Host-parasite Coevolutionary Dynamics Research Articles

Geography, phylogeny and host switch drive the coevolution of parasitic Gyrodactylus flatworms and their hosts

BackgroundGyrodactylus is a lineage of monogenean flatworm ectoparasites exhibiting many features that make them a suitable model to study the host-parasite coevolutionary dynamics. Previous coevolutionary studies of this lineage mainly relied on low-power datasets (a small number of samples and a single molecular marker) and (now) outdated algorithms.MethodsTo investigate the coevolutionary relationship of gyrodactylids and their fish hosts in high resolution, we used complete mitogenomes (including two newly sequenced Gyrodactylus species), a large number of species in the single-gene dataset, and four different coevolutionary algorithms.ResultsThe overall coevolutionary fit between the parasites and hosts was consistently significant. Multiple indicators confirmed that gyrodactylids are generally highly host-specific parasites, but several species could parasitize either multiple (more than 5) or phylogenetically distant fish hosts. The molecular dating results indicated that gyrodactylids tend to evolve towards high host specificity. Speciation by host switch was identified as a more important speciation mode than co-speciation. Assuming that the ancestral host belonged to Cypriniformes, we inferred four major host switch events to non-Cypriniformes hosts (mostly Salmoniformes), all of which occurred deep in the evolutionary history. Despite their relative rarity, these events had strong macroevolutionary consequences for gyrodactylid diversity. For example, in our dataset, 57.28% of all studied gyrodactylids parasitized only non-Cypriniformes hosts, which implies that the evolutionary history of more than half of all included lineages could be traced back to these major host switch events. The geographical co-occurrence of fishes and gyrodactylids determined the host use by these gyrodactylids, and geography accounted for most of the phylogenetic signal in host use.ConclusionsOur findings suggest that the coevolution of Gyrodactylus flatworms and their hosts is largely driven by geography, phylogeny, and host switches.Graphical

Host and parasite functional morphology jointly explain parasite specificity

Abstract Host–parasite coevolution is a major diversifying force. However, while the genetic determinants of host–parasite coevolution have received substantial attention, it remains unresolved how morphological adaptations contribute to host–parasite coevolutionary dynamics. We used a well‐studied and ecologically important host–parasite system to explore morphological adaptation in host–parasite interactions. In this daphniid‐fungal parasite system, infection occurs when fungal spores puncture the host gut and enter the body cavity. Prior work found genetic differences in the parasite associated with spore size. We studied how host gut traits, parasite spore size and host immune responses influenced the infection process. We collected parasite spores from two host species, the larger Daphnia dentifera and the smaller Ceriodaphnia dubia, and exposed both host species to spores sourced from each host. The ability of a spore to embed in the host gut and to penetrate into the body cavity was influenced by the host species that was exposed to the parasite (‘exposure host species’) and the species from which the spores were sourced (‘source host species’). Spores sourced from D. dentifera were better able to attack both hosts, but were especially good at attacking D. dentifera. These differences likely resulted from morphological differences, with a striking correspondence between the diameter of host guts and the size of the parasite spores. Immune responses were influenced by both exposure and source host, with D. dentifera‐sourced spores triggering a larger immune response in D. dentifera than in C. dubia. In addition, in C. dubia exposure hosts, D. dentifera‐sourced spores triggered a greater immune response than did C. dubia‐sourced spores. Only 13.5% of hosts that had at least one parasite spore penetrate ended up with terminal infections; all but one of these infections occurred in D. dentifera hosts exposed to D. dentifera‐sourced spores. Overall, infection was influenced by morphological traits of both hosts and parasites, with the outcome at each step of the infection process—and the likelihood of terminal infection—being determined by both the exposure host and the source host. Read the free Plain Language Summary for this article on the Journal blog.

Microbial protection favors parasite tolerance and alters host-parasite coevolutionary dynamics

SummaryCoevolution between hosts and parasites is a major driver of rapid evolutionary change1 and diversification.2,3 However, direct antagonistic interactions between hosts and parasites could be disrupted4 when host microbiota form a line of defense, a phenomenon widespread across animal and plant species.5,6 By suppressing parasite infection, protective microbiota could reduce the need for host-based defenses and favor host support for microbiota colonization,6 raising the possibility that the microbiota can alter host-parasite coevolutionary patterns and processes.7 Here, using an experimental evolution approach, we co-passaged populations of nematode host (Caenorhabditis elegans) and parasites (Staphylococcus aureus) when hosts were colonized (or not) by protective bacteria (Enterococcus faecalis). We found that microbial protection during coevolution resulted in the evolution of host mortality tolerance—higher survival following parasite infection—and in parasites adapting to microbial defenses. Compared to unprotected host-parasite coevolution, the protected treatment was associated with reduced dominance of fluctuating selection dynamics in host populations. No differences in host recombination rate or genetic diversity were detected. Genomic divergence was observed between parasite populations coevolved in protected and unprotected hosts. These findings indicate that protective host microbiota can determine the evolution of host defense strategies and shape host-parasite coevolutionary dynamics.

Inference of coevolutionary dynamics and parameters from host and parasite polymorphism data of repeated experiments.

There is a long-standing interest in understanding host-parasite coevolutionary dynamics and associated fitness effects. Increasing amounts of genomic data for both interacting species offer a promising source to identify candidate loci and to infer the main parameters of the past coevolutionary history. However, so far no method exists to perform the latter. By coupling a gene-for-gene model with coalescent simulations, we first show that three types of biological costs, namely, resistance, infectivity and infection, define the allele frequencies at the internal equilibrium point of the coevolution model. These in return determine the strength of selective signatures at the coevolving host and parasite loci. We apply an Approximate Bayesian Computation (ABC) approach on simulated datasets to infer these costs by jointly integrating host and parasite polymorphism data at the coevolving loci. To control for the effect of genetic drift on coevolutionary dynamics, we assume that 10 or 30 repetitions are available from controlled experiments or several natural populations. We study two scenarios: 1) the cost of infection and population sizes (host and parasite) are unknown while costs of infectivity and resistance are known, and 2) all three costs are unknown while populations sizes are known. Using the ABC model choice procedure, we show that for both scenarios, we can distinguish with high accuracy pairs of coevolving host and parasite loci from pairs of neutrally evolving loci, though the statistical power decreases with higher cost of infection. The accuracy of parameter inference is high under both scenarios especially when using both host and parasite data because parasite polymorphism data do inform on costs applying to the host and vice-versa. As the false positive rate to detect pairs of genes under coevolution is small, we suggest that our method complements recently developed methods to identify host and parasite candidate loci for functional studies.

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones.

The Red Queen hypothesis predicts that host-parasite coevolutionary dynamics can select for host resistance through increased genetic diversity, recombination and evolutionary rates. However, in haplodiploid organisms such as the honeybee (Apis mellifera), models suggest the selective pressure is weaker than in diploids. Haplodiploid sex determination, found in A.mellifera, can allow deleterious recessive alleles to persist in the population through the diploid sex with negative effects predominantly expressed in the haploid sex. To overcome these negative effects in haploid genomes, epistatic interactions have been hypothesized to play an important role. Here, we use the interaction between A.mellifera and the parasitic mite Varroa destructor to test epistasis in the expression of resistance, through the inhibition of parasite reproduction, in haploid drones. We find novel loci on three chromosomes which explain over 45% of the resistance phenotype. Two of these loci interact only additively, suggesting their expression is independent of each other, but both loci interact epistatically with the third locus. With drone offspring inheriting only one copy of the queen's chromosomes, the drones will only possess one of two queen alleles throughout the years-long lifetime of the honeybee colony. Varroa, in comparison, completes its highly inbred reproductive cycle in a matter of weeks, allowing it to rapidly evolve resistance. Faced with the rapidly evolving Varroa, a diversity of pathways and epistatic interactions for the inhibition of Varroa reproduction could therefore provide a selective advantage to the high levels of recombination seen in A.mellifera. This allows for the remixing of phenotypes despite a fixed queen genotype.

Consistent individual and sex-specific differences in behaviour of common cuckoo chicks: is there a potential impact on host-parasite coevolutionary dynamics?

Abstract Research on brood parasitism has focused primarily on specific host anti-parasite behaviours and parasite counter-adaptations, and little is known about other aspects of their behaviours such as consistent behavioural differences between individuals. Therefore, we examined consistency in behaviour of nestlings of common cuckoos (Cuculus canorus) raised by great reed warblers (Acrocephalus arundinaceus). Cuckoo chicks showed high repeatability of both aggressive behaviour and breath rate, and both traits were strongly correlated with each other. This represents the first evidence for consistent differences in behaviour among avian brood parasites. Males were consistently more aggressive and less stressed than females. Nestlings of both sexes that hatched later in the season exhibited higher levels of aggression and lower stress responses than nestlings hatched earlier. This suggests that rearing conditions (e.g., food availability and quality) may modulate stress and aggressive phenotypes of brood parasites. We discuss potential effects of the observed patterns on host-parasite dynamics.

Host mating system and coevolutionary dynamics shape the evolution of parasite avoidance in Caenorhabditis elegans host populations.

Hosts exhibit a variety of defence mechanisms against parasites, including avoidance. Both host-parasite coevolutionary dynamics and the host mating system can alter the evolutionary trajectories of populations. Does the nature of host-parasite interactions and the host mating system affect the mechanisms that evolve to confer host defence? In a previous experimental evolution study, mixed mating and obligately outcrossing Caenorhabditis elegans host populations adapted to either coevolving or static Serratia marcescens parasite populations. Here, we assessed parasite avoidance as a mechanism underlying host adaptation. We measured host feeding preference for the coevolved and static parasites vs preference for Escherichia coli, to assess the evolution of avoidance behaviour within our experiment. We found that mixed mating host populations evolved a preference for E. coli relative to the static parasite strain; therefore, the hosts evolved parasite avoidance as a defence. However, mixed mating hosts did not exhibit E. coli preference when exposed to coevolved parasites, so avoidance cannot account for host adaptation to coevolving parasites. Further, the obligately outcrossing host populations did not exhibit parasite avoidance in the presence of either static or coevolved parasites. Therefore, both the nature of host-parasite interactions and the host mating system shaped the evolution of host defence.

Host-parasite coevolutionary dynamics with generalized success/failure infection genetics.

Host-parasite infection genetics can be more complex than envisioned by classic models such as the gene-for-gene or matching-allele models. By means of a mathematical model, I investigate the coevolutionary dynamics arising from a large set of generalized models of infection genetics in which hosts are either fully resistant or fully susceptible to a parasite, depending on the genotype of both individuals. With a single diploid interaction locus in the hosts, many of the infection genetic models produce stable or neutrally stable genotype polymorphisms. However, only a few models, which are all different versions of the matching-allele model, lead to sustained cycles of genotype frequency fluctuations in both interacting species ("Red Queen" dynamics). By contrast, with two diploid interaction loci in the hosts, many infection genetics models that cannot be classified as one of the standard infection genetics models produce Red Queen dynamics. Sexual versus asexual reproduction and, in the former case, the rate of recombination between the interaction loci have a large impact on whether Red Queen dynamics arise from a given infection genetics model. This may have interesting but as yet unexplored implications with respect to the Red Queen hypothesis for the evolution of sex.

Effects of predation on real‐time host–parasite coevolutionary dynamics

The impact of community complexity on pairwise coevolutionary dynamics is theoretically dependent on the extent to which species evolve generalised or specialised adaptations to the multiple species they interact with. Here, we show that the bacteria Pseudomonas fluorescens diversifies into defence specialists, when coevolved simultaneously with a virus and a predatory protist, as a result of fitness trade-offs between defences against the two enemies. Strong bacteria-virus pairwise coevolution persisted, despite strong protist-imposed selection. However, the arms race dynamic (escalation of host resistance and parasite infectivity ranges) associated with bacteria-virus coevolution broke down to a greater extent in the presence of the protist, presumably through the elevated genetic and demographic costs of increased bacteria resistance ranges. These findings suggest that strong pairwise coevolution can persist even in complex communities, when conflicting selection leads to evolutionary diversification of different defence strategies.

Genetic differentiation of cercariae infrapopulations of the avian schistosome Trichobilharzia szidati based on RAPD markers and mitochondrial cox1 gene

Avian schistosome Trichobilharzia szidati is a member of the largest genus within the family Schistosomatidae (Trematoda). Population genetic structure of Trichobilharzia spp. schistosomes, causative agents of cercarial dermatitis in humans, has not been studied yet. The knowledge of the genetic structure of trichobilharzian populations is essential for understanding the host-parasite coevolutionary dynamics and epidemiology strategies. Here we examined genetic diversity in three geographically isolated local populations of T. szidati cercariae inhabiting Russia based on nuclear (randomly amplified polymorphic DNA, RAPD) and mt (cox1) markers. We analyzed T. szidati cercariae shed from seven naturally infected snails of Lymnaea stagnalis. Using three random primers, we demonstrated genetic variation among populations, thus posing genetic structure across geographic sites. Moreover, T. szidati cercariae have been genetically structured among hosts (infrapopulations). Molecular variance analysis was performed to test the significance of genetic differentiation within and between local populations. Of total parasitic diversity, 18.8% was partitioned between populations, whereas the higher contribution (48.9%) corresponds to the differences among individual cercariae within infrapopulations. In contrast to RAPD markers, a 1,125-bp fragment of cox1 mt gene failed to provide any significant within-species structure. The lack of geographic structuring was detected using unique haplotypes which were determined in the current work for Moscow and Western Siberian local populations as well as obtained previously for European isolates (Czech Republic and Germany). All T. szidati/Trichobilharzia ocellata haplotypes were found to be mixed across their geographical origin.

Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Insects harbour a wild diversity of symbionts that can spread and persist within populations by providing benefits to their host. The pea aphid Acyrthosiphon pisum maintains a facultative symbiosis with the bacterium Hamiltonella defensa, which provides enhanced resistance against the aphid parasitoid Aphidius ervi. Although the mechanisms associated with this symbiotic-mediated protection have been investigated thoroughly, little is known about its evolutionary effects on parasitoid populations. We used an experimental evolution procedure in which parasitoids were exposed either to highly resistant aphids harbouring the symbiont or to low innate resistant hosts free of H.defensa. Parasitoids exposed to H.defensa gained virulence over time, reaching the same parasitism rate as those exposed to low aphid innate resistance only. A fitness reduction was associated with this adaptation as the size of parasitoids exposed to H.defensa decreased through generations. This study highlighted the considerable role of symbionts in host-parasite co-evolutionary dynamics.

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.

The ecology and phylogeny of oomycete infections in Asplanchna rotifers

1. Recently, the potential for parasites to influence the ecology and evolution of their zooplankton hosts has been the subject of increasing study. However, most research to date has focussed on Daphnia hosts, and the potential for parasites to influence other zooplankton taxa remains largely unstudied. 2. During routine sampling of zooplankton in a eutrophic lake, we observed that the rotifer Asplanchna girodi was often infected with a parasitic oomycete. Epidemics of this parasite occurred frequently, with three separate events in a single year. Prevalence at peak infection ranged from 29 to 41% and epidemics lasted from 17 to 56 days. Our data indicate that high densities of the host population are required for epidemics to occur. 3. Our morphological and molecular analyses suggest that this parasite is in the genus Pythium. Most Pythium spp. are plant pathogens, but our study supports recent work on Daphnia, suggesting that Pythium spp. are also important parasites of zooplankton. 4. As the parasite in this study was recalcitrant to cultivation, we developed an alternative method to verify its identity. Our approach used quantitative PCR to show that the ribosomal sequences identified increased with increasing density of infected hosts and, thus, were associated with the parasite. This approach should be generally applicable to other plankton parasites that are difficult to cultivate outside their hosts. 5. Infections significantly reduced host fecundity, lifespan and population growth rate. As a result of the virulence of this parasite, it is likely to influence the population ecology and evolution of its Asplanchna host, and may be a useful model system for studies on host–parasite coevolutionary dynamics.

Epistatic interactions alter dynamics of multilocus gene-for-gene coevolution.

Fitness costs associated with resistance or virulence genes are thought to play a key role in determining the dynamics of gene-for-gene (GFG) host-parasite coevolution. However, the nature of interactions between fitness effects of multiple resistance or virulence genes (epistasis) has received less attention. To examine effects of the functional form of epistasis on the dynamics of GFG host-parasite coevolution we modified a classic multilocus GFG model framework. We show that the type of epistasis between virulence genes largely determines coevolutionary dynamics, and that coevolutionary fluctuations are more likely with acceleratingly costly (negative) than with linear or deceleratingly costly (positive) epistasis. Our results demonstrate that the specific forms of interaction between multiple resistance or virulence genes are a crucial determinant of host-parasite coevolutionary dynamics.

MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids

BackgroundThe haplochromine cichlid species assemblages of Lake Malawi and Victoria represent some of the most important study systems in evolutionary biology. Identifying adaptive divergence between closely-related species can provide important insights into the processes that may have contributed to these spectacular radiations. Here, we studied a pair of sympatric Lake Malawi species, Pseudotropheus fainzilberi and P. emmiltos, whose reproductive isolation depends on olfactory communication. We tested the hypothesis that these species have undergone divergent selection at MHC class II genes, which are known to contribute to olfactory-based mate choice in other taxa.Methodology/Principal FindingsDivergent selection on functional alleles was inferred from the higher genetic divergence at putative antigen binding sites (ABS) amino acid sequences than at putatively neutrally evolving sites at intron 1, exon 2 synonymous sequences and exon 2 amino acid residues outside the putative ABS. In addition, sympatric populations of these fish species differed significantly in communities of eukaryotic parasites.Conclusions/SignificanceWe propose that local host-parasite coevolutionary dynamics may have driven adaptive divergence in MHC alleles, influencing odor-mediated mate choice and leading to reproductive isolation. These results provide the first evidence for a novel mechanism of adaptive speciation and the first evidence of adaptive divergence at the MHC in closely related African cichlid fishes.