Parasite local adaptation in a geographic mosaic

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.     

Coevolution across landscapes: a spatially explicit model of parasitoid-host coevolution

The geographic mosaic theory of coevolution suggests that population spatial structure may have a strong impact on coevolutionary dynamics. Therefore, coevolution must be studied across geographic scales, not just in single populations. To examine the impact of movement rate on coevolutionary dynamics, we developed a spatially explicit model of host–parasitoid coevolution. We described space as a coupled-map lattice and assumed that resistance (defined as the ability of a host to encapsulate a parasitoid egg) and virulence (defined as the successful parasitization of a host) traits were graded and costly. The model explicitly detailed population and evolutionary dynamics. When holding all parameters constant and varying only the movement rate of the host and parasitoid, profoundly different dynamics were observed. We found that fluctuations in the mean levels of resistance and virulence in the global population were greatest when the movement rate of the host and parasitoid was high. In addition, we found that the variation in resistance and virulence levels among neighboring patches was greatest when the movement rates of the host and parasitoid was low. However, as the distance among patches increased, so did the variation in resistance and virulence levels regardless of movement rate. These generalizations did not hold when spatial patterns in the distribution of resistance and virulence traits, such as spirals, were observed. Finally, we found that the evolution of resistance and virulence caused the abundance of hosts to increase and the abundance of parasitoids to decrease. As a result, the spatial distribution of hosts and parasitoids was influenced.     

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

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

Dos and don'ts of testing the geographic mosaic theory of coevolution

The geographic mosaic theory of coevolution is stimulating much new research on interspecific interactions. We provide a guide to the fundamental components of the theory, its processes and main predictions. Our primary objectives are to clarify misconceptions regarding the geographic mosaic theory of coevolution and to describe how empiricists can test the theory rigorously. In particular, we explain why confirming the three main predicted empirical patterns (spatial variation in traits mediating interactions among species, trait mismatching among interacting species and few species-level coevolved traits) does not provide unequivocal support for the theory. We suggest that strong empirical tests of the geographic mosaic theory of coevolution should focus on its underlying processes: coevolutionary hot and cold spots, selection mosaics and trait remixing. We describe these processes and discuss potential ways each can be tested.     

Host-parasitoid association and diffuse coevolution: when to be a generalist?

In host-parasitoid communities, hosts are subjected to selective pressures from numerous parasitoid species, and parasitoids may attack several host species. The specificity of host resistance and parasitoid virulence is thus a key factor in host-parasitoid coevolution. A continuum of strategies exists, from strict specificity to a generalist strategy. The optimal level of specificity may differ in host and parasitoid. I investigated the optimal level of resistance specificity using a model in which the host could be attacked by two parasitoid species, with variable levels of defense specificity. The fitness of a parasitoid attacking two host species with different levels of virulence specificity was also modeled. Finally, a fluctuating environment was simulated by introducing variable probabilities of encounters between antagonistic species over several generations. If the frequency of encounters with the antagonistic species is fixed, then both host and parasitoid gain from a strategy of exclusive specialization toward the most frequent antagonist. If the frequency of encounters fluctuates between generations, generalist host resistance and partially specialist parasitoid virulence are favored. Generalist host resistance may be considered to be a bet-hedging response to an unpredictable environment. This asymmetry in host-parasitoid coevolution may account for some of the genetic structures observed in the field for host-parasitoid associations.     

Is parasitoid virulence against multiple hosts adaptive or constrained by phylogeny? A study of Leptopilina spp. (Hymenoptera: Figitidae)/Drosophila (Diptera: Drosophilidae) interactions

Summary. Some insects can develop immune resistance to koinobiont parasitoids. Reciprocally, adaptation to host immunology is critical for parasitoid success. Phylogenetic inertia and correlations between virulence against different hosts can act as constraints preventing these adaptations. Insights on these constraints may be obtained from the analysis of patterns of variations in the interactions at the species or genus level. Multivariate phylogenetic comparative methods were applied to virulence traits of 13 parasitoid strains of Leptopilina spp. (Hymenoptera: Figitidae) on five host strains of the Drosophila melanogaster species subgroup (Diptera Drosophilidae). Independent contrasts of virulence were calculated and principal component analysis (PCA) was performed on the independent contrasts to estimate the dimensionality of the interactions. Most of the variation of virulence was associated with the first component of the PCA (62.2%). But a significant proportion was explained by the second and third components, suggesting specific interactions. Strain–strain reciprocal specificity was observed in several pairs of host–parasitoid species. Significant phylogenetic inertia was observed on parasitoid virulence, but only at the genus level and only against hosts of intermediate resistance (phylogenetic R² between 0.62 and 0.85). Some parts of the interaction matrix exhibited specific interactions and others were fixed due to ancestral non-specific virulence (or avirulence). The results were interpreted viewing virulence as a threshold trait determined by underlying liability. When liability is far from the threshold, virulence is fixed. When liability is close to the threshold, virulence varies specifically and reciprocal adaptations can take place. These phylogenetic constraints may lead to a scenario of escape and radiation coevolution in the host–parasitoid system.     

Ample genetic variation but no evidence for genotype specificity in an all‐parthenogenetic host–parasitoid interaction

Antagonistic coevolution between hosts and parasites can result in negative frequency‐dependent selection and may thus be an important mechanism maintaining genetic variation in populations. Negative frequency‐dependence emerges readily if interactions between hosts and parasites are genotype‐specific such that no host genotype is most resistant to all parasite genotypes, and no parasite genotype is most infective on all hosts. Although there is increasing evidence for genotype specificity in interactions between hosts and pathogens or microparasites, the picture is less clear for insect host–parasitoid interactions. Here, we addressed this question in the black bean aphid (Aphis fabae) and its most important parasitoid Lysiphlebus fabarum. Because both antagonists are capable of parthenogenetic reproduction, this system allows for powerful tests of genotype × genotype interactions. Our test consisted of exposing multiple host clones to different parthenogenetic lines of parasitoids in all combinations, and this experiment was repeated with animals from four different sites. All aphids were free of endosymbiotic bacteria known to increase resistance to parasitoids. We observed ample genetic variation for host resistance and parasitoid infectivity, but there was no significant host clone × parasitoid line interaction, and this result was consistent across the four sites. Thus, there is no evidence for genotype specificity in the interaction between A. fabae and L. fabarum, suggesting that the observed variation is based on rather general mechanisms of defence and attack.     

Two non-linked genes for specific virulence of Leptopilina boulardi against Drosophila melanogaster and D. yakuba

The developmental success of Leptopilina boulardi parasitoids within host species of the melanogaster subgroup is determined mainly by their ability to suppress the host immune reaction (virulence). Host resistance and parasitoid virulence are genetically variable in both partners. A gene for specific resistance against L. boulardi (Rlb) has been identified in Drosophila melanogaster, and a gene for the immune suppression (IS) of D. melanogaster has been identified in L. boulardi. To understand the evolution of the IS gene, we determined its specificity regarding potential hosts of the melanogaster subgroup. It did not affect the virulence against any other species of the melanogaster subgroup and was called ISm for immune suppression of D. melanogaster. Another gene (ISy), non-linked to the gene ISm, was characterized for the specific immune suppression of D. yakuba. These results suggesting that natural selection for virulence against one host species does not influence the evolution of virulence against another will allow us to develop pertinent hypotheses concerning the evolution of this character which is expected to drive the evolution of the parasitoid toward narrow host specialization. This revised version was published online in July 2006 with corrections to the Cover Date.     

A model for the coevolution of resistance and virulence in coupled host—parasitoid interactions

A coevolutionary model is developed of the interaction between a host and an internal parasitoid, where the outcome of parasitism depends upon the extent to which individual hosts invest in resistance mechanisms and individual parasitoids in countermeasures (virulence). The host and parasitoid are assumed to have coupled population dynamics (of Nicholson–Bailey form) and to be composed of a series of asexual clones with different levels of resistance and virulence. Investment in resistance and virulence mechanisms is assumed to be costly. The model has two main outcomes. First, if resistance is relatively costly compared to virulence, the host may be selected not to invest in resistance mechanisms despite parasitoid investment in virulence, in effect trading off the risks of parasitism against the savings in costs. A number of cases which appear to correspond to this result have been reported. Second, for most other feasible parameter values, an arms race occurs between host and parasitoid, until effective resistance becomes so costly that the host abandons defence. This abandonment is followed by a reduction in parasitoid virulence and the cycle begins again. These cycles may explain reports of persistent additive genetic variation in resistance and virulence, and may also contribute towards population dynamic stability.     

High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster

Among the most common parasites of Drosophila in nature are parasitoid wasps, which lay their eggs in fly larvae and pupae. D. melanogaster larvae can mount a cellular immune response against wasp eggs, but female wasps inject venom along with their eggs to block this immune response. Genetic variation in flies for immune resistance against wasps and genetic variation in wasps for virulence against flies largely determines the outcome of any fly-wasp interaction. Interestingly, up to 90% of the variation in fly resistance against wasp parasitism has been linked to a very simple mechanism: flies with increased constitutive blood cell (hemocyte) production are more resistant. However, this relationship has not been tested for Drosophila hosts outside of the melanogaster subgroup, nor has it been tested across a diversity of parasitoid wasp species and strains. We compared hemocyte levels in two fly species from different subgroups, D. melanogaster and D. suzukii, and found that D. suzukii constitutively produces up to five times more hemocytes than D. melanogaster. Using a panel of 24 parasitoid wasp strains representing fifteen species, four families, and multiple virulence strategies, we found that D. suzukii was significantly more resistant to wasp parasitism than D. melanogaster. Thus, our data suggest that the relationship between hemocyte production and wasp resistance is general. However, at least one sympatric wasp species was a highly successful infector of D. suzukii, suggesting specialists can overcome the general resistance afforded to hosts by excessive hemocyte production. Given that D. suzukii is an emerging agricultural pest, identification of the few parasitoid wasps that successfully infect D. suzukii may have value for biocontrol.     

Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie

BACKGROUND: Coevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species. PRESENTATION OF THE HYPOTHESIS: When more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race. TESTING THE HYPOTHESIS: We propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization. IMPLICATIONS OF THE HYPOTHESIS: Genetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.     

The evolutionary significance of parasitism: do parasite‐driven genetic dynamics occur ex silico?

It has long been recognized that reciprocal antagonism might lock host and parasite populations into a process of constant change, adapting and reacting in open‐ended coevolution. A significant body of theory supports this intuition: dynamic genetic polymorphisms are a common outcome of computer simulations of host–parasite coevolution. These in silico experiments have also shown that dynamical interactions could be responsible for high levels of genetic diversity in host populations, and even be the principle determinant of rates of genetic recombination and sexuality. The evolutionary significance of parasitism depends on the strength and prevalence of parasite‐mediated selection in nature. Here I appraise whether parasitism is a pervasive agent of evolutionary change by detailing empirical evidence for selection. Although there is considerable evidence of genetic variation for resistance, and hence the potential for selection, direct observation of parasite‐driven genetic change is lacking.     

The maintenance of genetic diversity under host–parasite coevolution in finite,structured populations

As a corollary to the Red Queen hypothesis, host–parasite coevolution has been hypothesized to maintain genetic variation in both species. Recent theoretical work, however, suggests that reciprocal natural selection alone is insufficient to maintain variation at individual loci. As highlighted by our brief review of the theoretical literature, models of host–parasite coevolution often vary along multiple axes (e.g. inclusion of ecological feedbacks or abiotic selection mosaics), complicating a comprehensive understanding of the effects of interacting evolutionary processes on diversity. Here we develop a series of comparable models to explore the effect of interactions between spatial structures and antagonistic coevolution on genetic diversity. Using a matching alleles model in finite populations connected by migration, we find that, in contrast to panmictic populations, coevolution in a spatially structured environment can maintain genetic variation relative to neutral expectations with migration alone. These results demonstrate that geographic structure is essential for understanding the effect of coevolution on biological diversity.     

The coevolutionary dynamics of antagonistic interactions mediated by quantitative traits with evolving variances

Quantitative traits frequently mediate coevolutionary interactions between predator and prey or parasite and host. Previous efforts to understand and predict the coevolutionary dynamics of these interactions have generally assumed that standing genetic variation is fixed or absent altogether. We develop a genetically explicit model of coevolution that bridges the gap between these approaches by allowing genetic variation itself to evolve. Analysis of this model shows that the evolution of genetic variance has important consequences for the dynamics and outcome of coevolution. Of particular importance is our demonstration that coevolutionary cycles can emerge in the absence of stabilizing selection, an outcome not possible in previous models of coevolution mediated by quantitative traits. Whether coevolutionary cycles evolve depends upon the strength of selection, the number of loci, and the rate of mutation in each of the interacting species. Our results also generate novel predictions for the expected sign and magnitude of linkage disequilibria in each species.     

Do parasitoid preferences for different host species match virulence?

Abstract.  Leptopilina boulardi is a parasitoid wasp specialist of Drosophila larvae of the melanogaster subgroup. In Mediterranean areas, natural populations are highly virulent against their main host Drosophila melanogaster . In Congo, populations are less virulent against D. melanogaster but are able to develop successfully inside the tropical African species Drosophila yakuba . Host preferences are compared between two laboratory isofemale lines of L. boulardi , obtained from populations of Congo and Tunisia, respectively, and differing in virulence levels against D. melanogaster and D. yakuba . Host selection is studied by offering female parasitoids a choice between larvae of the two host species. In agreement with optimal foraging models, the line highly virulent against D. melanogaster shows a clear preference for this host species. The other line, less virulent against D. melanogaster but more virulent against D. yakuba , prefers to oviposit on D. yakuba . Such preferences can be observed after a period of host-patch exploitation only, suggesting that experience plays an important role in the host-selection process. These results evidence the existence of intraspecific variability in preference between two host species in L. boulardi , a major requisite in theoretical models of parasite specialization by the host. They also sustain the hypothesis that intraspecific variation in parasitoid preferences between host species might mirror intraspecific variation in virulence.     

GENOTYPIC VARIATION AND THE ROLE OF DEFENSIVE ENDOSYMBIONTS IN AN ALL-PARTHENOGENETIC HOST–PARASITOID INTERACTION

Models of host–parasite coevolution predict pronounced genetic dynamics if resistance and infectivity are genotype-specific or associated with costs, and if selection is fueled by sufficient genetic variation. We addressed these assumptions in the black bean aphid, Aphis fabae , and its parasitoid Lysiphlebus fabarum . Parasitoid genotypes differed in infectivity and host clones exhibited huge variation for susceptibility. This variation occurred at two levels. Clones harboring Hamiltonella defensa , a bacterial endosymbiont known to protect pea aphids against parasitoids, enjoyed greatly reduced susceptibility, yet clones without H. defensa also exhibited significant variation. Although there was no evidence for genotype-specificity in the H. defensa -free clones' interaction with parasitoids, we found such evidence in clones containing the bacterium. This suggests that parasitoid genotypes differ in their ability to overcome H. defensa , resulting in an apparent host × parasitoid genotype interaction that may in fact be due to an underlying symbiont × parasitoid genotype interaction. Aphid susceptibility to parasitoids correlated negatively with fecundity and rate of increase, due to H. defensa -bearing clones being more fecund on average. Hence, possessing symbionts may also be favorable in the absence of parasitoids, which raises the question why H. defensa does not go to fixation and highlights the need to develop new models to understand the dynamics of endosymbiont-mediated coevolution.     

THE POTENTIAL FOR COEVOLUTION IN A HOST-PARASITOID SYSTEM. II. GENETIC VARIATION WITHIN A POPULATION OF WASPS IN THE ABILITY TO PARASITIZE AN APHID HOST

Much of the study of coevolution has focused on the adaptations that have resulted from interactions between species. For reciprocal evolution to occur, there must be genetic variation in each species for traits that directly affect their interaction. Here I report evidence of significant additive genetic variance within a population of parasitic wasps in the ability to successfully parasitize an aphid host. These data, combined with companion work documenting clonal variation in a population of aphids from the same site, provide evidence that within the same population both a host and its parasitoid have the potential for specific and reciprocal genetic interactions.     

Increasing productivity accelerates host-parasite coevolution

Host-parasite coevolution is believed to influence a range of evolutionary and ecological processes, including population dynamics, evolution of diversity, sexual reproduction and parasite virulence. The impact of coevolution on these processes will depend on its rate, which is likely to be affected by the energy flowing through an ecosystem, or productivity. We addressed how productivity affected rates of coevolution during a coevolutionary arms race between experimental populations of bacteria and their parasitic viruses (phages). As hypothesized, the rate of coevolution between bacterial resistance and phage infectivity increased with increased productivity. This relationship can in part be explained by reduced competitiveness of resistant bacteria in low compared with high productivity environments, leading to weaker selection for resistance in the former. The data further suggest that variation in productivity can generate variation in selection for resistance across landscapes, a result that is crucial to the geographic mosaic theory of coevolution.     

Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid

Parasitoids that must kill the host to complete their development are expected to evolve towards increased virulence. In some conditions however Leptopilina boulardi loses its ability to counteract the host immune reaction. This trait is determined by major genes. For each host species there is a specific gene for immune suppression by the parasite. Here the geographic variations of the immunosuppressive gene frequencies are investigated in relation to the distribution of the host species. The necessity to deal with host immunity is a major constraint on the host range of L. boulardi. Against Drosophila simulans and D. yakuba. the presence of the immunosuppressive allele is correlated with the presence of the host species in the locality. Against D. melanogaster. the data suggest that this gene is counterselected when the parasite is exposed to numerous host species. This counterselection is explained by the existence of a cost of immunosuppressive genes. Against D. yakuba, this cost was evaluated in population cages as a selective coefficient of s = -0.20. The cost differs between the genes. Against D. melanogaster, it was not significant in population cage conditions. The parasitoid invests more in the suppression of the D. yakuba reaction than that of D. melanogaster. This variation of the investment in immunosuppression is discussed within the framework of the adaptive budget theory.