Parasite-mediated Selection Research Articles

Parasite-mediated selection amidst marked inter-annual variation in mite parasitism and damselfly life history traits

"Parasite-mediated selection amidst marked inter-annual variation in mite parasitism and damselfly life history traits." Écoscience, 17(3), p. 343

Local exposure shapes spatial patterns in infectivity and community structure of Daphnia parasites

1. Spatial patterns in parasite community structure are probably driven by the availability of infectious stages. This is because hosts become infected through picking up infectious stages from their environment. Several studies have, however, reported strong genotype by genotype interactions and parasite-mediated selection in hosts. This leads to the prediction of a parasite by host population interaction with respect to infection rates and intensities, which may also shape spatial patterns in parasite community structure. 2. Using the water flea Daphnia magna and its microparasites as a model, we carried out a laboratory experiment to test explicitly to what extent parasite community structure in host populations is determined by the availability of infectious stages in the sediment they are exposed to, and to what extent host population identity and location play a role. 3. We exposed 10 D. magna host populations each to sediment of their own habitat and sediment of the other nine habitats, and monitored the parasite community of the resulting experimental populations. 4. Sediment seems to be a strong determinant of parasite infection rates, while there was no overall effect of host population. Sympatric parasite and host population combinations did in most cases not result in significantly different infection rates than allopatric parasite and host combinations. Our results indicate that spore availability could be the key variable determining parasite community structure in natural Daphnia populations.

Sympatric and allopatric divergence of MHC genes in threespine stickleback.

Parasites can strongly affect the evolution of their hosts, but their effects on host diversification are less clear. In theory, contrasting parasite communities in different foraging habitats could generate divergent selection on hosts and promote ecological speciation. Immune systems are costly to maintain, adaptable, and an important component of individual fitness. As a result, immune system genes, such as those of the Major Histocompatability Complex (MHC), can change rapidly in response to parasite-mediated selection. In threespine stickleback (Gasterosteus aculeatus), as well as in other vertebrates, MHC genes have been linked with female mating preference, suggesting that divergent selection acting on MHC genes might influence speciation. Here, we examined genetic variation at MHC Class II loci of sticklebacks from two lakes with a limnetic and benthic species pair, and two lakes with a single species. In both lakes with species pairs, limnetics and benthics differed in their composition of MHC alleles, and limnetics had fewer MHC alleles per individual than benthics. Similar to the limnetics, the allopatric population with a pelagic phenotype had few MHC alleles per individual, suggesting a correlation between MHC genotype and foraging habitat. Using a simulation model we show that the diversity and composition of MHC alleles in a sympatric species pair depends on the amount of assortative mating and on the strength of parasite-mediated selection in adjacent foraging habitats. Our results indicate parallel divergence in the number of MHC alleles between sympatric stickleback species, possibly resulting from the contrasting parasite communities in littoral and pelagic habitats of lakes.

Reversed parasite-mediated selection in sticklebacks from eutrophied habitats

Sexual selection is often assumed to increase the viability of populations by increasing the quality of offspring produced. Presently, human-induced environmental changes are altering the process of sexual selection by influencing male–male interactions and female mate choice. Here, we show that increased density of filamentous algae due to eutrophication reverses parasite-mediated selection during reproduction in threespine sticklebacks (Gasterosteus aculeatus). When we manipulated the density of artificial algae in a breeding area in the Baltic Sea, more males nested in dense than in sparse vegetation, but the males in dense vegetation were more parasitized. Interestingly, heavily parasitized males acquired more eggs than less parasitized males in dense vegetation but not in sparse vegetation. The higher probability of reproduction for parasitized males in dense algae growth could be due to impaired visibility relaxing male–male competition or reducing female choosiness. This could favour males in poor condition that often invest more in attracting females than males in good condition. In sparse vegetation, parasitized males may have a lower reproductive success due to intense male–male competition, careful female choice and high predation rate selecting against parasitized males. The results suggest that eutrophication could alter the fraction of the population that reproduces, which could have long-term evolutionary consequences.

A Review of Red Queen Models for the Persistence of Obligate Sexual Reproduction

I present a historical review of coevolutionary models for the evolutionary persistence of sexual reproduction. The focus is on the fate of obligately sexual populations facing competition with one or more obligately asexual clones. An early simulation model by Hamilton (Hamilton WD. 1980. Sex versus non-sex versus parasite. Oikos. 35:282-290.) suggested that parasites could be an important force in selecting against asexual clones, leading to the persistence of sex. This result was consistent with a number of independent verbal models generated from 1975-1983. Conversely, the models by May and Anderson (May RM, Anderson RM. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B Biol Sci. 219:281-313.), which included more epidemiological detail, suggested that parasites were an unlikely source of selection to favor sexual over asexual reproduction. Thus began an oscillation of opinion regarding the role of parasites in selection for sex. It would seem at present that some of the differences of opinion over time stemmed from the different ways that models were constructed, including whether the sexual population was in competition with a genetically diverse asexual population or a single clonal genotype. On theoretical grounds, parasite-mediated selection for sex seems more likely if the sexual population has options in genotypic space that are not available to the clones. Models that incorporate more ecological realism also seem more favorable to the parasite theory of sex.

Antagonistic Coevolution and Sex

One of the leading hypotheses for the maintenance of sexual reproduction is the Red Queen hypothesis. The underlying premise of the Red Queen hypothesis is that parasites rapidly evolve to infect common host genotypes. This response by parasites could result in the long-term maintenance of genetic variation and may favor sexual reproduction over asexual reproduction. The underlying ideas present a wonderful microcosm for teaching evolution. Here I present the reasons for why sex is anomalous for evolutionary theory, the rationale underlying the Red Queen hypothesis, and some empirical studies of the Red Queen hypothesis using a freshwater snail. The empirical results are consistent with the Red Queen hypothesis. In addition, the distribution of sexual and asexual reproduction in the snail leads naturally to thinking about coevolution in a geographic mosaic of parasite-mediated natural selection.

Arms Race Coevolution: The Local and Geographical Structure of a Host–Parasite Interaction

Consideration of complex geographic patterns of reciprocal adaptation has provided insight into new features of the coevolutionary process. In this paper, we provide ecological, historical, and geographical evidence for coevolution under complex temporal and spatial scenarios that include intermittent selection, species turnover across localities, and a range of trait match/mismatch across populations. Our study focuses on a plant host–parasitic plant interaction endemic to arid and semiarid regions of Chile. The long spines of Chilean cacti have been suggested to evolve under parasite-mediated selection as a first line of defense against the mistletoe Tristerix aphyllus. The mistletoe, in turn, has evolved an extremely long morphological structure that emerges from the seed endosperm (radicle) to reach the host cuticle. When spine length was traced along cactus phylogenies, a significant association between spine length and parasitism was detected, indicating that defensive traits evolved in high correspondence with the presence or absence of parasitism in two cactus lineages. Assessment of spine-radicle matching across populations revealed a potential for coevolution in 50% of interaction pairs. Interestingly, hot spots for coevolution did not distribute at random across sites. On the contrary, interaction pairs showing high matching values occur mostly in the northern distribution of the interaction, suggesting a geographical structure for coevolution in this system. Only three sampled interaction pairs were so mismatched that reciprocal selection could not occur given current trait distributions. Overall, different lines of evidence indicate that arms-race coevolution is an ongoing phenomenon that occurs in the global system of interconnected populations.

Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha)

Despite growing evidence for parasite-mediated selection on the vertebrate major histocompatibility complex (MHC), little is known about variation in the bacterial parasite community within and among host populations or its influence on MHC evolution. In this study, we characterize variation in the parasitic bacterial community associated with Chinook salmon (Oncorhynchus tshawytscha) fry in five populations in British Columbia (BC), Canada across 2 years, and examine whether bacterial infections are a potential source of selection on the MHC. We found an unprecedented diversity of bacteria infecting fry with a total of 55 unique bacteria identified. Bacterial infection rates varied from 9% to 29% among populations and there was a significant isolation by distance relationship in bacterial community phylogenetic similarity across the populations. Spatial variation in the frequency of infections and in the phylogenetic similarity of bacterial communities may result in differential parasite-mediated selection at the MHC across populations. Across all populations, we found evidence of a heterozygote advantage at the MHC class II, which may be a source of balancing selection on this locus. Interestingly, a co-inertia analysis indicated only susceptibility associations between a few of the MHC class I and II alleles and specific bacterial parasites; there was no evidence that any of the alleles provided resistance to the bacteria. Our results reveal a complex bacterial community infecting populations of a fish and underscore the importance of considering the role of multiple pathogens in the evolution of host adaptations.

Quantifying Adaptive Evolution in the Drosophila Immune System

It is estimated that a large proportion of amino acid substitutions in Drosophila have been fixed by natural selection, and as organisms are faced with an ever-changing array of pathogens and parasites to which they must adapt, we have investigated the role of parasite-mediated selection as a likely cause. To quantify the effect, and to identify which genes and pathways are most likely to be involved in the host–parasite arms race, we have re-sequenced population samples of 136 immunity and 287 position-matched non-immunity genes in two species of Drosophila. Using these data, and a new extension of the McDonald-Kreitman approach, we estimate that natural selection fixes advantageous amino acid changes in immunity genes at nearly double the rate of other genes. We find the rate of adaptive evolution in immunity genes is also more variable than other genes, with a small subset of immune genes evolving under intense selection. These genes, which are likely to represent hotspots of host–parasite coevolution, tend to share similar functions or belong to the same pathways, such as the antiviral RNAi pathway and the IMD signalling pathway. These patterns appear to be general features of immune system evolution in both species, as rates of adaptive evolution are correlated between the D. melanogaster and D. simulans lineages. In summary, our data provide quantitative estimates of the elevated rate of adaptive evolution in immune system genes relative to the rest of the genome, and they suggest that adaptation to parasites is an important force driving molecular evolution.

Ecological feedbacks and the evolution of resistance

1. The idea that parasites can affect host diversity is pervasive, and the possibility that parasites can increase host diversity is of particular interest. In this review, we focus on diversity in the resistance of hosts to their parasites, and on the different ways in which parasites can increase or decrease this resistance diversity. 2. Theoretically, parasites can exert many different types of selection on host populations, which each have consequences for host diversity. Specifically, theory predicts that parasites can exert negative frequency-dependent selection (NFDS) and disruptive selection on resistance, both of which increase host diversity, as well as directional selection and stabilizing selection on resistance, both of which decrease host diversity. 3. Despite these theoretical predictions, most biologists think of only NFDS or directional selection for increased resistance in response to parasitism. Here, we present empirical support for all of these types of selection occurring in natural populations. Interestingly, several recent studies demonstrate that there is spatiotemporal variation in the type of selection that occurs (and, therefore, in the effects of parasitism on host diversity). 4. A key question that remains, then, is: What determines the type of parasite-mediated selection that occurs? Theory demonstrates that the answer to this question lies, at least in part, with trade-offs associated with resistance. Specifically, the type of evolution that occurs depends critically on the strength and shape of these trade-offs. This, combined with empirical evidence for a strong effect of environment on the shape and strength of trade-offs, may explain the observed spatiotemporal variation in parasite-mediated selection. 5. We conclude that spatiotemporal variation in parasite-driven evolution is likely to be common, and that this variation may be driven by ecological factors. We suggest that the feedback between ecological and evolutionary dynamics in host-parasite interactions is likely to be a productive area of research. In particular, studies addressing the role of ecological factors (e.g. productivity and predation regimes) in driving the outcome of parasite-mediated selection on host populations are warranted. Such studies are necessary if we are to understand the mechanisms underlying the observed variation in the effects of parasites on host diversity.

The maintenance of sex: host–parasite coevolution with density‐dependent virulence

Why don't asexual females replace sexual females in most natural populations of eukaryotes? One promising explanation is that parasites could counter the reproductive advantages of asexual reproduction by exerting frequency-dependent selection against common clones (the Red Queen hypothesis). One apparent limitation of the Red Queen theory, however, is that parasites would seem to be required by theory to be highly virulent. In the present study, I present a population-dynamic view of competition between sexual females and asexual females that interact with co-evolving parasites. The results show that asexual populations have higher carrying capacities, and more unstable population dynamics, than sexual populations. The results also suggest that the spread of a clone into a sexual population could increase the effective parasite virulence as population density increases. This combination of parasite-mediated frequency-dependent selection, and density-dependent virulence, could lead to the coexistence of sexual and asexual reproductive strategies and the long-term persistence of sex.

Inferring selection in the Anopheles gambiae species complex: an example from immune-related serine protease inhibitors.

BackgroundMosquitoes of the Anopheles gambiae species complex are the primary vectors of human malaria in sub-Saharan Africa. Many host genes have been shown to affect Plasmodium development in the mosquito, and so are expected to engage in an evolutionary arms race with the pathogen. However, there is little conclusive evidence that any of these mosquito genes evolve rapidly, or show other signatures of adaptive evolution.MethodsThree serine protease inhibitors have previously been identified as candidate immune system genes mediating mosquito-Plasmodium interaction, and serine protease inhibitors have been identified as hot-spots of adaptive evolution in other taxa. Population-genetic tests for selection, including a recent multi-gene extension of the McDonald-Kreitman test, were applied to 16 serine protease inhibitors and 16 other genes sampled from the An. gambiae species complex in both East and West Africa.ResultsSerine protease inhibitors were found to show a marginally significant trend towards higher levels of amino acid diversity than other genes, and display extensive genetic structuring associated with the 2La chromosomal inversion. However, although serpins are candidate targets for strong parasite-mediated selection, no evidence was found for rapid adaptive evolution in these genes.ConclusionIt is well known that phylogenetic and population history in the An. gambiae complex can present special problems for the application of standard population-genetic tests for selection, and this may explain the failure of this study to detect selection acting on serine protease inhibitors. The pitfalls of uncritically applying these tests in this species complex are highlighted, and the future prospects for detecting selection acting on the An. gambiae genome are discussed.

Parasite-mediated selection amidst marked inter-annual variation in mite parasitism and damselfly life history traits

Parasite-mediated selection in host populations is thought to vary in magnitude temporally. We monitored variation in life history traits that are known or suspected to influence fitness in a population of damselflies parasitized by larval water mites. Mite prevalence and intensity varied considerably over 5 y and was often higher in females. Prevalence and intensity were highest in the years when the damselfly emergence periods were early and of short duration, which also corresponded to damselflies emerging at larger sizes. Mites appeared to exert negative effects on apparent survival in some years only, and only for females, suggesting that parasite-mediated selection on damselflies is variable and dependent on other factors such as emergence times, weather, and sex and body size of hosts.

Evidence of parasite‐mediated disruptive selection on genetic diversity in a wild fish population

Identifying the processes maintaining genetic variability in wild populations is a major concern in conservation and evolutionary biology. Parasite-mediated selection may strongly affect genetic variability in wild populations. The inbreeding depression theory predicts that directional selection imposed by parasites should act against the most inbred hosts, thus favouring genetic diversity in wild populations. We have tested this prediction by evaluating the strength and shape of the relationship between the load of a harmful fin-feeder ectoparasite (Tracheliastes polycolpus) and the genome-wide genetic diversity (i.e. heterozygosity measured at a set of 15 microsatellites) of its fish host, the rostrum dace (Leuciscus leuciscus). Contrary to expectation, we found a nonlinear relationship between host genetic diversity and ectoparasite load, with hosts that were either homozygous or heterozygous harbouring significantly fewer parasites than hosts with an intermediate level of heterozygosity. This relationship suggests that parasites could increase the variance of global heterozygosity in this host population through disruptive selection on genetic diversity. Moreover, when genetic diversity was measured at each locus separately, we found two very strong positive associations between host genetic diversity and the ectoparasite load. This latter result has three main implications: (i) genome-wide effect cannot alone explain the nonlinear relationship between global heterozygosity and ectoparasite load, (ii) negative non-additive allelic interactions (i.e. underdominance) may be a mechanism for resisting ectoparasite infection, and (iii) ectoparasites may favour homozygosity at some loci in this host population.

Caution on the assessment of intestinal parasitic load in studying parasite-mediated sexual selection: The case of Blackbirds coccidiosis

The parasite-mediated sexual selection (PMSS) theory has led to an increasing number of experimental studies essentially focussed on blood parasites. Currently, more research is being carried out on intestinal parasites in relationship to this theory. Before testing the theory with gastrointestinal parasites, it is important: (i) to determine an optimal research methodology to obtain an accurate assessment of parasite burden and (ii) to have information about life-history traits of the parasite to interpret data appropriately. In this study, we present data on oocyst output of Isospora turdi in the faeces of blackbirds ( Turdus merula) that illustrate the importance of developing methods that are relevant for a particular model system, instead of relying on existing methods that may work in other systems. Our results show that: (i) a single droplet of faeces will accurately indicate the parasitic load in blackbirds, (ii) oocyst shedding varies greatly within and between days, (iii) the course of infection is characterised with two successive peaks of oocyst shedding, (iv) infection lasts approximately 1 month and (iv) there is no effect of sex, size of infective dose or re-infection on the course of infection. We discuss the practical implications of these results in determining the reliability of, and in avoiding erroneous conclusions about, PMSS when using intestinal parasites as models. In particular, we emphasise that numerous measurements must be performed on different days. In addition, faeces must be collected at a particular time of day because there is a strong temporal variation in oocyst shedding. Finally, a standardised methodology that has been developed for a particular host–parasite assemblage does not necessarily work with other biological models. Together, our results should encourage future investigators to identify an accurate methodology for assessing parasitic load as a first step before testing hypotheses associated with the PMSS theory.

Do feather-degrading bacteria affect sexually selected plumage color?

Models of parasite-mediated sexual selection propose that males with more elaborate sexual traits will have fewer parasites. These models have generally been tested using metazoan or protozoan parasites of the blood, gut, or integument. Fewer studies have examined sexual ornaments in relation to bacterial infections. While most surface bacteria are harmless or beneficial, feather-degrading bacteria may have detrimental effects. In this study, we examined the relationships between overall bacterial load, feather-degrading bacterial load, and sexually selected carotenoid-based plumage color in a wild population of house finches (Carpodacus mexicanus). We found that males with the redder plumage preferred by females had similar overall bacterial loads, but lower feather-degrading bacterial loads, than males with less red plumage. These data suggest that plumage color can signal abundance of feather-degrading bacteria to potential mates. It remains unclear whether feather-degrading bacteria directly or indirectly affect plumage color, but the observed correlations suggest that feather-degrading bacteria may play some role in sexual selection.

Carotenoid-Based Masks in the European GoldfinchCarduelis carduelisReflect Different Information in Males and Females

Sexual selection may play an important role in the evolution of carotenoid-based signals. According to the parasite-mediated sexual selection hypothesis, organism health, parasite resistance and the expression of ornaments are linked. While some studies have analysed the expression of male carotenoid-based ornaments in relation to parasites and immune system capacities, few studies have focused on carotenoid-derived colour patches expressed in both sexes. We analysed the relationships between endoparasite (blood and systemic parasites) loads, haematological values and the components of red mask colour in wild European Goldfinches Carduelis carduelis, a species with a carotenoid-based facial mask in both sexes. Both, males and females were assessed for immune quality and face mask expression. Face mask coloration was sexually dichromatic, males have less orange masks than females. The yellow component of the mask showed less intensity in females infected with Haemoproteus blood parasites. The total leukocyte count was inversely correlated to the yellow component of the mask in females, suggesting that mask colour reflects the immune status of females during the breeding season. Isospora infection appeared to limit the UV reflection of the red mask of females.

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.

Multiple parasites mediate balancing selection at two MHC class II genes in the fossorial water vole: insights from multivariate analyses and population genetics

We investigated the factors mediating selection acting on two MHC class II genes (DQA and DRB) in water vole (Arvicola scherman) natural populations in the French Jura Mountains. Population genetics showed significant homogeneity in allelic frequencies at the DQA1 locus as opposed to neutral markers (nine microsatellites), indicating balancing selection acting on this gene. Moreover, almost exhaustive screening for parasites, including gastrointestinal helminths, brain coccidia and antibodies against viruses responsible for zoonoses, was carried out. We applied a co-inertia approach to the genetic and parasitological data sets to avoid statistical problems related to multiple testing. Two alleles, Arte-DRB-11 and Arte-DRB-15, displayed antagonistic associations with the nematode Trichuris arvicolae, revealing the potential parasite-mediated selection acting on DRB locus. Selection mechanisms acting on the two MHC class II genes thus appeared different. Moreover, overdominance as balancing selection mechanism was showed highly unlikely in this system.

Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni)

Understanding the selective forces that shape genetic variation in natural populations remains a high priority in evolutionary biology. Genes at the major histocompatibility complex (MHC) have become excellent models for the investigation of adaptive variation and natural selection because of their crucial role in fighting off pathogens. Here we present one of the first data sets examining patterns of MHC variation in wild populations of a bird of prey, the lesser kestrel, Falco naumanni. We report extensive polymorphism at the second exon of a putatively functional MHC class II gene, Fana-DAB*1. Overall, 103 alleles were isolated from 121 individuals sampled from Spain to Kazakhstan. Bayesian inference of diversifying selection suggests that several amino acid sites may have experienced strong positive selection (omega = 4.02 per codon). The analysis also suggests a prominent role of recombination in generating and maintaining MHC diversity (rho = 4Nc = 0.389 per codon, theta = 0.017 per codon). Both the Fana-DAB*1 locus and a set of eight polymorphic microsatellite markers revealed an isolation-by-distance pattern across the Western Palaearctic (r = 0.67; P = 0.01 and r = 0.50; P = 0.04, respectively). Nonetheless, geographical variation at the MHC contrasts with relatively uniform distributions in the frequencies of microsatellite alleles. In addition, we found lower fixation rates in the MHC than those predicted by genetic drift after controlling for neutral mitochondrial sequences. Our results therefore underscore the role of balancing selection as well as spatial variations in parasite-mediated selection regimes in shaping MHC diversity when gene flow is limited.