selection mosaics to generate and maintain coevolutionary diversification in long-standing host-pathogen interactions.     

Natural selection drives the fine-scale divergence of a coevolutionary arms race involving a long-mouthed weevil and its obligate host plant

Background

One of the major recent advances in evolutionary biology is the recognition that evolutionary interactions between species are substantially differentiated among geographic populations. To date, several authors have revealed natural selection pressures mediating the geographically-divergent processes of coevolution. How local, then, is the geographic structuring of natural selection in coevolutionary systems?

Results

I examined the spatial scale of a "geographic selection mosaic," focusing on a system involving a seed-predatory insect, the camellia weevil (Curculio camelliae), and its host plant, the Japanese camellia (Camellia japonica). In this system, female weevils excavate camellia fruits with their extremely-long mouthparts to lay eggs into seeds, while camellia seeds are protected by thick pericarps. Quantitative evaluation of natural selection demonstrated that thicker camellia pericarps are significantly favored in some, but not all, populations within a small island (Yakushima Island, Japan; diameter ca. 30 km). At the extreme, camellia populations separated by only several kilometers were subject to different selection pressures. Interestingly, in a population with the thickest pericarps, camellia individuals with intermediate pericarp thickness had relatively high fitness when the potential costs of producing thick pericarps were considered. Also importantly, some parameters of the weevil - camellia interaction such as the severity of seed infestation showed clines along temperature, suggesting the effects of climate on the fine-scale geographic differentiation of the coevolutionary processes.

Conclusion

These results show that natural selection can drive the geographic differentiation of interspecific interactions at surprisingly small spatial scales. Future studies should reveal the evolutionary/ecological outcomes of the "fine scale geographic mosaics" in biological communities.     

Hot spots become cold spots: coevolution in variable temperature environments

Antagonistic coevolution between hosts and parasites is a key process in the genesis and maintenance of biological diversity. Whereas coevolutionary dynamics show distinct patterns under favourable environmental conditions, the effects of more realistic, variable conditions are largely unknown. We investigated the impact of a fluctuating environment on antagonistic coevolution in experimental microcosms of Pseudomonas fluorescens SBW25 and lytic phage SBWΦ2. High‐frequency temperature fluctuations caused no deviations from typical coevolutionary arms race dynamics. However, coevolution was stalled during periods of high temperature under intermediate‐ and low‐frequency fluctuations, generating temporary coevolutionary cold spots. Temperature variation affected population density, providing evidence that eco‐evolutionary feedbacks act through variable bacteria–phage encounter rates. Our study shows that environmental fluctuations can drive antagonistic species interactions into and out of coevolutionary cold and hot spots. Whether coevolution persists or stalls depends on the frequency of change and the environmental optima of both interacting players.     

Coevolution between hosts and parasites with partially overlapping geographic ranges

Many host species interact with a specific parasite within only a fraction of their geographical range. Where host and parasite overlap geographically, selection may be reciprocal constituting a coevolutionary hot spot. Host evolution, however, may be driven primarily by selection imposed by alternative biotic or abiotic factors that occur outside such hot spots. To evaluate the importance of coevolutionary hot spots for host and parasite evolution, we analyse a spatially explicit genetic model for a host that overlaps with a parasite in only part of its geographical range. Our results show that there is a critical amount of overlap beyond which reciprocal selection leads to a coevolutionary response in the host. This critical amount of overlap depends upon the explicit spatial configuration of hot spots. When the amount of overlap exceeds this first critical level, host-parasite coevolution commonly generates stable allele frequency clines rather than oscillations. It is within this region that one of the primary predictions of the geographic mosaic theory is realized, and local maladaptation is prevalent in both species. Past a further threshold of overlap between the species oscillations do evolve, but allele frequencies in both species are spatially synchronous and local maladaptation is absent in both species. A consequence of such transitions between coevolutionary dynamics is that parasite adaptation is inversely proportional to the fraction of its host's range that it occupies. Hence, as the geographical range of a parasite increases, it becomes increasingly maladapted to the host. This suggests a novel mechanism through which the geographical range of parasites may be limited.     

Coevolutionary interactions between a haploid species and a diploid species

We investigate a general model describing coevolutionary interaction between a haploid population and a diploid population, each with two alleles at a single locus. Both species are allowed to evolve, with the fitness of the genotypes of each species assumed to depend linearly on the frequencies of the genotypes of the other species. We explore the resulting outcomes of these interactions, in particular determining the location of equilibria under various conditions. The coevolution here is much more complex than that between two haploid populations and allows for the possibility of two polymorphic equilibria. To allow for further analysis, we construct a semi-symmetric model. The variety of outcomes possible even in this second model provides support for the geographic mosaic theory of coevolution by suggesting the possibility of small local populations coevolving to very different outcomes, leading to a shifting geographic mosaic as neighboring populations interact with each other through migration.     

The potential of a population genomics approach to analyse geographic mosaics of plant--insect coevolution

A central issue in the evolutionary ecology of species interactions is coevolution, which involves the reciprocal selection between individuals of interacting species. Understanding the importance of coevolution in shaping species interactions requires the consideration of spatial variation in their strength. This is exactly what the, recently developed, geographic mosaic theory of coevolution addresses. Another major development in the study of population ecology is the introduction of the population genomics approach in this field of research. This approach addresses spatial processes through molecular methods. It is of particular interest that population genomics is especially applicable to natural populations of non-model species. We describe how population genomics can be used in the context of the geographic mosaic of coevolution, specifically to identify coevolutionary hot-spots, and to attribute genetic variation found at specific loci to processes of selection versus trait remixing. The proposed integration of the population genomics approach with the conceptual framework of the geographic mosaic of coevolution is illustrated with a few selected, particularly demonstrative, examples from the realm of insect--plant interactions.     

Arms Race Coevolution: The Local and Geographical Structure of a Host–Parasite Interaction

Consideration of complex geographic patterns of reciprocal adaptation has provided insight into new features of the coevolutionary process. In this paper, we provide ecological, historical, and geographical evidence for coevolution under complex temporal and spatial scenarios that include intermittent selection, species turnover across localities, and a range of trait match/mismatch across populations. Our study focuses on a plant host–parasitic plant interaction endemic to arid and semiarid regions of Chile. The long spines of Chilean cacti have been suggested to evolve under parasite-mediated selection as a first line of defense against the mistletoe Tristerix aphyllus. The mistletoe, in turn, has evolved an extremely long morphological structure that emerges from the seed endosperm (radicle) to reach the host cuticle. When spine length was traced along cactus phylogenies, a significant association between spine length and parasitism was detected, indicating that defensive traits evolved in high correspondence with the presence or absence of parasitism in two cactus lineages. Assessment of spine-radicle matching across populations revealed a potential for coevolution in 50% of interaction pairs. Interestingly, hot spots for coevolution did not distribute at random across sites. On the contrary, interaction pairs showing high matching values occur mostly in the northern distribution of the interaction, suggesting a geographical structure for coevolution in this system. Only three sampled interaction pairs were so mismatched that reciprocal selection could not occur given current trait distributions. Overall, different lines of evidence indicate that arms-race coevolution is an ongoing phenomenon that occurs in the global system of interconnected populations.     

Four Central Points About Coevolution

Much of evolution is about the coevolution of species with each other. In recent years, we have learned that coevolution is much more pervasive, dynamic, and relentless than we previously thought. There are four central points about coevolution that we should teach the next generation of students to help them understand the importance of the coevolutionary process in shaping the web of life. (1) Complex organisms require coevolved interactions to survive and reproduce. (2) Species-rich ecosystems are built on a base of coevolved interactions. (3) Coevolution takes multiple forms and generates a diversity of ecological outcomes. (4) Interactions coevolve as constantly changing geographic mosaics.     

Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457bp allele: a mosaic of coevolution at a small geographic scale

The level of defense against great spotted cuckoo (Clamator glandarius) parasitism in different European populations of magpie (Pica pica) depends on selection pressures due to parasitism and gene flow between populations, which suggests the existence of coevolutionary hot spots within a European metapopulation. A mosaic of coevolution is theoretically possible at small geographical scales and with strong gene flow, because, among other reasons, plots may differ in productivity (i.e., reproductive success of hosts in the absence of parasitism) and defensive genotypes theoretically should be more common in plots of high productivity. Here, we tested this prediction by exploring the relationship between parasitism rate, level of defense against parasitism (estimated as both rejection rate and the frequency of the 457bp microsatellite allele associated with foreign egg rejection in magpies), and some variables related to the productivity (average laying date, clutch size, and number of hatchlings per nest) of magpies breeding in different subpopulations. We found that both estimates of defensive ability (egg rejection rate and frequency of the 457bp allele) covaried significantly with between-plot differences in probability of parasitism, laying date, and number of hatchlings per nest. Moreover, the parasitism rate was larger in more productive plots. These results confirm the existence of a mosaic of coevolution at a very local geographical scale, and the association between laying date and number of hatchlings with variables related to defensive ability and the selection pressure arising from parasitism supports the prediction of coevolutionary gradients in relation to host productivity.     

A meta-analysis of factors affecting local adaptation between interacting species

Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.     

The population biology of coevolution

New populational approaches to the study of coevolution among species are confronting two major problems: the geographic scale at which coevolution proceeds, and the long-standing issue of how species may coevolve with more than one other species. By incorporating the ecological structure of life histories and populations into analyses of the coevolutionary process, these studies are indicating that coevolutionary change is much more ecologically dynamic than indicated by earlier work. Rather than simply a slow, stately process shaping species over long periods of time, parts of the coevolutionary process may proceed rapidly (sometimes observable in less than a decade), continually molding and remolding populations and communities locally and over broad geographic scales.     

Genetic covariation of the marine fungal symbiont Haloguignardia irritans (Ascomycota, Pezizomycotina) with its algal hosts Cystoseira and Halidrys (Phaeophyceae, Fucales) along the west coast of North America

The fungal endophyte Haloguignardia irritans induces gall formation on the brown algal genera Cystoseira and Halidrys occurring from Oregon to Baja California, Mexico. Here we examine genetic covariation and compare rDNA phylogenies to investigate the coevolutionary histories of H. irritans and its algal hosts. Despite recognition of H. irritans as a single morphological species, internal transcribed spacer rDNA sequences representative of its geographic range are characterized by sequence variation at the intraspecific to intrageneric levels. An assessment of parallel cladogenesis between endophyte and host phylogenies provides evidence for a combination of independent fungal divergence and host jumping, similar to that observed in terrestrial lichens. Our results suggest that reduced gene flow due to geographic isolation is a major contributing factor to more concerted covariation observed at one island site, rather than to differences among algal host species alone. Because geography and its effects on gene flow can create heterogeneous mosaics of coevolution for symbioses in terrestrial environments, our results support the notion that conservation efforts toward the maintenance of genetic diversity in marine environments should likewise consider geographic complexity and its effects on coevolving marine species.