The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system

The geographical mosaic theory of coevolution predicts differences in the advance or trajectory of the coevolutionary process between local communities due to their composition and the strength of ecological selection pressures through competition and resource availability. In this study, we investigate local co-adaptation in different populations of a social parasite. We conducted cross-fostering experiments to test for interpopulational differences in raiding efficiency between various populations of a slave-making ant and the defence abilities of local hosts. Here, we demonstrate that the success of raids strongly depends on the combination of populations of the parasite Harpagoxenus sublaevis and its host Leptothorax acervorum, indicating very localized coevolution. We found no absolute differences between slave-maker populations; the outcome of an encounter depended more on whether the two opponents occur in sympatry or allopatry. Furthermore, this study supports the results of our earlier work, that the unparasitized English L. acervorum population is most aggressive against the parasite.     

Migratory behavior of birds affects their coevolutionary relationship with blood parasites

Host traits, such as migratory behavior, could facilitate the dispersal of disease-causing parasites, potentially leading to the transfer of infections both across geographic areas and between host species. There is, however, little quantitative information on whether variation in such host attributes does indeed affect the evolutionary outcome of host-parasite associations. Here, we employ Leucocytozoon blood parasites of birds, a group of parasites closely related to avian malaria, to study host-parasite coevolution in relation to host behavior using a phylogenetic comparative approach. We reconstruct the molecular phylogenies of both the hosts and parasites and use cophylogenetic tools to assess whether each host-parasite association contributes significantly to the overall congruence between the two phylogenies. We find evidence for a significant fit between host and parasite phylogenies in this system, but show that this is due only to associations between nonmigrant parasites and their hosts. We also show that migrant bird species harbor a greater genetic diversity of parasites compared with nonmigrant species. Taken together, these results suggest that the migratory habits of birds could influence their coevolutionary relationship with their parasites, and that consideration of host traits is important in predicting the outcome of coevolutionary interactions.     

Antagonistic coevolution between a bacterium and a bacteriophage

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

Advice of the rose: experimental coevolution of a trematode parasite and its snail host

Understanding host-parasite coevolution requires multigenerational studies in which changes in both parasite infectivity and host susceptibility are monitored. We conducted a coevolution experiment that examined six generations of interaction between a freshwater snail (Potamopyrgus antipodarum) and one of its common parasites (the sterilizing trematode, Microphallus sp.). In one treatment (recycled), the parasite was reintroduced into the same population of host snails. In the second treatment (lagged), the host snails received parasites from the recycled treatment, but the addition of these parasites did not begin until the second generation. Hence any parasite-mediated genetic changes of the host in the lagged treatment were expected to be one generation behind those in the recycled treatment. The lagged treatment thus allowed us to test for time lags in parasite adaptation, as predicted by the Red Queen model of host-parasite coevolution. Finally, in the third treatment (control), parasites were not added. The results showed that parasites from the recycled treatment were significantly more infective to snails from the lagged treatment than from the recycled treatment. In addition, the hosts from the recycled treatment diverged from the control hosts with regard to their susceptibility to parasites collected from the field. Taken together, the results are consistent with time lagged, frequency-dependent selection and rapid coevolution between hosts and parasites.     

Relative number of generations of hosts and parasites does not influence parasite local adaptation in coevolving populations of bacteria and phages

A potential consequence of host-parasite coevolution in spatially structured populations is parasite local adaptation: local parasites perform better than foreign parasites on their local host populations. It has been suggested that the generally shorter generation times of parasites compared with their hosts contributes to parasites, rather than hosts, being locally adapted. We tested the hypothesis that relative generation times of hosts and parasites affect local adaptation of hosts and parasites, using the bacterium Pseudomonas fluorescens and a lytic phage as host and parasite, respectively. Generation times were not directly manipulated, but instead one of the coevolving partners was regularly removed and replaced with a population from an earlier time point. Thus, one partner underwent more generations than the other. Manipulations were carried out at both early and later periods of coevolutionary interactions. At early stages of coevolution, host and parasites that underwent relatively more generations displayed higher levels of resistance and infectivity, respectively. However, the relative number of generations that bacteria and phages underwent did not change the level of local adaptation relative to control populations. This is likely because generalist hosts and parasites are favoured during early stages of coevolution, preventing local adaptation. By contrast, at later stages manipulations had no effect on either average levels of resistance or infectivity, or alter the level of local adaptation relative to the controls, possibly because traits other than resistance and infectivity were under strong selection. Taken together, these data suggest that the relative generation times of hosts and parasites may not be an important determinant of local adaptation in this system.     

Causal mechanisms underlying host specificity in bat ectoparasites

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.     

On genetic specificity in symbiont-mediated host-parasite coevolution

Existing theory of host-parasite interactions has identified the genetic specificity of interaction as a key variable affecting the outcome of coevolution. The Matching Alleles (MA) and Gene For Gene (GFG) models have been extensively studied as the canonical examples of specific and non-specific interaction. The generality of these models has recently been challenged by uncovering real-world host-parasite systems exhibiting specificity patterns that fit neither MA nor GFG, and by the discovery of symbiotic bacteria protecting insect hosts against parasites. In the present paper we address both challenges, simulating a large number of non-canonical models of host-parasite interactions that explicitly incorporate symbiont-based host resistance. To assess the genetic specialisation in these hybrid models, we develop a quantitative index of specificity applicable to any coevolutionary model based on a fitness matrix. We find qualitative and quantitative effects of host-parasite and symbiont-parasite specificities on genotype frequency dynamics, allele survival, and mean host and parasite fitnesses.     

Genetic basis of infectivity evolution in a bacteriophage

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

Coevolution between slave-making ants and their hosts: host specificity and geographical variation

We explored the impact of a slave-making ant, Protomognathus americanus, on two of its hosts, Leptothorax longispinosus and L. ambiguus. We showed that, on average, slave-maker colonies conduct raids on 2.7 L. longispinosus and 1.4 L. ambiguus nests in a single year. The more common host, L. longispinosus, survives raiding and colony-founding events in a third of the cases, but the less common host rarely survives attacks from the slave-makers. We compare our results, collected in Vermont, to a study conducted in New York where the slave-maker pressure is much stronger. Our results suggest that in Vermont the slave-maker has a sparing strategy when raiding L. longispinosus, but not when raiding L. ambiguus. Thus coevolution between slave-making ants and their hosts shows host specificity and geographical variation.     

The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.     

The impact of environmental change on host-parasite coevolutionary dynamics

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

Specificity of host-parasite relations between arthropods and terrestrial vertebrates

Specificity of partners in host-parasite system is one of its main characteristics. Unfortunately this term has different senses in scientific literature. In everyday practice one judges an extent of host specificity of a parasite mainly by indices of its occurrence and abundance on different host species. An occurrence of parasites in nature reflects general result of complex eco-physiological interrelationships between partners in hostparasite system. Specificity of parasites in a choice of hosts may depend on a belonging of the latter to certain taxa (phylogenetic specificity), or on biotic and abiotic factors (ecological specificity). In arthropods, the phylogentic specificity and coevolution are characteristic to a greater extent for permanent hosts (lice, Mallophaga, cheyletoid and feather mites). A coevolutionaryphylogenesis is disturbed by transfers of parasites onto new hosts, by different rates of speciation in filial lines or by an extinction of several parasite taxa. In temporary parasites different forms of ecological specificity are prevalent. A host specificity is expressed to the lesser extent in mosquitoes, horseflies and in other blood-sucking Diptera. In temporary parasites with a long-term feeding (ticks) coevolutionary sequences are relatively rare, because this parasites had to adapt not only to a life on host, but also to a lesser stable environment. In some nest-burrow bloodsuckers (fleas, gamasid mites and argasid ticks) the ecological specificity is shown no by their relations with certain host species, but by an associations with habitats occupied by hosts (burrow, nests, caves). In relation with a high dynamics of host-parasite system, a specificity of its partners is comparative and it is kept up only under specific ecological conditions.     

THE EFFECTS OF HOST GENOTYPE AND SPATIAL DISTRIBUTION ON TREMATODE PARASITISM IN A BIVALVE POPULATION

A basic assumption underlying models of host-parasite coevolution is the existence of additive genetic variation among hosts for resistance to parasites. However, estimates of additive genetic variation are lacking for natural populations of invertebrates. Testing this assumption is especially important in view of current models that suggest parasites may be responsible for the evolution of sex, such as the Red Queen hypothesis. This hypothesis suggests that the twofold reproductive disadvantage of sex relative to parthenogenesis can be overcome by the more rapid production of rare genotypes resistant to parasites. Here I present evidence of significant levels of additive genetic variance in parasite resistance for an invertebrate host-parasite system in nature. Using families of the bivalve mollusc, Transennella tantilla, cultured in the laboratory, then exposed to parasites in the field, I quantified heritable variation in parasite resistance under natural conditions. The spatial distribution of outplanted hosts was also varied to determine environmental contributions to levels of parasite infection and to estimate potential interactions of host genotype with environment. The results show moderate but significant levels of heritability for resistance to parasites (h² = 0.36). The spatial distribution of hosts also significantly influenced parasite prevalence such that increased host aggregation resulted in decreased levels of parasite infection. Family mean correlations across environments were positive, indicating no genotype-environment interaction. Therefore, these results provide support for important assumptions underlying coevolutionary models of host-parasite systems.     

Antagonistic coevolution limits population persistence of a virus in a thermally deteriorating environment

Understanding the conditions under which rapid evolutionary adaptation can prevent population extinction in deteriorating environments (i.e. evolutionary rescue) is a crucial aim in the face of global climate change. Despite a rapidly growing body of work in this area, little attention has been paid to the importance of interspecific coevolutionary interactions. Antagonistic coevolution commonly observed between hosts and parasites is likely to retard evolutionary rescue because it often reduces population sizes, and results in the evolution of costly host defence and parasite counter-defence. We used experimental populations of a bacterium Pseudomonas fluorescens SBW25 and a bacteriophage virus (SBW25Φ2), to study how host-parasite coevolution impacts viral population persistence in the face of gradually increasing temperature, an environmental stress for the virus but not the bacterium. The virus persisted much longer when it evolved in the presence of an evolutionarily constant host genotype (i.e. in the absence of coevolution) than when the bacterium and virus coevolved. Further experiments suggest that both a reduction in population size and costly infectivity strategies contributed to viral extinction as a result of coevolution. The results highlight the importance of interspecific evolutionary interactions for the evolutionary responses of populations to global climate change.     

The mode of host-parasite interaction shapes coevolutionary dynamics and the fate of host cooperation

Antagonistic coevolution between hosts and parasites can have a major impact on host population structures, and hence on the evolution of social traits. Using stochastic modelling techniques in the context of bacteria-virus interactions, we investigate the impact of coevolution across a continuum of host-parasite genetic specificity (specifically, where genotypes have the same infectivity/resistance ranges (matching alleles, MA) to highly variable ranges (gene-for-gene, GFG)) on population genetic structure, and on the social behaviour of the host. We find that host cooperation is more likely to be maintained towards the MA end of the continuum, as the more frequent bottlenecks associated with an MA-like interaction can prevent defector invasion, and can even allow migrant cooperators to invade populations of defectors.     

The role of phylogeny and ecology in experimental host specificity: insights from a eugregarine-host system

The degree to which parasites use hosts is fundamental to host-parasite coevolution studies, yet difficult to assess and interpret in an evolutionary manner. Previous assessments of parasitism in eugregarine-host systems suggest high degrees of host specificity to particular host stages and host species; however, rarely have the evolutionary constraints on host specificity been studied experimentally. A series of experimental infections were conducted to determine the extent of host stadium specificity (larval vs. adult stage) and host specificity among 6 tenebrionid host species and 5 eugregarine parasite species. Eugregarines from all host species infected both the larva and adult stages of the host, and each parasite taxa colonized several host species (Tribolium spp. and Palorus subdepressus). Parasite infection patterns were not congruent with host phylogeny, suggesting that host phylogeny is not a significant predictor of host-parasite interactions in this system. However, the 2 host stages produced significantly different numbers of parasite propagules, indicating that ecological factors may be important determinants of host specificity in this host-parasite system. While field infections reflect extant natural infection patterns of parasites, experimental infections can demonstrate potential host-parasite interactions, which aids in identifying factors that may be significant in shaping future host-parasite interactions.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

The role of epistasis on the evolution of recombination in host-parasite coevolution

Antagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.     

Host population bottlenecks drive parasite extinction during antagonistic coevolution

Host–parasite interactions are often characterized by large fluctuations in host population size, and we investigated how such host bottlenecks affected coevolution between a bacterium and a virus. Previous theory suggests that host bottlenecks should provide parasites with an evolutionary advantage, but instead we found that phages were rapidly driven to extinction when coevolving with hosts exposed to large genetic bottlenecks. This was caused by the stochastic loss of sensitive bacteria, which are required for phage persistence and infectivity evolution. Our findings emphasize the importance of feedbacks between ecological and coevolutionary dynamics, and how this feedback can qualitatively alter coevolutionary dynamics.