Molecular evidence of host-associated genetic divergence in the holly leafminer Phytomyza glabricola (Diptera: Agromyzidae): apparent discordance among marker systems

Host races play a central part in understanding the role of host plant mediated divergence and speciation of phytophagous insects. Of greatest interest are host-associated populations that have recently diverged; however, finding genetic evidence for very recent divergences is difficult because initially only a few loci are expected to evolve diagnostic differences. The holly leafminer Phytomyza glabricola feeds on two hollies, Ilex glabra and I. coriacea, that are broadly sympatric throughout most of their ranges. The leafminer is often present on both host plants and exhibits a dramatic life history difference on the two hosts, suggesting that host races may be present. We collected 1393 bp of mitochondrial cytochrome oxidase I (COI) sequence and amplified fragment length polymorphism (AFLP) data (45 polymorphic bands) from sympatric populations of flies reared from the two hosts. Phylogenetic and frequency analysis of mitochondrial COI sequence data uncovered considerable variation but no structuring by the host plant, and only limited differentiation among geographical locations. In contrast, analysis of AFLP frequency data found a significant effect with host plant, and a much smaller effect with geographical location. Likewise, neighbour-joining analysis of AFLP data resulted in clustering by host plant. The AFLP data indicate that P. glabricola is most likely comprised of two host races. Because there were no fixed differences in mitochondrial or AFLP data, this host-associated divergence is likely to have occurred very recently. P. glabricola therefore provides a new sympatric system for exploring the role of geography and ecological specialization in the speciation of phytophagous insects.     

Cascading host-associated genetic differentiation in parasitoids of phytophagous insects

The extraordinary diversity of phytophagous insects may be attributable to their narrow specialization as parasites of plants, with selective tradeoffs associated with alternate host plants driving genetic divergence of host-associated forms via ecological speciation. Most phytophagous insects in turn are attacked by parasitoid insects, which are similarly specialized and may also undergo host-associated differentiation (HAD). A particularly interesting possibility is that HAD by phytophagous insects might lead to HAD in parasitoids, as parasitoids evolve divergent lineages on the new host plant-specific lineages of their phytophagous hosts. We call this process 'cascading host-associated differentiation' (cascading HAD). We tested for cascading HAD in parasitoids of two phytophagous insects, each of which consists of genetically distinct host-associated lineages on the same pair of goldenrods (Solidago). Each parasitoid exhibited significant host-associated genetic divergence, and the distribution and patterns of divergence are consistent with divergence in sympatry. Although evidence for cascading HAD is currently limited, our results suggest that it could play an important role in the diversification of parasitoids attacking phytophagous insects. The existence of cryptic host-associated lineages also suggests that the diversity of parasitoids may be vastly underestimated.     

Lack of genetic structure among Eurasian populations of the tick Ixodesricinus contrasts with marked divergence from north-African populations

Host-parasite interactions may select for significant novel mutations with major evolutionary consequences for both partners. In poor active dispersers such as ticks, their population structures are shaped by their host movements. Here, we use population genetics and phylogeography to investigate the evolutionary history of the most common tick in Europe, Ixodes ricinus, a vector of pathogenic agents causing diseases in humans and animals. Two mitochondrial and four nuclear genes were sequenced for 60 individuals collected on four geographical scales (local, regional, Eurasian and western Palearctic scales). The overall level of nucleotide diversity was low and the variability did not differ at the local, regional or Eurasian scales but increased two fold for the western Palearctic scale. Moreover, the phylogenetic trees indicated an absence of genetic structure among Eurasian ticks, contrasting with a strong differentiation of the north-African ticks which formed a divergent clade. The homogeneity in Eurasian ticks may be explained by gene flows due to passive dispersal of ticks by hosts within a continuous population and recent range expansion of I. ricinus as shown by the fit of the observed frequency distribution of numbers of mismatches between pairwise sequences with the demographic expansion model (Harpending raggedness index, P = 0.74). The genetic divergence of the north-African populations could be explained by genetic drift in these small populations that are geographically isolated and/or selection pressures due to different ecological conditions (seasonal activity, pathogenic agents and hosts communities). The consequences of these results on the epidemiology of vector-borne diseases are discussed.     

Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus Hyalopterus (Hemiptera: Aphididae)

Over the past several decades biologists' fascination with plant-herbivore interactions has generated intensive research into the implications of these interactions for insect diversification. The study of closely related phytophagous insect species or populations from an evolutionary perspective can help illuminate ecological and selective forces that drive these interactions. Here we present such an analysis for aphids in the genus Hyalopterus (Hemiptera: Aphididae), a cosmopolitan group that feeds on plants in the genus Prunus (Rosaceae). Hyalopterus currently contains two recognized species associated with different Prunus species, although the taxonomy and evolutionary history of the group is poorly understood. Using mitochondrial COI sequences, 16S rDNA sequences from the aphid endosymbiont Buchnera aphidicola, and nine microsatellite loci we investigated population structure in Hyalopterus from the most commonly used Prunus host species throughout the Mediterranean as well as in California, where the species H. pruni is an invasive pest. We found three deeply divergent lineages structured in large part by specific associations with plum, almond, and peach trees. There was no evidence that geographic or temporal barriers could explain the overall diversity in the genus. Levels of genetic differentiation are consistent with that typically attributed to aphid species and indicate divergence times older than the domestication of Prunus for agriculture. Interestingly, in addition to their typical hosts, aphids from each of the three lineages were frequently found on apricot trees. Apricot also appears to act as a resource mediated hybrid zone for plum and almond associated lineages. Together, results suggest that host plants have played a role in maintaining host-associated differentiation in Hyalopterus for as long as several million years, despite worldwide movement of host plants and the potential for ongoing hybridization.     

Integrating ancient patterns and current dynamics of insect-plant interactions: Taxonomic and geographic variation in herbivore specialization

The search for pattern in the ecology and evolutionary biology of insect-plant associations has fascinated biologists for centuries.High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted.This review addresses several aspects of local insect specialization,host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence,and ecological ...     

Integrating ancient patterns and current dynamics of insect–plant interactions: Taxonomic and geographic variation in herbivore specialization

Abstract The search for pattern in the ecology and evolutionary biology of insect–plant associations has fascinated biologists for centuries. High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted. This review addresses several aspects of local insect specialization, host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence, and ecological (including “hybrid”) speciation, with special reference to the generation of biodiversity and the geographic and taxonomic identification of “species borders” for swallowtail butterflies (Papilionidae). From ancient phytochemically defined angiosperm affiliations that trace back millions of years to recent and very local specialized populations, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of localized ecological patterns and genetically based evolutionary processes. They have served as a useful group for evaluating the feeding specialization/physiological efficiency hypothesis. They have shown how the abiotic (thermal) environment interacts with host nutrirional suitability to generate “voltinism/suitability” gradients in specialization or preference latitudinally, and geographical mosaics locally. Several studies reviewed here suggest strongly that the oscillation hypothesis for speciation does have considerable merit, but at the same time, some species-level host specializations may lead to evolutionary dead-ends, especially with rapid environmental/habitat changes involving their host plants. Latitudinal gradients in species richness and degree of herbivore feeding specialization have been impacted by recent developments in ecological genetics and evolutionary ecology. Localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious, with simple definitions still debated. However, molecular analyses combined with ecological, ethological and physiological studies, have already begun to unveil some answers for many important ecological/evolutionary questions.     

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

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

Host plant associations in the spider mite Tetranychus urticae (Acari: Tetranychidae): insights from molecular phylogeography

This article integrates studies on the genetic variation of T. urticae populations and the interspecific variation of several tetranychid species. It aims at obtaining insights into the roles of the historical, geographical and ecological factors in the partitioning of variation of species. Two types of molecular markers were used to determine whether the patterns of genetic variation in mites inhabiting different host plants can shed light on the existence of host plant associations. The ribosomal sequences of the second internal transcribed spacer (ITS2), which evolves through concerted evolution, are good indicators of long-term isolation between populations and reveal exceptional homogeneity in a worldwide sampling of T. urticae. The mitochondrial cytochrome oxidase I (COI) sequences do not disclose old divergences related to host plant in this mite but rather suggest recent geographic colonization patterns of the species. Allozyme variation on a fine scale gives some evidence of host associations in the case of citrus trees. However, if any divergence of mites related to this host plant exists, it probably prevails in local populations only and it should not be old enough to be revealed by a phylogenetic analysis of mitochondrial COI sequences. The phyletic constraint in the evolution of feeding specificity in the family Tetra-nychidae is investigated based on a phylogenetic analysis of mitochondrial sequences. The results provide some support for the hypothesis that an evolutionary trend towards polyphagy has occurred in the family. Overall, it seems that the major characteristic of T. urticae is its high colonization potential. Polyphagy has enhanced its successful spread and may have led to connectivity between populations worldwide. © Rapid Science Ltd. 1998     

A role for both ecology and geography as mechanisms of genetic differentiation in specialized butterflies

An important mechanism of speciation for specialized phytophagous insects is host-associated differentiation, in which natural selection drives the evolution of reproductive isolation. Here we use molecular population genetics data to test the hypothesis that regional and local specialization on three alternate hosts restricts gene flow in the Mitoura gryneus species complex of butterflies. Over half of the variation in mitochondrial DNA sequences is explained by host plant association (?_CT = 0.57, P = 0.002) consistent with the hypothesis of host-associated divergence on the three hosts. AFLP analyses revealed the number of clusters of individuals was K = 2, with all individuals associated with one host grouping separately from all other host-associated individuals. Combined with previous experimental results, these findings present evidence of varying levels of differentiation among host associations and identify a role for both isolation in allopatry as well as ecological factors in limiting gene exchange. The Mitoura species complex includes multiple, differentiated lineages at varying stages of divergence, providing an opportunity to examine the multifarious mechanisms that generate biodiversity in phytophagous insects.     

Impacts of climate warming on hybrid zone movement: Geographically diffuse and biologically porous “species borders”

Abstract The ecology and evolutionary biology of insect–plant associations has realized extensive attention, especially during the past 60 years. The classifications (categorical designations) of continuous variation in biodiversity, ranging from global patterns (e.g., latitudinal gradients in species richness/diversity and degree of herbivore feeding specialization) to localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious. Semantic and biosystematic (taxonomical) disagreements sometimes detract from more important ecological and evolutionary processes that drive diversification, the dynamics of gene flow and local extinctions. This review addresses several aspects of insect specialization, host‐associated divergence and ecological (including “hybrid”) speciation, with special reference to the climate warming impacts on species borders of hybridizing swallowtail butterflies (Papilionidae). Interspecific hybrid introgression may result in collapse of multi‐species communities or increase species numbers via homoploid hybrid speciation. We may see diverging, merging, or emerging genotypes across hybrid zones, all part of the ongoing processes of evolution. Molecular analyses of genetic mosaics and genomic dynamics with “divergence hitchhiking”, combined with ecological, ethological and physiological studies of “species porosity”, have already begun to unveil some answers for some important ecological/evolutionary questions. (i) How rapidly can host‐associated divergence lead to new species (and why doesn't it always do so, e.g., resulting in “incomplete” speciation)? (ii) How might “speciation genes” function, and how/where would we find them? (iii) Can oscillations from specialists to generalists and back to specialists help explain global diversity in herbivorous insects? (iv) How could recombinant interspecific hybridization lead to divergence and speciation? From ancient phytochemically defined angiosperm affiliations to recent and very local geographical mosaics, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of ecological patterns and evolutionary processes, including host‐associated genetic divergence, genomic mosaics, genetic hitchhiking and sex‐linked speciation genes. Apparent homoploid hybrid speciation in Papilio appears to have been catalyzed by climate warming‐induced interspecific introgression of some, but not all, species diagnostic traits, reflecting strong divergent selection (discordant), especially on the Z (= X) chromosome. Reproductive isolation of these novel recombinant hybrid genotypes appears to be accomplished via a delayed post‐diapause emergence or temporal isolation, and is perhaps aided by the thermal landscape. Changing thermal landscapes appear to have created (and may destroy) novel recombinant hybrid genotypes and hybrid species.     

HOST‐ASSOCIATED GENETIC DIFFERENTIATION IN PHYTOPHAGOUS INSECTS: GENERAL PHENOMENON OR ISOLATED EXCEPTIONS? EVIDENCE FROM A GOLDENROD‐INSECT COMMUNITY

There is growing awareness of the importance of natural selection in driving genetic divergence and speciation, and several of the most apparent cases of this ecological speciation are provided by the existence of genetically distinct host forms in phytophagous insects. Such examples of host-associated differentiation (HAD) have become increasingly documented, and the implications of this phenomenon for the diversification of insects are becoming widely appreciated. However, instances of HAD remain rare relative to insect diversity and are sparsely distributed both ecologically and taxonomically. We sought to assess the frequency of HAD in a model herbivore community by examining genetic divergence in a variety of herbivores that feed on two closely related and broadly sympatric species of goldenrod (Solidago altissima and S. gigantea). Using mitochondrial DNA and allozyme data, in conjunction with previously published studies, we found that four of nine herbivores exhibited evidence of HAD, including possible host races or cryptic species. Using a range of reasonable substitution rate estimates for cytochrome oxidase I mitochondrial DNA, we found that HAD appears to have proceeded asynchronously across taxa. This pattern, along with the broadly sympatric distribution of host plants and the specialized life histories of the phytophagous insects, is consistent with sympatric divergence in some or all of these taxa. Although further behavioral and ecological study is needed, our survey of HAD in a community of herbivores indicates that ecological (perhaps sympatric) speciation may have been responsible for generating a significant fraction of the extant diversity of phytophagous insects.     

Reproductive strategies of the seabird tick Ixodes uriae (Acari: Ixodidae)

Ixodes uriae is a common ectoparasite of colonial seabirds in the circumpolar areas of both hemispheres. Despite its potential effects on host population dynamics and its role as a vector of pathogens, little is known about the reproductive strategies of this tick under natural conditions. Multiple mating of engorged females has been recorded in several instances, but the resulting paternity of offspring and its potential evolutionary significance have never been evaluated. Here, the paternity of offspring produced by females collected in the field was determined by using 5 polymorphic microsatellite markers. The results indicate that multiple mating in I. uriae can lead to multiple paternity in broods and, given the life history of this parasite, may be related to the adaptive benefits of producing genetically diverse offspring. Copulations took place both before and after the female's blood meal, but most successful fertilizations seemed to occur before engorgement. This suggests that the mating strategies of this tick may have evolved in response to local environmental constraints and, in particular, to the availability of conspecific ticks.     

The underrated importance of predation in transmission ecology of direct lifecycle parasites

Most parasites with complex life cycles exploit trophic webs to pass from host to host in order to develop and, eventually, reproduce. Thus predation constitutes the necessary route for transmission. Conversely, the transmission of parasites that use a single host to develop and reproduce should be, in principle, not particularly affected by host trophic ecology. Here I challenge this view, showing that predation may be relevant also for direct lifecycle parasites. I used a large dataset of fish trophic interactions to investigate if the degree of monogenean species overlap in predators and prey deviated from randomness. I demonstrated that predators and prey often share more monogenean parasite genera than explained by host habitat ecology, geographical distribution and phylogeny. This suggests that predation may play an important role in promoting monogenean host range expansion. In addition, a non‐negligible proportion of considered prey–predator pairs showed a significantly high overlap in their monogenean parasites at the species level. This may indicate a tendency of some monogenean parasites to evolve transmission strategies targeted towards host interactions. If this hypothesis is true, these monogenean parasites would be much more vulnerable to co‐extinction than previously thought. Synthesis Predation is not expected to play an important role in the ecology and evolution of simple life cycle parasites. Yet, several predator fish tend to share with their prey more monogenean parasites than one would expect predicted from their geographical distribution, habitat preference, and or phylogenetic relationships. This suggests that some monogenean parasites have evolved transmission strategies more targeted towards host interactions than towards species‐specific traits. If this hypothesis is supported, it would have strong implications on host–parasite evolutionary ecology, primarily, suggesting the existence of peculiar situations where some parasites have evolved high specialized host finding behaviors to expand their host range.     

Interactions retain the co‐phylogenetic matching that communities lost

Both species and their interactions are affected by changes that occur at evolutionary time‐scales, and these changes shape both ecological communities and their phylogenetic structure. That said, extant ecological community structure is contingent upon random chance, environmental filters and local effects. It is therefore unclear how much ecological signal local communities should retain. Here we show that, in a host–parasite system where species interactions vary substantially over a continental gradient, the ecological significance of individual interactions is maintained across different scales. Notably, this occurs despite the fact that observed community variation at the local scale frequently tends to weaken or remove community‐wide phylogenetic signal. When considered in terms of the interplay between community ecology and coevolutionary theory, our results demonstrate that individual interactions are capable and indeed likely to show a consistent signature of past evolutionary history even when woven into communities that do not.     

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

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

Architecture of an antagonistic tree/fungus network: the asymmetric influence of past evolutionary history

Background

Compartmentalization and nestedness are common patterns in ecological networks. The aim of this study was to elucidate some of the processes shaping these patterns in a well resolved network of host/pathogen interactions.

Methology/Principal Findings

Based on a long-term (1972–2005) survey of forest health at the regional scale (all French forests; 15 million ha), we uncovered an almost fully connected network of 51 tree taxa and 157 parasitic fungal species. Our analyses revealed that the compartmentalization of the network maps out the ancient evolutionary history of seed plants, but not the ancient evolutionary history of fungal species. The very early divergence of the major fungal phyla may account for this asymmetric influence of past evolutionary history. Unlike compartmentalization, nestedness did not reflect any consistent phylogenetic signal. Instead, it seemed to reflect the ecological features of the current species, such as the relative abundance of tree species and the life-history strategies of fungal pathogens. We discussed how the evolution of host range in fungal species may account for the observed nested patterns.

Conclusion/Significance

Overall, our analyses emphasized how the current complexity of ecological networks results from the diversification of the species and their interactions over evolutionary times. They confirmed that the current architecture of ecological networks is not only dependant on recent ecological processes.     

PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification.

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus

Historical contingency and determinism are often cast as opposing paradigms under which evolutionary diversification operates. It may be, however, that both factors act together to promote evolutionary divergence, although there are few examples of such interaction in nature. We tested phylogenetic predictions of an explicit historical model of divergence (double invasions of freshwater by marine ancestors) in sympatric species of three-spined sticklebacks (Gasterosteus aculeatus) where determinism has been implicated as an important factor driving evolutionary novelty. Microsatellite DNA variation at six loci revealed relatively low genetic variation in freshwater populations, supporting the hypothesis that they were derived by colonization of freshwater by more diverse marine ancestors. Phylogenetic and genetic distance analyses suggested that pairs of sympatric species have evolved multiple times, further implicating determinism as a factor in speciation. Our data also supported predictions based on the hypothesis that the evolution of sympatric species was contingent upon 'double invasions' of postglacial lakes by ancestral marine sticklebacks. Sympatric sticklebacks, therefore, provide an example of adaptive radiation by determinism contingent upon historical conditions promoting unique ecological interactions, and illustrate how contingency and determinism may interact to generate geographical variation in species diversity     

Population structure and the co-evolution between social parasites and their hosts

Co-evolutionary trajectories of host-parasite interactions are strongly affected by the antagonists' evolutionary potential, which in turn depends on population sizes as well as levels of recombination, mutation, and gene flow. Under similar selection pressures, the opponent with the higher evolutionary rate is expected to lead the co-evolutionary arms race and to develop local adaptations. Here, we use mitochondrial DNA sequence data and microsatellite markers to assess the amount of genetic variability and levels of gene flow in two host-parasite systems, each consisting of an ant social parasite--the European slavemaker Harpagoxenus sublaevis and the North American slavemaker Protomognathus americanus--and its two main host species. Our population genetic analyses revealed limited gene flow between individual populations of both host and parasite species, allowing for a geographic mosaic of co-evolution. In a between-system comparison, we found less genetic variability and more pronounced structure in Europe, where previous behavioural studies demonstrated strong local adaptation. Within the European host-parasite system, the larger host species Leptothorax acervorum exhibited higher levels of both genetic variability and gene flow, and previous field data showed that it is less affected by the social parasite H. sublaevis than the smaller host Leptothorax muscorum, which has genetically depleted and isolated populations. In North America, the parasite P. americanus showed higher levels of gene flow between sites, but overall less genetic diversity than its hyper-variable main host species, Temnothorax longispinosus. Interestingly, recent ecological and chemical studies demonstrated adaptation of P. americanus to local host populations, indicating the importance of migration in co-evolutionary interactions.