Geographic Mosaic Theory Of Coevolution Research Articles

The coevolutionary mosaic of bat betacoronavirus emergence risk.

Pathogen evolution is one of the least predictable components of disease emergence, particularly in nature. Here, building on principles established by the geographic mosaic theory of coevolution, we develop a quantitative, spatially explicit framework for mapping the evolutionary risk of viral emergence. Driven by interest in diseases like Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS), and Coronavirus disease 2019 (COVID-19), we examine the global biogeography of bat-origin betacoronaviruses, and find that coevolutionary principles suggest geographies of risk that are distinct from the hotspots and coldspots of host richness. Further, our framework helps explain patterns like a unique pool of merbecoviruses in the Neotropics, a recently discovered lineage of divergent nobecoviruses in Madagascar, and-most importantly-hotspots of diversification in southeast Asia, sub-Saharan Africa, and the Middle East that correspond to the site of previous zoonotic emergence events. Our framework may help identify hotspots of future risk that have also been previously overlooked, like West Africa and the Indian subcontinent, and may more broadly help researchers understand how host ecology shapes the evolution and diversity of pandemic threats.

A test of the Geographic Mosaic Theory of Coevolution: investigating widespread species of Amazonian Protium (Burseraceae) trees, their chemical defenses, and their associated herbivore faunas

IntroductionPlants and their insect herbivores represent a large fraction of the species in Amazonian forests and are often directly implicated in the origin and maintenance of biodiversity at local and regional scales. How these interactions may change over geographic distance is unknown because very few studies have investigated the herbivore fauna and defense chemicals of any host plant species at multiple sites in tropical forests. One hypothesis, the Geographic Mosaic Theory of Coevolution, predicts that if herbivore assemblages turn over in different parts of a plant’s range, then plant defense chemicals should also change, reflecting local selection pressures.MethodsWe tested this theory by studying 12 species of Protium (Burseraceae) trees that occur in both Iquitos, Peru, and Manaus, Brazil, in rainforests separated by 1500 km. We surveyed all insects observed directly feeding on the plants in both locations for 48 weeks in Manaus and 64 weeks in Iquitos. We analyzed the secondary metabolites in the leaves of all species in both locations using GC/MS and HPLC.Results and DiscussionAlthough in both locations we found that Protium herbivores were dominated by insects from the orders Hemiptera, Coleoptera and Lepidoptera, we found almost complete turnover in the herbivore species composition in the two sites, and each host plant species had a different assemblage of herbivores in each location. Comparing the phylogenetic beta-diversity, we found low similarity in herbivore phylogenetic relatedness between host plant species in the two locations. However, the secondary metabolites found within a Protium species were similar across the two locations. We found no strong evidence that individuals from a host plant species in Iquitos or Manaus expressed locally-adapted defense chemicals, as individuals from geographic locations did not form clusters when looking at patterns of chemical similarity. These results are not consistent with the Geographic Mosaic Theory of Coevolution. The most intriguing pattern we found was a strong correlation between the diversity of herbivores per host plant species in both locations. We also found that plants with high chemical richness had lower numbers of herbivore species and numbers of total herbivores in both locations. We conclude that high chemical diversity is the most effective strategy for Protium trees to reduce insect herbivore attacks. We speculate that each secondary metabolite is effective at repelling only a few insect herbivores, and that different chemicals are likely effective in different parts of a plants’ geographic range. Future studies should investigate additional locations and additional natural enemies (i.e., fungal pathogens) to test the hypothesis that chemical diversity reduces attack from natural enemies and may explain the ecological and evolutionary success of rainforest trees over time and space.

Diversity of Herbicide-Resistance Mechanisms of Avena fatua L. to Acetyl-CoA Carboxylase-Inhibiting Herbicides in the Bajio, Mexico.

Herbicide resistance is an evolutionary process that affects entire agricultural regions’ yield and productivity. The high number of farms and the diversity of weed management can generate hot selection spots throughout the regions. Resistant biotypes can present a diversity of mechanisms of resistance and resistance factors depending on selective conditions inside the farm; this situation is similar to predictions by the geographic mosaic theory of coevolution. In Mexico, the agricultural region of the Bajio has been affected by herbicide resistance for 25 years. To date, Avena fatua L. is one of the most abundant and problematic weed species. The objective of this study was to determine the mechanism of resistance of biotypes with failures in weed control in 70 wheat and barley crop fields in the Bajio, Mexico. The results showed that 70% of farms have biotypes with target site resistance (TSR). The most common mutations were Trp–1999–Cys, Asp–2078–Gly, Ile–2041–Asn, and some of such mutations confer cross-resistance to ACCase-inhibiting herbicides. Metabolomic fingerprinting showed four different metabolic expression patterns. The results confirmed that in the Bajio, there exist multiple selection sites for both resistance mechanisms, which proves that this area can be considered as a geographic mosaic of resistance.

The geographic mosaic in parallel: Matching patterns of newt tetrodotoxin levels and snake resistance in multiple predator-prey pairs.

The Geographic Mosaic Theory of Coevolution predicts that coevolutionary arms races will vary over time and space because of the diverse ecological settings and population histories of interacting species across the landscape. Thus, understanding coevolution may require investigating broad sets of populations sampled across the range of the interaction. In addition, comparing coevolutionary dynamics between similar systems may reveal the importance of specific factors that structure coevolution. Here, we examine geographic patterns of prey traits and predator traits in the relatively unstudied interaction between the Sierra garter snake (Thamnophis couchii) and sympatric prey, the rough-skinned newt (Taricha granulosa), Sierra newt (Ta. sierrae) and California newt (Ta. torosa). This system parallels, in space and phenotypes, a classic example of coevolution between predatory common garter snakes (Th. sirtalis) and their toxic newt prey exhibiting hotspots of newt tetrodotoxin (TTX) levels and matching snake TTX resistance. We quantified prey and predator traits from hundreds of individuals across their distributions, and functional trait matching at sympatric sites. We show strong regional patterns of trait covariation across the shared ranges of Th. couchii and newt prey. Traits differ significantly among localities, with lower newt TTX levels and snake TTX resistance at the northern latitudes, and higher TTX levels and snake resistance at southern latitudes. Newts and snakes in northern populations show the highest degree of functional trait matching despite possessing the least extreme traits. Conversely, newts and snakes in southern populations show the greatest mismatch despite possessing exaggerated traits, with some snakes so resistant to TTX they would be unaffected by any sympatric newt. Nevertheless, individual variation was substantial, and appears to offer the opportunity for continued reciprocal selection in most populations. Overall, the three species of newts appear to be engaged in a TTX-mediated arms race with Th. couchii. These patterns are congruent with those seen between newts and Th. sirtalis, including the same latitudinal gradient in trait covariation, and the potential 'escape' from the arms race by snake predators. Such concordance in broad scale patterns across two distinct systems suggests common phenomena might structure geographic mosaics in similar ways.

Local Adaptation of Bacterial Symbionts within a Geographic Mosaic of Antibiotic Coevolution.

The geographic mosaic theory of coevolution (GMC) posits that coevolutionary dynamics go beyond local coevolution and are comprised of the following three components: geographic selection mosaics, coevolutionary hot spots, and trait remixing. It is unclear whether the GMC applies to bacteria, as horizontal gene transfer and cosmopolitan dispersal may violate theoretical assumptions. Here, we test key GMC predictions in an antibiotic-producing bacterial symbiont (genus Pseudonocardia) that protects the crops of neotropical fungus-farming ants (Apterostigma dentigerum) from a specialized pathogen (genus Escovopsis). We found that Pseudonocardia antibiotic inhibition of common Escovopsis pathogens was elevated in A. dentigerum colonies from Panama compared to those from Costa Rica. Furthermore, a Panama Canal Zone population of Pseudonocardia on Barro Colorado Island (BCI) was locally adapted, whereas two neighboring populations were not, consistent with a GMC-predicted selection mosaic and a hot spot of adaptation surrounded by areas of maladaptation. Maladaptation was shaped by incongruent Pseudonocardia-Escovopsis population genetic structure, whereas local adaptation was facilitated by geographic isolation on BCI after the flooding of the Panama Canal. Genomic assessments of antibiotic potential of 29 Pseudonocardia strains identified diverse and unique biosynthetic gene clusters in BCI strains despite low genetic diversity in the core genome. The strength of antibiotic inhibition was not correlated with the presence/absence of individual biosynthetic gene clusters or with parasite location. Rather, biosynthetic gene clusters have undergone selective sweeps, suggesting that the trait remixing dynamics conferring the long-term maintenance of antibiotic potency rely on evolutionary genetic changes within already-present biosynthetic gene clusters and not simply on the horizontal acquisition of novel genetic elements or pathways.IMPORTANCE Recently, coevolutionary theory in macroorganisms has been advanced by the geographic mosaic theory of coevolution (GMC), which considers how geography and local adaptation shape coevolutionary dynamics. Here, we test GMC in an ancient symbiosis in which the ant Apterostigma dentigerum cultivates fungi in an agricultural system analogous to human farming. The cultivars are parasitized by the fungus Escovopsis The ants maintain symbiotic actinobacteria with antibiotic properties that help combat Escovopsis infection. This antibiotic symbiosis has persisted for tens of millions of years, raising the question of how antibiotic potency is maintained over these time scales. Our study tests the GMC in a bacterial defensive symbiosis and in a multipartite symbiosis framework. Our results show that this multipartite symbiotic system conforms to the GMC and demonstrate that this theory is applicable in both microbes and indirect symbiont-symbiont interactions.

The geographical and seasonal mosaic in a plant-herbivore interaction: patterns of defences and herbivory by a specialist and a non-specialist

In order to evaluate the geographic mosaic theory of coevolution, it is crucial to investigate geographical variation on the outcome of ecological interactions and the functional traits which dictate these outcomes. Plant populations are attacked by specialist and non-specialist herbivores and may have different types of chemical and biotic defences. We investigated geographical and seasonal variation in the interaction between the plant Crotalaria pallida and its two major herbivores (the specialist Utetheisa ornatrix and the non-specialist Etiella zinckenella). We first showed that attack by the two herbivores and a chemical and a biotic defence vary greatly in time and space. Second, we performed a common garden experiment that revealed genetic variation among populations in herbivore resistance and a chemical defence, but no genetic variation in a biotic defence. Third, we sampled 20 populations on a much larger geographical scale and showed great variation in attack rates by the two herbivores and a chemical defence. Finally, we showed that herbivory is not correlated with a chemical defence in the 20 field populations. Our study shows that to understand the evolution of ecological interactions it is crucial to investigate how the outcome of the interaction and the important species traits vary geographically and seasonally.

Assessing Specialized Metabolite Diversity in the Cosmopolitan Plant Genus Euphorbia L.

Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.

Geographic mosaic theory of coevolution in plant and pollinator interaction: Process, evidence, prospect

Coevolution refers to evolutionary changes in the traits of two or more interacting species caused by reciprocal natural selection. Geographic mosaic theory of coevolution (GMC) proposes that the dynamics of coevolution between pairs or group of species often occur at different geographic scales. There are three hypotheses on the coevolutionary process. (1) Different evolutionary interaction trajectories among populations are likely to generate a selection mosaic. (2) A mixture of coevolutionary hotspots and coldspots. Hot spots are the subset of communities in which much of the coevolutionary change occurs and coldspots refer to areas where coevolutionary selection hardly occurs or completely does not occur. (3) There is a continual population remixing of the range of coevolving traits, resulting from the selection mosaic, coevolutionary hotspots, gene flow, random genetic drift, and local extinction of subpopulations. Studies of GMC between plants and pollinators indicate that shifts of effective pollinators among different geographic populations may cause divergence in floral traits (i.e., pollination ecotype). Changes of pollinator assemblages or species components have been illustrated coevolving with floral morphology or reward among populations from different altitudes or habitats. Here, recent case studies of GMC between plants and pollinators are grouped into five categories: Floral morphology and pollinator components, corolla tube/nectar spur and pollinator feeding structure, floral color, floral scents, floral rewards and pollinator assemblages. Floral tube or nectar spur length is positively related to pollinator body structures, such as the proboscis and leg length. The adaptation of flower color and pollinator vision provides a series of examples for the GMC. With the increase of altitude, flower color changed from blue and ultraviolet blue adapted to bee vision to blue-green and green adapted to fly vision. Recent study indicated that the difference in cycad odor components related to a shift of beetle species in different regions, suggesting a potential coevolutionary relationship between flower odor and pollinators. Studies showed that where bees foraged more nectar, flowers secreted more nectar, suggesting that floral reward amounts and types coevolve with pollinators among different geographic populations. An examination of GMC in plant-pollinator interactions involves three steps in general: (1) Detection of the relationship between floral traits and pollinator shift or body structure. (2) Transplanting experiments to detect differences in seed set between native phenotypes and transplanted phenotypes. (3) Single pollinator visit experiment to detect pollen output differences between native and transplanted phenotypes. Experimental evolutionary biology not only can test whether floral variation is related to pollinator shifts, but also make people aware of the impact of the reduction or loss of pollinators on the evolutionary consequences. To illustrate GMC between plants and pollinators, it is essential to isolate the evolutionary changes in traits caused by biotic factors or abiotic factors in future. It would be highly appreciated if genome scans and analysis are used in further studies to explore the genome-wide patterns of GMC between plants and pollinators.

The development, misuse and evidence of the concept “coevolution”

Natural selection is one of the most important components of organic evolution, while the concept of coevolution proposes that reciprocal selection generated by interacting species could also drive their organic evolution. Formally raised in 1964, the concept of coevolution has extensively developed, but been misused or even abused. Although continuously emerging studies have verified that some ecological interactions are indeed coevolution, queries of whether it is an acceptable concept remain. To clarify the precise use of the concept, we list and re-induce mistakes in using or misunderstanding of coevolution. Here a concise principle for correct usage is suggested, i.e. confirming three aspects: species interaction, reciprocal selection as well as co-phylogenesis. Bibliometric methods are applied to quantify the development of the coevolution concept, showing the bursting expansion of the term “coevolution” into study fields beyond evolutionary biology, and revealing that current usage of “coevolution” still remains within a reasonable range. Currently, studies of ecological interactions are commonly considered as in the coevolution field. Differences and commonsense of the other six related terms, namely coadaptation, cooperation, interaction, interplay, mutualism and symbiosis, are briefly discussed. Finally, case studies of frontier topics of coevolution, geographic mosaic theory of coevolution, are introduced. A better understanding of the coevolution concept could be achieved if misuse or abuse is avoided. This paper may provide references for future coevolution studies.

The geographic mosaic of coevolution in mutualistic networks

Ecological interactions shape adaptations through coevolution not only between pairs of species but also through entire multispecies assemblages. Local coevolution can then be further altered through spatial processes that have been formally partitioned in the geographic mosaic theory of coevolution. A major current challenge is to understand the spatial patterns of coadaptation that emerge across ecosystems through the interplay between gene flow and selection in networks of interacting species. Here, we combine a coevolutionary model, network theory, and empirical information on species interactions to investigate how gene flow and geographical variation in selection affect trait patterns in mutualistic networks. We show that gene flow has the surprising effect of favoring trait matching, especially among generalist species in species-rich networks typical of pollination and seed dispersal interactions. Using an analytical approximation of our model, we demonstrate that gene flow promotes trait matching by making the adaptive landscapes of different species more similar to each other. We use this result to show that the progressive loss of gene flow associated with habitat fragmentation may undermine coadaptation in mutualisms. Our results therefore provide predictions of how spatial processes shape the evolution of species-rich interactions and how the widespread fragmentation of natural landscapes may modify the coevolutionary process.

Evolutionary Responses to Conditionality in Species Interactions across Environmental Gradients.

The outcomes of many species interactions are conditional on the environments in which they occur. Often, interactions grade from being more positive under stressful or low-resource conditions to more antagonistic or neutral under benign conditions. Here, we take predictions about two well-supported ecological theories on conditionality-limiting resource models and the stress-gradient hypothesis-and combine them with those from the geographic mosaic theory of coevolution (GMTC) to generate predictions for systematic patterns of adaptation and coadaptation between partners along abiotic gradients. When interactions become more positive in stressful environments, mutations that increase fitness in one partner may also increase fitness in the other; because fitnesses are aligned, selection should favor greater mutualistic adaptation and coadaptation between interacting species in stressful ends of environmental gradients. As a corollary, in benign environments antagonistic coadaptation could result in Red Queen or arms-race dynamics or the reduction of antagonism through character displacement and niche partitioning. Here, we distinguish between generally mutualistic or antagonistic adaptation (i.e., mutations in one partner that have similar effects across multiple populations of the other) and specific adaptations to sympatric partners (local adaptation), which can occur either alone or simultaneously. We then outline the kinds of data required to test these predictions, develop experimental designs and statistical methods, and demonstrate these using simulations based on GMTC models. Our methods can be applied to a range of conditional outcomes and may also be useful in assisted translocation approaches in the face of climate change.

Myiarchus flycatchers are the primary seed dispersers of Bursera longipes in a Mexican dry forest.

We evaluated the seed dispersal of Bursera longipes by birds along a successional gradient of tropical dry forest (TDF) in southwestern Mexico. B. longipes is an endemic tree to the TDF in the Balsas basin. The relative abundance of frugivorous birds, their frequency of visits to B. longipes and the number of removed fruits were recorded at three study sites with different stages of forest succession (early, intermediate and mature) characterized by distinct floristic and structural elements. Flycatchers of the Myiarchus and Tyrannus genera removed the majority of fruits at each site. Overall, visits to B. longipes were less frequent at the early successional site. Birds that function as legitimate dispersers by consuming whole seeds and regurgitating or defecating intact seeds in the process also remove the pseudoaril from seeds, thereby facilitating the germination process. The highest germination percentages were recorded for seeds that passed through the digestive system of two migratory flycatchers: M. cinerascens and M. nutingii. Perch plants, mainly composed of legumes (e.g., Eysenhardtia polystachya, Acacia cochliacantha, Calliandra eryophylla, Mimosa polyantha), serve also as nurse plants since the number of young individuals recruited from B. longipes was higher under these than expected by chance. This study shows that Myiarchus flycatchers are the most efficient seed dispersers of B. longipes across all successional stages. This suggests a close mutualistic relationship derived from adaptive processes and local specializations throughout the distribution of both taxa, as supported by the geographic mosaic theory of coevolution.

Geographic mosaic of plant evolution: extrafloral nectary variation mediated by ant and herbivore assemblages.

Herbivory is an ecological process that is known to generate different patterns of selection on defensive plant traits across populations. Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT). Here, we hypothesize that herbivory represents a strong pressure for extrafloral nectary (EFN) bearing plants, with differences in herbivore and ant visitor assemblages leading to different evolutionary pressures among localities and ultimately to differences in EFN abundance and function. In this study, we investigate this hypothesis by analyzing 10 populations of Anemopaegma album (30 individuals per population) distributed through ca. 600 km of Neotropical savanna and covering most of the geographic range of this plant species. A common garden experiment revealed a phenotypic differentiation in EFN abundance, in which field and experimental plants showed a similar pattern of EFN variation among populations. We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities. Instead, a more complex pattern of ant–EFN variation, a geographic mosaic, emerged throughout the geographical range of A. album. We modeled the functional relationship between EFNs and ant traits across ant species and extended this phenotypic interface to characterize local situations of phenotypic matching and mismatching at the population level. Two distinct types of phenotypic matching emerged throughout populations: (1) a population with smaller ants (Crematogaster crinosa) matched with low abundance of EFNs; and (2) seven populations with bigger ants (Camponotus species) matched with higher EFN abundances. Three matched populations showed the highest plant performance and narrower variance of EFN abundance, representing potential plant evolutionary hotspots. Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores. Our findings provide insights on the ecology and evolution of plant–ant guarding systems, and suggest new directions to research on facultative mutualistic interactions at wide geographic scales.

The Population Structure of Antibiotic-Producing Bacterial Symbionts ofApterostigma dentigerumAnts: Impacts of Coevolution and Multipartite Symbiosis

Fungus-growing ants (Attini) are part of a complex symbiosis with Basidiomycetous fungi, which the ants cultivate for food, Ascomycetous fungal pathogens (Escovopsis), which parasitize cultivars, and Actinobacteria, which produce antibiotic compounds that suppress pathogen growth. Earlier studies that have characterized the association between attine ants and their bacterial symbionts have employed broad phylogenetic approaches, with conclusions ranging from a diffuse coevolved mutualism to no specificity being reported. However, the geographic mosaic theory of coevolution proposes that coevolved interactions likely occur at a level above local populations but within species. Moreover, the scale of population subdivision is likely to impact coevolutionary dynamics. Here, we describe the population structure of bacteria associated with the attine Apterostigma dentigerum across Central America using multilocus sequence typing (MLST) of six housekeeping genes. The majority (90%) of bacteria that were isolated grouped into a single clade within the genus Pseudonocardia. In contrast to studies that have suggested that Pseudonocardia dispersal is high and therefore unconstrained by ant associations, we found highly structured ([Formula: see text]) and dispersal-limited (i.e., significant isolation by distance; [Formula: see text], [Formula: see text]) populations over even a relatively small scale (e.g., within the Panama Canal Zone). Estimates of recombination versus mutation were uncharacteristically low compared with estimates for free-living Actinobacteria (e.g., [Formula: see text] in La Selva, Costa Rica), which suggests that recombination is constrained by association with ant hosts. Furthermore, Pseudonocardia population structure was correlated with that of Escovopsis species ([Formula: see text], [Formula: see text]), supporting the bacteria's role in disease suppression. Overall, the population dynamics of symbiotic Pseudonocardia are more consistent with a specialized mutualistic association than with recently proposed models of low specificity and frequent horizontal acquisition.

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.

Large scale geographic clines of parasite damage to Populus tremula L.

According to the geographic mosaic theory of coevolution (GMTC), clines of traits reflecting local co‐adaptation (including resistance genes) should be common between a host and its parasite and should persist across time. To test the GMTC‐assumption of persistent clinal patterns we compared the natural prevalence of two parasites on aspen Populus tremula trees: mining moths of the genus Phyllocnistis and leaf rust Melampsora spp. Damage data were collated from the Swedish National Forest Damage Inventory (2004–2006). In addition, occurrence of the parasites was scored in field conditions in two common gardens in the north and south of Sweden over five growing seasons (2004–2008), then related to biomass (stem height and diameter) and to concentrations of eleven leaf phenolics. Phyllocnistis mainly occurred in the northern garden, a distribution range which was confirmed by the countrywide inventory, although Phyllocnistis was more abundant on southern clones, providing evidence for possible local maladaptation. Melampsora occurred all over the country and in both gardens, but built up more quickly on northern clones, which suggests a centre of local clone maladaptation in the north. Stem growth also followed a clinal pattern as did the concentration of three phenolic compounds: benzoic acid, catechin and cinnamic acid. However, only benzoic acid was related to parasite presence: negatively to Phyllocnistis and positively to Melampsora and it could thus be a potential trait under selection.In conclusion, clines of Phyllocnistis were stronger and more persistent compared to Melampsora, which showed contrasting clines of varying strength. Our data thus support the assumption of the GMTC model that clines exist in the border between hot and cold spots and that they may be less persistent for parasites with an elevated gene flow, and/or for parasites which cover relatively larger hot spots surrounded by fewer cold spots.

Ongoing coevolution in mycorrhizal interactions

Coevolution can be a potent force in maintaining and generating biological diversity. Although coevolution is likely to have played a key role in the early development of mycorrhizal interactions, it is unclear how important coevolutionary processes are for ongoing trait evolution in those interactions. Empirical studies have shown that candidate coevolving traits, such as mycorrhizal colonization intensity, exhibit substantial heritable genetic variation within plant and fungal species and are influenced by plant genotype x fungal genotype interactions, suggesting the potential for ongoing coevolutionary selection. Selective source analysis (SSA) could be employed to build on these results, testing explicitly for ongoing coevolutionary selection and analyzing the influence of community context on local coevolutionary selection. Recent empirical studies suggest the potential for coevolution to drive adaptive differentiation among populations of plants and fungi, but further studies, especially using SSA in the context of field reciprocal transplant experiments, are needed to determine the importance of coevolutionary selection compared with nonreciprocal selection on species traits.

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

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

When Is Correlation Coevolution?

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

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

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