Rapidly fluctuating environments constrain coevolutionary arms races by impeding selective sweeps

Although pervasive, the impact of temporal environmental heterogeneity on coevolutionary processes is poorly understood. Productivity is a key temporally heterogeneous variable, and increasing productivity has been shown to increase rates of antagonistic arms race coevolution, and lead to the evolution of more broadly resistant hosts and more broadly infectious parasites. We investigated the effects of the grain of environmental heterogeneity, in terms of fluctuations in productivity, on bacteria–phage coevolution. Our findings demonstrate that environmental heterogeneity could constrain antagonistic coevolution, but that its effect was dependent upon the grain of heterogeneity, such that both the rate and extent of coevolution were most strongly limited in fine-grained, rapidly fluctuating heterogeneous environments. We further demonstrate that rapid environmental fluctuations were likely to have impeded selective sweeps of resistance alleles, which occurred over longer durations than the fastest, but not the slowest, frequency of fluctuations used. Taken together our results suggest that fine-grained environmental heterogeneity constrained the coevolutionary arms race by impeding selective sweeps.

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title: The Geographic Mosaic of Coevolution
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title: Increasing productivity accelerates host–parasite coevolution
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title: Population mixing accelerates coevolution
abstract: Theory predicts that mixing in spatially structured populations of hosts and parasites can increase the rate of antagonistic coevolution. We experimentally tested this prediction by allowing populations of bacteria (Pseudomonas fluorescens) and parasitic bacteriophage to coevolve in mixed and unmixed microcosms. Coevolution proceeded at approximately twice the rate in mixed populations compared with unmixed populations and caused the evolution of more resistant hosts and more infective parasites.

title: Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages
abstract: Spatial abiotic heterogeneity can result in divergent selection, hence might increase the magnitude of host–parasite local adaptation (the mean difference in fitness of sympatric vs. allopatric host–parasite combinations). We explicitly tested this hypothesis by measuring local adaptation in experimentally coevolved populations of bacteria and viruses evolved in the same or different nutrient media. Consistent with previous work, we found that mean levels of evolved phage infectivity and bacteria resistance varied with nutrient concentration, with maximal levels at nutrient concentrations that supported the greatest densities of bacteria. Despite this variation in evolved mean infectivity and resistance between treatments, we found that parasite local adaptation was greatly increased when measured between populations evolved in different, compared with the same, media. This pattern is likely to have resulted from different media imposing divergent selection on bacterial hosts, and phages in turn adapting to their local hosts. These results demonstrate that the abiotic environment can play a strong and predictable role in driving patterns of local adaptation.

title: Coevolution in Temporally Variable Environments
abstract: 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.

title: Antagonistic coevolution across productivity gradients: an experimental test of the effects of dispersal
abstract: Coevolution commonly occurs in spatially heterogeneous environments, resulting in variable selection pressures acting on coevolving species. Dispersal across such environments is predicted to have a major impact on local coevolutionary dynamics. Here, we address how co‐dispersal of coevolving populations of host and parasite across an environmental productivity gradient affected coevolution in experimental populations of bacteria and their parasitic viruses (phages). The rate of coevolution between bacteria and phages was greater in high‐productivity environments. High‐productivity immigrants (∼2% of the recipient population) caused coevolutionary dynamics (rates of coevolution and degree of generalist evolution) in low‐productivity environments to be largely indistinguishable from high‐productivity environments, whereas immigration from low‐productivity environments (∼0.5% of the population) had no discernable impact. These results could not be explained by demography alone, but rather high‐productivity immigrants had a selective advantage in low‐productivity environments, but not vice versa. Coevolutionary interactions in high‐productivity environments are therefore likely to have a disproportionate impact on coevolution across the landscape as a whole.

title: Gene Flow Reverses an Adaptive Cline in a Coevolving Host‐Parasitoid Interaction
abstract: Many natural populations are characterized by clinal patterns of adaptation, but it is unclear how gene flow and environmental gradients interact to drive such clines. We addressed this question by directly manipulating dispersal and productivity in an experimental landscape containing a microbial parasitoid, the bacteriophage T7, and its host, the bacterium Escherichia coli. We observed that the adaptation of parasitoids increased on hosts originating from lower‐productivity communities in the absence of gene flow. However, adaptation decreased along the same productivity gradient with experimentally imposed gene flow of the host and parasitoid. This occurred despite relatively low rates of gene flow.

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

title: Source Populations Act as Coevolutionary Pacemakers in Experimental Selection Mosaics Containing Hotspots and Coldspots
abstract: Natural populations of hosts and their enemies are often spatially structured, with patches that vary in the strength of reciprocal selection, so‐called coevolutionary hotspots and coldspots with strong or weak reciprocal selection, respectively. Theory predicts that dispersal from hotspots should intensify coevolution in coldspots, whereas dispersal from coldspots should weaken coevolution in hotspots; however, there have been few empirical tests. We addressed this using paired populations of the bacterium Pseudomonas fluorescens and the phage SBW25Φ2 linked by one‐way dispersal. Within each population, the strength of reciprocal selection was manipulated by altering the bacteria‐phage encounter rate, which changes the rate of coevolution without affecting environmental productivity. We observed that dispersal from hotspots accelerated coevolution in coldspots, while dispersal from coldspots decelerated coevolution in hotspots. These results confirm theoretical predictions and suggest that source populations can act as coevolutionary “pacemakers” for recipient populations, overriding local conditions.

title: Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution
abstract: 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.

title: GENETIC POLYMORPHISM IN HETEROGENEOUS ENVIRONMENTS: A DECADE LATER
abstract: Ten years ago, Joseph Felsenstein (35) and I (56) both wrote reviews discussing the maintenance of genetic polymorphisms in heterogeneous environments. I addressed the question of the importance in maintaining genetic variation of diversifying selection (sometimes called the niche-variation hypothesis), i.e. selection for different alleles in different environments. My focus was on the evidence and theory supporting the connection of a variable environment with genetic variation, particularly as an explanation for the large amounts of allozymic variation. At that time, the empirical evidence suggesting a genetic-environment connection for allozymic variation was mostly correlative and not in general experimentally based. Theory suggested, however, that polymorphism maintenance was possible in a variable environment; it was most likely when there was variable selection in space and limited gene flow and/or habitat selection. The purpose of this review is to evaluate the research of the intervening decade on genetic polymorphism in variable environments. The topics of this review are divided in a fashion similar to that of the earlier review. First, I mention some recent work in which there has been detailed investigation of the relationship of different environments and the maintenance of genetic variation. Second, I review the theoretical developments in the past decade. Finally, I discuss recent experimental work in some detail. An emphasis in the review is to evaluate these experimental studies, a number of which were designed specifically to determine the importance of heterogeneous environments in maintaining genetic variation.

title: Pulsed-Resource Dynamics Constrain the Evolution of Predator-Prey Interactions
abstract: Although temporal variability in the physical environment plays a major role in population fluctuations, little is known about how it drives the ecological and evolutionary dynamics of species interactions. We studied experimentally how extrinsic resource pulses affect evolutionary and ecological dynamics between the prey bacterium Serratia marcescens and the predatory protozoan Tetrahymena thermophila. Predation increased the frequency of defensive, nonpigmented prey types, which bore competitive costs in terms of reduced maximum growth rate, most in a constant-resource environment. Furthermore, the predator densities of the pulsed-resource environment regularly fluctuated above and below the mean predator densities of the constant environment. These results suggest that selection favored fast-growing competitor prey types over defensive but slower-growing prey types more often in the pulsed-resource environment (abundance of resources and low predation risk). As a result, the selection for prey defense fluctuated more in the pulsed-resource environment, leading to a weaker mean response in prey defense. At the ecological level, the evolution of prey defense weakened the relative strength of top-down regulation on prey community. This was more evident in the constant-resource environment, whereas the slow emergence of defensive prey types gradually decreased the amplitude of predator peaks in the pulsed-resource environment. Our study suggests that rapid evolution plays a smaller role in the ecological dynamics of communities dominated by resource pulses.

title: The impact of environmental change on host–parasite coevolutionary dynamics
abstract: Environmental factors are known to affect the strength and the specificity of interactions between hosts and parasites. However, how this shapes patterns of coevolutionary dynamics is not clear. Here, we construct a simple mathematical model to study the effect of environmental change on host–parasite coevolutionary outcome when interactions are of the matching-alleles or the gene-for-gene type. Environmental changes may effectively alter the selective pressure and the level of specialism in the population. Our results suggest that environmental change altering the specificity of selection in antagonistic interactions can produce alternating time windows of cyclical allele-frequency dynamics and cessation thereof. This type of environmental impact can also explain the maintenance of polymorphism in gene-for-gene interactions without costs. Overall, our study points to the potential consequences of environmental variation in coevolution, and thus the importance of characterizing genotype-by-genotype-by-environment interactions in natural host–parasite systems, especially those that change the direction of selection acting between the two species.

title: Antagonistic coevolution between a bacterium and a bacteriophage
abstract: Antagonistic coevolution between hosts and parasites is believed to play a pivotal role in host and parasite population dynamics, the evolutionary maintenance of sex and the evolution of parasite virulence. Furthermore, antagonistic coevolution is believed to be responsible for rapid differentiation of both hosts and parasites between geographically structured populations. Yet empirical evidence for host–parasite antagonistic coevolution, and its impact on between-population genetic divergence, is limited. Here we demonstrate a long–term arms race between the infectivity of a viral parasite (bacteriophage; phage) and the resistance of its bacterial host. Coevolution was largely driven by directional selection, with hosts becoming resistant to a wider range of parasite genotypes and parasites infective to a wider range of host genotypes. Coevolution followed divergent trajectories between replicate communities despite establishment with isogenic bacteria and phage, and resulted in bacteria adapted to their own, compared with other, phage populations.

title: Experimental coevolution of species interactions.
abstract: Coevolution, the process of reciprocal adaptation and counter-adaptation between ecologically interacting species, affects most organisms and is considered a key force structuring biological diversity. Our understanding of the pattern and process of coevolution, particularly of antagonistic species interactions, has been hugely advanced in recent years by an upsurge in experimental studies that directly observe coevolution in the laboratory. These experiments pose new questions by revealing novel facets of the coevolutionary process not captured by current theory, while also providing the first empirical tests of longstanding coevolutionary ideas, including the influential Red Queen hypothesis. In this article, we highlight emerging directions for this field, including experimental coevolution of mutualistic interactions and understanding how pairwise coevolutionary processes scale up within species-rich communities.

title: Experimental coevolution with bacteria and phage. The Pseudomonas fluorescens--Phi2 model system.
abstract: Parasites are ubiquitous in biological systems and antagonistic coevolution between hosts and parasites is thought be a major ecological and evolutionary force. Recent experiments using laboratory populations of bacteria and their parasitic viruses, phage, have provided the first direct empirical evidence of antagonistic coevolution in action. In this article we describe this model system and synthesise recent findings that address the causes and consequences of antagonistic coevolution.

title: Host-parasite coevolutionary arms races give way to fluctuating selection.
abstract: Host-parasite coevolution is a key driver of biological diversity and parasite virulence, but its effects depend on the nature of coevolutionary dynamics over time. We used phenotypic data from coevolving populations of the bacterium Pseudomonas fluorescens SBW25 and parasitic phage SBW25Φ2, and genetic data from the phage tail fibre gene (implicated in infectivity evolution) to show that arms race dynamics, typical of short-term studies, decelerate over time. We attribute this effect to increasing costs of generalism for phages and bacteria with increasing infectivity and resistance. By contrast, fluctuating selection on individual host and parasite genotypes was maintained over time, becoming increasingly important for the phenotypic properties of parasite and host populations. Given that costs of generalism are reported for many other systems, arms races may generally give way to fluctuating selection in antagonistically coevolving populations.

title: The impact of parasite dispersal on antagonistic host–parasite coevolution
abstract: Coevolving populations of hosts and parasites are often subdivided into a set of patches connected by dispersal. Higher relative rates of parasite compared with host dispersal are expected to lead to parasite local adaptation. However, we know of no studies that have considered the implications of higher relative rates of parasite dispersal for other aspects of the coevolutionary process, such as the rate of coevolution and extent of evolutionary escalation of resistance and infectivity traits. We investigated the effect of phage dispersal on coevolution in experimental metapopulations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage SBW25Φ2. Both the rate of coevolution and the breadth of evolved infectivity and resistance ranges peaked at intermediate rates of parasite dispersal. These results suggest that parasite dispersal can enhance the evolutionary potential of parasites through provision of novel genetic variation, but that high rates of parasite dispersal can impede the evolution of parasites by homogenizing genetic variation between patches, thereby constraining coevolution.

title: Differential impact of simultaneous migration on coevolving hosts and parasites
abstract: BackgroundThe dynamics of antagonistic host-parasite coevolution are believed to be crucially dependent on the rate of migration between populations. We addressed how the rate of simultaneous migration of host and parasite affected resistance and infectivity evolution of coevolving meta-populations of the bacterium Pseudomonas fluorescens and a viral parasite (bacteriophage). The increase in genetic variation resulting from small amounts of migration is expected to increase rates of adaptation of both host and parasite. However, previous studies suggest phages should benefit more from migration than bacteria; because in the absence of migration, phages are more genetically limited and have a lower evolutionary potential compared to the bacteria.ResultsThe results supported the hypothesis: migration increased the resistance of bacteria to their local (sympatric) hosts. Moreover, migration benefited phages more than hosts with respect to 'global' (measured with respect to the whole range of migration regimes) patterns of resistance and infectivity, because of the differential evolutionary responses of bacteria and phage to different migration regimes. Specifically, we found bacterial global resistance peaked at intermediate rates of migration, whereas phage global infectivity plateaued when migration rates were greater than zero.ConclusionThese results suggest that simultaneous migration of hosts and parasites can dramatically affect the interaction of host and parasite. More specifically, the organism with the lower evolutionary potential may gain the greater evolutionary advantage from migration.

title: Construction and validation of a neutrally-marked strain of Pseudomonas fluorescens SBW25.
abstract: Neutrally marked bacterial strains are useful in many experimental evolution and molecular ecology studies to assess the relative fitness of a given strain. Here we describe the construction and validation of a neutral marker for the model organism Pseudomonas fluorescens SBW25. The marked strain, called SBW25-lacZ, was created by integrating a promoterless 'lacZ into the defective prophage locus of the SBW25 chromosome. Fitness assays conducted in various laboratory media and in planta revealed that the fitness levels of SBW25-lacZ were comparable with the wild-type ancestor.

title: Antagonistic coevolution accelerates molecular evolution
abstract: The Red Queen hypothesis proposes that coevolution of interacting species (such as hosts and parasites) should drive molecular evolution through continual natural selection for adaptation and counter-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity genes is consistent with this, the long time periods typically required to study coevolution have so far prevented any direct empirical test. Here we show, using experimental populations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage Φ2 (refs 10, 11), that the rate of molecular evolution in the phage was far higher when both bacterium and phage coevolved with each other than when phage evolved against a constant host genotype. Coevolution also resulted in far greater genetic divergence between replicate populations, which was correlated with the range of hosts that coevolved phage were able to infect. Consistent with this, the most rapidly evolving phage genes under coevolution were those involved in host infection. These results demonstrate, at both the genomic and phenotypic level, that antagonistic coevolution is a cause of rapid and divergent evolution, and is likely to be a major driver of evolutionary change within species.

title: Genetic basis of infectivity evolution in a bacteriophage
abstract: Antagonistic coevolution between hosts and parasites is probably ubiquitous. However, very little is known of the genetic changes associated with parasite infectivity evolution during adaptation to a coevolving host. We followed the phenotypic and genetic changes in a lytic virus population (bacteriophage; phage Φ2) that coevolved with its bacterial host, Pseudomonas fluorescens SBW25. First, we show the rapid evolution of numerous unique phage infectivity phenotypes, and that both phage host range and bacterial resistance to individual phage increased over coevolutionary time. Second, each of the distinct phage phenotypes in our study had a unique genotype, and molecular evolution did not act uniformly across the phage genome during coevolution. In particular, we detected numerous substitutions on the tail fibre gene, which is involved in the first step of the host–parasite interaction: host adsorption. None of the observed mutations could be directly linked with infection against a particular host, suggesting that the phenotypic effects of infectivity mutations are probably epistatic. However, phage genotypes with the broadest host ranges had the largest number of nonsynonymous amino acid changes on genes implicated in infectivity evolution. An understanding of the molecular genetics of phage infectivity has helped to explain the complex phenotypic coevolutionary dynamics in this system.

title: Predation and resource fluctuations drive eco-evolutionary dynamics of a bacterial community
abstract: Predation and temporal resource availability are among the most important factors determining prey community dynamics and composition. Both factors have been shown to affect prey diversity, but less is known about their interactive effects, especially in rapidly evolving prey communities. In a laboratory microcosm experiment, we manipulated the presence of the predatory protozoan Tetrahymena thermophila and the temporal patterns in the availability of resources for a bacterial prey community. We found that both predation and temporal fluctuations in prey resources resulted in a more even prey community, and these factors also interacted so that the effect of predation was only seen in a fluctuating environment. One possible explanation for this finding could be differences in prey species grazing resistance and resource use abilities, which likely had the greatest effect on prey community structure in fluctuating environments with periodical resource limitation. We also found that prey communities evolved to be more grazing-resistant during the experiment, and that this effect was due to a clear increase in the grazing resistance of the bacterium Serratia marcescens. Our results demonstrate that temporal variability in prey resources and predation can promote more even prey species proportions by allowing the existence of both defensive and competitive prey life-history strategies.

title: Coevolution Drives Temporal Changes in Fitness and Diversity Across Environments in a Bacteria–Bacteriophage Interaction
abstract: Coevolutionary interactions are thought to play a crucial role in diversification of hosts and parasitoids. Furthermore, resource availability has been shown to be a fundamental driver of species diversity. Yet, we still do not have a clear understanding of how resource availability mediates the diversity generated by coevolution between hosts and parasitoids over time. We used experiments with bacteria and bacteriophage to test how resources affect variation in the competitive ability of resistant hosts and temporal patterns of diversity in the host and parasitoid as a result of antagonistic coevolution. Bacteria and bacteriophage coevolved for over 150 bacterial generations under high and low-resource conditions. We measured relative competitive ability of the resistant hosts and phenotypic diversity of hosts and parasitoids after the initial invasion of resistant mutants and again at the end of the experiment. Variation in relative competitive ability of the hosts was both time- and environment-dependent. The diversity of resistant hosts, and the abundance of host-range mutants attacking these phenotypes, differed among environments and changed over time, but the direction of these changes differed between the host and parasitoid. Our results demonstrate that patterns of fitness and diversity resulting from coevolutionary interactions can be highly dynamic.

title: Temporal dynamics of antagonism and mutualism in a geographically variable plant-insect interaction.
abstract: Variation among sites and years in the local ecological outcome of interspecific interactions can generate a geographic mosaic of coevolution, as indicated by recent mathematical models. We evaluated whether local temporal dynamics of ecological outcome in the interaction between the moth Greya politella (Prodoxidae) and its host plant Lithophragma parviflorum (Saxifragaceae) are likely to mitigate or magnify geographic differences in ecological outcome found in earlier studies. The moths are highly host-specific pollinating floral parasites, and the mutualism can be swamped in some populations by the presence of effective co-pollinators. Hence, differing community contexts can shift the outcome of the interaction from mutualism to commensalism or antagonism. During each of four years, we evaluated the effect of Greya oviposition on seed development through a paired design that controlled for plant genotype and microenvironment. At Turnbull National Wildlife Refuge in Washington State, the interaction was significantly mutualistic in all four years. Mutualism in this population was indicated by a higher probability of development of capsules visited by ovipositing Greya than capsules not visited by Greya on the same plant. At Rapid River, Idaho, the interaction was commensalistic in three years and antagonistic in one year. Antagonism in this population was indicated by selective withering of capsules containing Greya eggs. Overall, the results suggest stable geographic differences in the range of ecological outcomes in this plant-insect interaction under different community contexts.

title: COEVOLUTION BETWEEN HISPANIOLAN CROSSBILLS AND PINE: DOES MORE TIME ALLOW FOR GREATER PHENOTYPIC ESCALATION AT LOWER LATITUDE?
abstract: (Aves: Loxia) and several conifers have coevolved in predator–prey arms races over the last 10,000 years. However, the extent to which coevolutionary arms races have contributed to the adaptive radiation of crossbills or to any other adaptive radiation is largely unknown. Here we extend our previous studies of geographically structured coevolution by considering a crossbill–conifer interaction that has persisted for a much longer time period and involves a conifer with more variable annual seed production. We examined geographic variation in the cone and seed traits of two sister species of pines, Pinus occidentalis and P. cubensis, on the islands of Hispaniola and Cuba, respectively. We also compared the Hispaniolan crossbill (Loxia megaplaga) to its sister taxa the North American white-winged crossbill (Loxia leucoptera leucoptera). The Hispaniolan crossbill is endemic to Hispaniola whereas Cuba lacks crossbills. In addition and in contrast to previous studies, the variation in selection experienced by these pines due to crossbills is not confounded by the occurrence of selection by tree squirrels (Tamiasciurus and Sciurus). As predicted if P. occidentalis has evolved defenses in response to selection exerted by crossbills, cones of P. occidentalis have scales that are 53% thicker than those of P. cubensis. Cones of P. occidentalis, but not P. cubensis, also have well-developed spines, a known defense against vertebrate seed predators. Consistent with patterns of divergence seen in crossbills coevolving locally with other conifers, the Hispaniolan crossbill has evolved a bill that is 25% deeper than the white-winged crossbill. Together with phylogenetic analyses, our results suggest that predator–prey coevolution between Hispaniolan crossbills and P. occidentalis over approximately 600,000 years has caused substantial morphological evolution in both the crossbill and pine. This also indicates that cone crop fluctuations do not prevent crossbills and conifers from coevolving. Furthermore, because the traits at the phenotypic interface of the interaction apparently remain the same over at least several hundred thousand years, divergence as a result of coevolution is greater at lower latitude where crossbill–conifer interactions have been less interrupted by Pleistocene events.

title: Imbalance of Predator and Prey Armament: Geographic Clines in Phenotypic Interface and Natural Selection
abstract: 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.

title: Coevolution between crossbills and black pine: the importance of competitors, forest area and resource stability
abstract: Studies of predator‐prey interactions have found that geographically structured coevolution has played an important role in the adaptive diversification of crossbills (Loxia spp.). We extend those studies by considering common crossbills (L. curvirostra) in the Mediterranean where they rely on seeds in the cones of black pine (Pinus nigra). On the continent, where tree squirrels (Sciurus vulgaris) are present, enhanced defenses against crossbills were most evident in larger areas of pine forest. On islands in the absence of tree squirrels, crossbills and black pine have coevolved in a predator‐prey arms race on Cyprus but not Corsica. In contrast to other conifers that island endemic crossbills rely upon, black pine does not hold seeds in its cones year round. Consequently, key to the strong crossbill–pine interaction on Cyprus is likely the presence of an alternative conifer that provides seeds during early summer when black pine seeds are scarce.