Fine-scale local adaptation of weevil mouthpart length and camellia pericarp thickness: altitudinal gradient of a putative arms race

Although coevolutionary theory predicts that evolutionary interactions between species are spatially hierarchical, few studies have examined coevolutionary processes at multiple spatial scales. In an antagonistic system involving a plant, the Japanese camellia (Camellia japonica), and its obligate seed predator, the camellia weevil (Curculio camelliae), I elucidated the local adaptation of a camellia defensive armament (pericarp thickness) and a weevil offensive armament (rostrum length) within Yakushima Island (ca. 30 km in diameter), compared to a larger-scale variation in those traits throughout Japan reported in previous studies. Results showed that camellia pericarp thickness and weevil rostrum length vary remarkably within several kilometers on this island. In addition, geographic variation in each camellia and weevil armament was best explained by the armament size of the sympatric participant than by abiotic environmental heterogeneity. However, I also found that camellia pericarp thickness significantly decreased in cool-temperate (i.e., highland) areas, suggesting the contributions of climate on the spatial structuring of the weevil-camellia interaction. Interestingly, relatively thin pericarps occurred not only in the highlands but also in some low-altitude areas, indicating that other factors such as nonrandom or asymmetric gene flow play important roles in the metapopulation processes of interspecific interactions at small spatial scales.     

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.     

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.     

Phylogeography and the geographic cline in the armament of a seed-predatory weevil: effects of historical events vs. natural selection from the host plant

Japanese camellia (Camellia japonica) and its seed predator, the camellia weevil (Curculio camelliae), provide a notable example of a geographic mosaic of coevolution. In the species interaction, the offensive trait of the weevil (rostrum length) and the defensive trait of the plant (pericarp thickness) are involved in a geographically-structured arms race, and these traits and selective pressures acting on the plant defence vary greatly across a geographical landscape. To further explore the geographical structure of this interspecific interaction, we tested whether the geographical variation in the weevil rostrum over an 800-km range along latitude is attributed to local natural selection or constrained by historical (phylogeographical) events of local populations. Phylogeographical analyses of the mitochondrial DNA sequences of the camellia weevil revealed that this species has experienced differentiation into two regions, with a population bottleneck and subsequent range and/or population expansion within each region. Although these phylogeographical factors have affected the variation in rostrum length, analyses of competing factors for the geographical variation revealed that this pattern is primarily determined by the defensive trait of the host plant rather than by the effects of historical events of populations and a climatic factor (annual mean temperature). Thus, our study suggests the overwhelming strength of coevolutionary selection against the effect of historical events, which may have limited local adaptation.     

Weevils and camellias in a Darwin’s race: model system for the study of eco-evolutionary interactions between species

Organisms are surrounded by their predators, parasites, hosts, and mutualists, being involved in reciprocal adaptation processes with such “biotic environment”. The concept of “coevolution”, therefore, provides a basis for the comprehensive understanding of evolutionary and ecological dynamics in biological communities and ecosystems. Recent studies have shown that coevolutionary processes are spatially heterogeneous and that traits mediating interspecific interactions can evolve rapidly in natural communities. Here, I discuss factors promoting the geographic differentiation of coevolutionary interactions, the spatial scales of the geographic structuring, and the pace of coevolutionary changes, reviewing findings in the arms race coevolution involving a long-mouthed weevil and its host camellia plant. Evolutionary, ecological, and population genetic studies on the system illuminated that viewpoints from the aspect of “coevolving biosphere” were important for predicting how ongoing anthropogenic change in global environment alter the spatiotemporal dynamics of biological communities.     

Climatic gradients of arms race coevolution

In nature, spatiotemporally dynamic coevolutionary processes play major roles in the foundation and maintenance of biodiversity. Here, we examined the arms race coevolution involving a seed-eating weevil with a long snout and its camellia plant host with a thick fruit coat (pericarp) throughout the marked climatic gradient observed across the Japanese islands. Results demonstrated that female weevils, which bored holes through camellia pericarps to lay eggs into seeds, had evolved much longer snouts than males, especially in areas in which Japanese camellia pericarps were very thick. The thickness of the plant pericarp was heritable, and the camellia plant evolved a significantly thicker pericarp on islands with the weevil than on islands without it. Across populations with weevils, resource allocation to plant defense increased with increasing annual mean temperature or annual precipitation, thereby geographically differentiating the evolutionary and ecological interactions between the two species. Given that the coevolutionary relationship exhibited appreciable variation across a relatively small range of annual mean temperatures, ongoing global climatic change can dramatically alter the coevolutionary process, thereby changing the ecological interaction between these species.     

Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection

The escalation of defensive/offensive arms is ubiquitous in prey-predator evolutionary interactions. However, there may be a geographically varying imbalance in the armaments of participating species that affects the outcome of local interactions. In a system involving the Japanese camellia (Camellia japonica) and its obligate seed predator, the camellia weevil (Curculio camelliae), we investigated the geographic variation in physical defensive/offensive traits and that in natural selection on the plant's defense among 17 populations over a 700-km-wide area in Japan. The sizes of the plant defensive apparatus (pericarp thickness) and the weevil offensive apparatus (rostrum length) clearly correlated with each other across populations. Nevertheless, the balance in armaments between the two species was geographically structured. In the populations for which the balance was relatively advantageous for the plant's defense, natural selection on the trait was stronger because in the other populations, most plant individuals were too vulnerable to resist the attacks of the weevil, and their seeds were infested independent of pericarp thickness. We also found that the imbalance between the defensive/offensive armaments and the intensity of natural selection showed clear latitudinal clines. Overall, our results suggest that the imbalance of armament between sympatric prey and predator could determine the strength of local selection and that climatic conditions could affect the local and overall trajectory of coevolutionary arms races.     

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.     

Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution

Species interactions commonly coevolve as complex geographic mosaics of populations shaped by differences in local selection and gene flow. We use a haploid matching-alleles model for coevolution to evaluate how a pair of species coevolves when fitness interactions are reciprocal in some locations ("hot spots") but not in others ("cold spots"). Our analyses consider mutualistic and antagonistic interspecific interactions and a variety of gene flow patterns between hot and cold spots. We found that hot and cold spots together with gene flow influence coevolutionary dynamics in four important ways. First, hot spots need not be ubiquitous to have a global influence on evolution, although rare hot spots will not have a disproportionate impact unless selection is relatively strong there. Second, asymmetries in gene flow can influence local adaptation, sometimes creating stable equilibria at which species experience minimal fitness in hot spots and maximal fitness in cold spots, or vice versa. Third, asymmetries in gene flow are no more important than asymmetries in population regulation for determining the maintenance of local polymorphisms through coevolution. Fourth, intraspecific allele frequency differences among hot and cold spot populations evolve under some, but not all, conditions. That is, selection mosaics are indeed capable of producing spatially variable coevolutionary outcomes across the landscapes over which species interact. Altogether, our analyses indicate that coevolutionary trajectories can be strongly shaped by the geographic distribution of coevolutionary hot and cold spots, and by the pattern of gene flow among populations.     

Evolution of spatially structured host–parasite interactions

Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host–parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life‐history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host–parasite life cycle and on which life‐history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host–parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.     

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.     

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.     

Evolutionary ecology and the conservation of biodiversity

Studies on evolving interactions among species and the coevolutionary process have suggested that the conservation of biodiversity requires a broad geographic perspective, if the `interaction biodiversity' of the earth is to be conserved with its species diversity. Continued maintenance of the geographic mosaic of specialization, defense and population structure appears to be crucial to the coevolutionary process and the long-term persistence of some interspecific interactions.     

Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races

Abstract Despite the fact that parasite dispersal is likely to be one of the most important processes influencing the dynamics and coevolution of host-parasite interactions, little information is available on the factors that affect it. In most cases, opportunities for parasite dispersal should be closely linked to host biology. Here we use microsatellite genetic markers to compare the population structure and dispersal of two host races of the seabird tick Ixodes uriae at the scale of the North Atlantic. Interestingly, tick populations showed high within-population genetic variation and relatively low population differentiation. However, gene flow at different spatial scales seemed to depend on the host species exploited. The black-legged kittiwake ( Rissa tridactyla ) had structured tick populations showing patterns of isolation by distance, whereas tick populations of the Atlantic puffin ( Fratercula arctica ) were only weakly structured at the largest scale considered. Host-dependent rates of tick dispersal between colonies will alter infestation probabilities and local dynamics and may thus modify the adaptation potential of ticks to local hosts. Moreover, as I. uriae is a vector of the Lyme disease agent Borrelia burgdorferi sensu lato in both hemispheres, the large-scale movements of birds and the subsequent dispersal of ticks will have important consequences for the dynamics and coevolutionary interactions of this microparasite with its different vertebrate and invertebrate hosts.     

Adaptive divergence of scaling relationships mediates the arms race between a weevil and its host plant

Coevolution of exaggerated morphologies between insects and plants is a well-known but poorly understood phenomenon in evolutionary biology. In the antagonistic interaction between a seed-predatory insect, the camellia weevil (Curculio camelliae), and its host plant, Japanese camellia (Camellia japonica), we examined the evolutionary trajectory of an exaggerated offensive trait of the weevil (rostrum length) in terms of scaling relationship. Sampling throughout Japan revealed that the ratio of the rostrum length to overall body size was correlated with the ratio of the pericarp thickness to overall fruit size across the localities. We found a geographical interpopulation divergence in a parameter pertaining to the allometric equation of rostrum length (the coefficient a in y=axb, where y and x denote rostrum and body lengths, respectively), and the pattern of geographical differentiation in the allometric coefficient was closely correlated with the variation in the pericarp thickness of Japanese camellia. Our results provide a novel example of a geographically diverged scaling relationship in an insect morphology resulting from a coevolutionary arms race with its host plant.     

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.     

Comparative population genetic structures and local adaptation of two mutualists

Similar patterns of dispersal and gene flow between closely associated organisms may promote local adaptation and coevolutionary processes. We compare the genetic structures of the two species of a plant genus (Roridula gorgonias and R. dentata) and their respective obligately associated hemipteran mutualists (Pameridea roridulae and P. marlothi) using allozymes. In addition, we determine whether genetic structure is related to differences in host choice by Pameridea. Allozyme variation was found to be very structured among plant populations but less so among hemipteran populations. Strong genetic structuring among hemipteran populations was only evident when large distances isolated the plant populations on which they live. Although genetic distances among plant populations were correlated with genetic distances among hemipteran populations, genetic distances of both plants and hemipterans were better correlated with geographic distance. Because Roridula and Pameridea have different scales of gene flow, adaptation at the local population level is unlikely. However, the restricted gene flow of both plants and hemipterans could enable adaptation to occur at a regional level. In choice experiments, the hemipteran (Pameridea) has a strong preference for its carnivorous host plant (Roridula) above unrelated host plants. Pameridea also prefers its host species to its closely related sister species. Specialization at the specific level is likely to reinforce cospeciation processes in this mutualism. However, Pameridea does not exhibit intraspecific preferences toward plants from their natal populations above plants from isolated, non-natal populations.     

Recurrent evolution of host-specialized races in a globally distributed parasite

The outcome of coevolutionary interactions is predicted to vary across landscapes depending on local conditions and levels of gene flow, with some populations evolving more extreme specializations than others. Using a globally distributed parasite of colonial seabirds, the tick Ixodes uriae, we examined how host availability and geographic isolation influences this process. In particular, we sampled ticks from 30 populations of six different seabird host species, three in the Southern Hemisphere and three in the Northern Hemisphere. We show that parasite races have evolved independently on hosts of both hemispheres. Moreover, the degree of differentiation between tick races varied spatially within each region and suggests that the divergence of tick races is an ongoing process that has occurred multiple times across isolated areas. As I. uriae is vector to the bacterium responsible for Lyme disease Borrelia burgdorferi sensu lato, these results may have important consequence for the epidemiology of this disease. With the increased occurrence of novel interspecific interactions due to global change, these results also stress the importance of the combined effects of gene flow and selection for parasite diversification.     

THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with “stepping-stone” distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping-stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate “host races.” Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.