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.     

Spatial geographic mosaic in an aquatic predator-prey network

The geographic mosaic theory of coevolution predicts 1) spatial variation in predatory structures as well as prey defensive traits, and 2) trait matching in some areas and trait mismatching in others mediated by gene flow. We examined gene flow and documented spatial variation in crushing resistance in the freshwater snails Mexipyrgus churinceanus, Mexithauma quadripaludium, Nymphophilus minckleyi, and its relationship to the relative frequency of the crushing morphotype in the trophically polymorphic fish Herichthys minckleyi. Crushing resistance and the frequency of the crushing morphotype did show spatial variation among 11 naturally replicated communities in the Cuatro Ciénegas valley in Mexico where these species are all endemic. The variation in crushing resistance among populations was not explained by geographic proximity or by genetic similarity in any species. We detected clear phylogeographic patterns and limited gene flow for the snails but not for the fish. Gene flow among snail populations in Cuatro Ciénegas could explain the mosaic of local divergence in shell strength and be preventing the fixation of the crushing morphotype in Herichthys minckleyi. Finally, consistent with trait matching across the mosaic, the frequency of the fish morphotype was negatively correlated with shell crushing resistance likely reflecting the relative disadvantage of the crushing morphotype in communities where the snails exhibit relatively high crushing resistance.     

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.     

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.     

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.     

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.     

A combination of functionally different plant traits provides a means to quantitatively predict a broad range of species assemblages in NW Europe

Assembly theory predicts that filtering processes will select species by their attributes to build a community. Some filters increase functional similarity among species, while others lead to dissimilarity. Assuming converging processes to be dominant within habitats, we tested in this study whether species assemblages across a wide range of habitats can be distinguished quantitatively by their mean trait compositions. In addition, we investigated how many and which traits are needed to describe the differences between species assemblages best. The approach has been applied on a dataset that included 12 plant traits and 7644 vegetation relevés covering a wide range of habitats in the Netherlands. We demonstrate that due to the dominant role of converging processes 1) the functional composition can explain up to 80% of the floristic differences between species assemblages using seven plant traits, showing that plant trait combinations provide a powerful tool for predicting the occurrence of species assemblages across different habitats; 2) to achieve a high performance, traits should be taken from different strategy components, i.e. traits that are functionally orthogonal, which does not necessarily coincide with low trait‐trait correlations; 3) the different strategy components identified in this study correspond to the strategy components of some conventional plant ecological strategy schemes (PESS) – schemes to describe the variation between individual species. However, some PESS merge traits into one strategy component that are shown to be functionally different when predicting species assemblages. If such PESS is used to predict assemblages, this leads to a loss in predictive capacity. Potentially, our new approach is globally applicable to quantify community assembly patterns. However this needs to be tested.     

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.     

Coevolution by different functional mechanisms modulates the structure and dynamics of antagonistic and mutualistic networks

A central problem in the study of species interactions is to understand the underlying ecological and evolutionary mechanisms that shape and are shaped by trait evolution in interacting assemblages. The patterns of interaction among species (i.e. network structure) provide the pathways for evolution and coevolution, which are modulated by how traits affect individual fitness (i.e. functional mechanisms). Functional mechanisms, in turn, also affect the likelihood of an ecological interaction, shaping the structure of interaction networks. Here, we build adaptive network models to explore the potential role of coevolution by two functional mechanisms, trait matching and exploitation barrier, in driving trait evolution and the structure of interaction networks. We use these models to explore how different scenarios of coevolution and functional mechanisms reproduce the empirical network patterns observed in antagonistic and mutualistic interactions and affect trait evolution. Scenarios assuming coevolutionary feedback with a strong effect of functional mechanism better reproduce the empirical structure of networks. Antagonistic and mutualistic networks, however, are better explained by different functional mechanisms and the structure of antagonisms is better reproduced than that of mutualisms. Scenarios assuming coevolution by strong trait matching between interacting partners better explain the structure of antagonistic networks, whereas those assuming strong barrier effects better reproduce the structure of mutualistic networks. The dynamics resulting from the feedback between strong functional mechanisms and coevolution favor the stability of antagonisms and mutualisms. Selection favoring trait matching reduces temporal trait fluctuation and the magnitude of arms races in antagonisms, whereas selection due to exploitation barriers reduces temporal trait fluctuations in mutualisms. Our results indicate that coevolutionary models better reproduce the network structure of antagonisms than those of mutualisms and that different functional mechanisms may favor the persistence of antagonistic and mutualistic interacting assemblages.     

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.     

The causes of variation in the presence of genetic covariance between sexual traits and preferences

Mating traits and mate preferences often show patterns of tight correspondence across populations and species. These patterns of apparent coevolution may result from a genetic association between traits and preferences (i.e. trait–preference genetic covariance). We review the literature on trait–preference covariance to determine its prevalence and potential biological relevance. Of the 43 studies we identified, a surprising 63% detected covariance. We test multiple hypotheses for factors that may influence the likelihood of detecting this covariance. The main predictor was the presence of genetic variation in mate preferences, which is one of the three main conditions required for the establishment of covariance. In fact, 89% of the nine studies where heritability of preference was high detected covariance. Variables pertaining to the experimental methods and type of traits involved in different studies did not greatly influence the detection of trait–preference covariance. Trait–preference genetic covariance appears to be widespread and therefore represents an important and currently underappreciated factor in the coevolution of traits and preferences.     

The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).     

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.     

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.     

The role of ecology,neutral processes and antagonistic coevolution in an apparent sexual arms race

Some of the strongest examples of a sexual ‘arms race’ come from observations of correlated evolution in sexually antagonistic traits among populations. However, it remains unclear whether these cases truly represent sexually antagonistic coevolution; alternatively, ecological or neutral processes might also drive correlated evolution. To investigate these alternatives, we evaluated the contributions of intersex genetic correlations, ecological context, neutral genetic divergence and sexual coevolution in the correlated evolution of antagonistic traits among populations of Gerris incognitus water striders. We could not detect intersex genetic correlations for these sexually antagonistic traits. Ecological variation was related to population variation in the key female antagonistic trait (spine length, a defence against males), as well as body size. Nevertheless, population covariation between sexually antagonistic traits remained substantial and significant even after accounting for all of these processes. Our results therefore provide strong evidence for a contemporary sexual arms race.     

Evolutionarily unstable fitness maxima and stable fitness minima of continuous traits

Summary We present models of adaptive change in continuous traits for the following situations: (1) adaptation of a single trait within a single population in which the fitness of a given individual depends on the population's mean trait value as well as its own trait value; (2) adaptation of two (or more) traits within a single population; (3) adaptation in two or more interacting species. We analyse a dynamic model of these adaptive scenarios in which the rate of change of the mean trait value is an increasing function of the fitness gradient (i.e. the rate of increase of individual fitness with the individual's trait value). Such models have been employed in evolutionary game theory and are often appropriate both for the evolution of quantitative genetic traits and for the behavioural adjustment of phenotypically plastic traits. The dynamics of the adaptation of several different ecologically important traits can result in characters that minimize individual fitness and can preclude evolution towards characters that maximize individual fitness. We discuss biological circumstances that are likely to produce such adaptive failures for situations involving foraging, predator avoidance, competition and coevolution. The results argue for greater attention to dynamical stability in models of the evolution of continuous traits.     

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.     

Challenges in linking trait patterns to niche differentiation

Among approaches to establish the importance of niche differentiation for species coexistence, the use of functional traits is attractive for its potential to suggest specific coexistence mechanisms. Recent studies have looked for trait patterns reflective of niche differentiation, building on a line of research with a deep but somewhat neglected history. We review the field from its foundation in limiting similarity theory in the 1960s to its resurgence in 2000s, and find the theory of trait patterning still in a stage of development. Elements still to be accounted for include environmental fluctuations, multidimensional niche space, transient dynamics, immigration, intraspecific variation, evolution and spatial scales. Recent empirical methods are better than early approaches, but still focus on patterning arising in simplistic models, and should rigorously link niche space with trait space, use informative null models, and adopt new metrics of pattern as theory develops. Because tests based on overly simplistic expectations of trait pattern are of little value, we argue that progress in the field requires theory development, which should entail exploring patterns across a set of conceptual and system‐specific models of competition along trait axes. Synthesis Traits relate to ecological performance and are easy to measure. Trait patterns can thus be a practical tool for inferring community assembly processes, and have been extensively used for this purpose. Classical trait patterning theory dates back to the 1960s, and despite heavy criticism still persists in empirical studies. Here we highlight steps needed for traits to realize their potential. These include firmly linking them to niche axes, and updating pattern expectations to consider recent results from models of niche dynamics, such as the emergence of species clusters. Further theory development should reveal whether there is a common traits‐based signature across different niche mechanisms.     

Evolution and coevolution in mutualistic networks

A major current challenge in evolutionary biology is to understand how networks of interacting species shape the coevolutionary process. We combined a model for trait evolution with data for twenty plant-animal assemblages to explore coevolution in mutualistic networks. The results revealed three fundamental aspects of coevolution in species-rich mutualisms. First, coevolution shapes species traits throughout mutualistic networks by speeding up the overall rate of evolution. Second, coevolution results in higher trait complementarity in interacting partners and trait convergence in species in the same trophic level. Third, convergence is higher in the presence of super-generalists, which are species that interact with multiple groups of species. We predict that worldwide shifts in the occurrence of super-generalists will alter how coevolution shapes webs of interacting species. Introduced species such as honeybees will favour trait convergence in invaded communities, whereas the loss of large frugivores will lead to increased trait dissimilarity in tropical ecosystems.     

Predictors of Species Sensitivity to Fragmentation

We reviewed empirical data and hypotheses derived from demographic, optimal foraging, life-history, community, and biogeographic theory for predicting the sensitivity of species to habitat fragmentation. We found 12 traits or trait groups that have been suggested as predictors of species sensitivity: population size; population fluctuation and storage effect; dispersal power; reproductive potential; annual survival; sociality; body size; trophic position; ecological specialisation, microhabitat and matrix use; disturbance and competition sensitive traits; rarity; and biogeographic position. For each trait we discuss the theoretical justification for its sensitivity to fragmentation and empirical evidence for and against the suitability of the trait as a predictor of fragmentation sensitivity. Where relevant, we also discuss experimental design problems for testing the underlying hypotheses. There is good empirical support for 6 of the 12 traits as sensitivity predictors: population size; population fluctuation and storage effects; traits associated with competitive ability and disturbance sensitivity in plants; microhabitat specialisation and matrix use; rarity in the form of low abundance within a habitat; and relative biogeographic position. Few clear patterns emerge for the remaining traits from empirical studies if examined in isolation. Consequently, interactions of species traits and environmental conditions must be considered if we want to be able to predict species sensitivity to fragmentation. We develop a classification of fragmentation sensitivity based on specific trait combinations and discuss the implications of the results for ecological theory.