Epidemiology of a <Emphasis Type="Italic">Daphnia</Emphasis> brood parasite and its implications on host life-history traits

Parasites influence host life-history traits and therefore might crucially shape host populations in natural systems. In a series of laboratory experiments, we studied the impact of an oomycete brood parasite on its Daphnia (waterflea) host. We asked whether Daphnia dump the infected brood and subsequently are able to reproduce again as was occasionally observed in a preliminary study. No viable offspring developed from infected clutches, but 78% of the infected females produced healthy offspring after releasing the infected brood while molting. Neither those offsprings’ development success nor their mothers’ reproductive potential was affected by the brood parasite. However, infected Daphnia had a reduced life-span and suffered an increased susceptibility to another parasite, an unidentified bacterium. Additionally, we studied the prevalence of this brood parasite and the unidentified bacterium in a natural Daphnia assemblage in a pre-alpine lake, across changing demographic and environmental conditions. The brood parasite epidemic seemed to be host-density dependent. Our results show that the brood parasite’s impact on the host population is enhanced when combined with the unidentified bacterium.     

Parasitism increases offspring size in a damselfly: experimental evidence for parasite-mediated maternal effects

The effects of parasites on host fitness and the fitness effects of maternal effects are widely discussed. In this study, I conducted an experiment linking both aspects. I manipulated the ectoparasite load (Acari: Arrenurus cuspidator) of damselflies, Coenagrion puella, and found that larvae from mothers with high parasite loads were larger (assessed by head width) than larvae from mothers with low parasite loads. Furthermore, there was a negative correlation between the number of eggs laid and parasite load. Parasitized mothers thus seemed to have fewer, but probably better, offspring. The ecological significance of these parasite-mediated maternal effects remains to be tested. However, size-dependent cannibalism almost certainly has important consequences for population dynamics. Copyright 1999 The Association for the Study of Animal Behaviour.     

MHC-mediated mate choice increases parasite resistance in salmon

Natural (parasite-driven) and sexual selection are thought to maintain high polymorphism in the genes of the major histocompatibility complex (MHC), but support for a link between mate choice, MHC variation and increased parasite resistance is circumstantial. We compared MHC diversity and Anisakis loads among anadromous Atlantic salmon (Salmo salar L.) returning to four rivers to spawn, which had originated from natural spawning (parents allowed to mate freely) or artificial crosses (parents deprived from the potential benefits of mate choice). We found that the offspring of artificially bred salmon had higher parasite loads and were almost four times more likely to be infected than free-mating salmon, despite having similar levels of MHC diversity. Moreover, the offspring of wild salmon were more MHC dissimilar than the offspring of artificially crossed salmon, and uninfected fish were more dissimilar for MHC than infected fish. Thus, our results suggest a link between disassortative mating and offspring benefits and indicate that MHC-mediated mate choice and natural (parasite-driven) selection act in combination to maintain MHC diversity, and hence fitness. Therefore, artificial breeding programmes that negate the potential genetic benefits of mate choice may result in inherently inferior offspring, regardless of population size, rearing conditions or genetic diversity.     

Genetic variation for maternal effects on parasite susceptibility

The expression of infectious disease is increasingly recognized to be impacted by maternal effects, where the environmental conditions experienced by mothers alter resistance to infection in offspring, independent of heritability. Here, we studied how maternal effects (high or low food availability to mothers) mediated the resistance of the crustacean Daphnia magna to its bacterial parasite Pasteuria ramosa. We sought to disentangle maternal effects from the effects of host genetic background by studying how maternal effects varied across 24 host genotypes sampled from a natural population. Under low‐food conditions, females produced offspring that were relatively resistant, but this maternal effect varied strikingly between host genotypes, i.e. there were genotype by maternal environment interactions. As infection with P. ramosa causes a substantial reduction in host fecundity, this maternal effect had a large effect on host fitness. Maternal effects were also shown to impact parasite fitness, both because they prevented the establishment of the parasites and because even when parasites did establish in the offspring of poorly fed mothers, and they tended to grow more slowly. These effects indicate that food stress in the maternal generation can greatly influence parasite susceptibility and thus perhaps the evolution and coevolution of host–parasite interactions.     

Apparent vector‐mediated parent‐to‐offspring transmission in an avian malaria‐like parasite

Parasite transmission strategies strongly impact host–parasite co‐evolution and virulence. However, studies of vector‐borne parasites such as avian malaria have neglected the potential effects of host relatedness on the exchange of parasites. To test whether extended parental care in the presence of vectors increases the probability of transmission from parents to offspring, we used high‐throughput sequencing to develop microsatellites for malaria‐like Leucocytozoon parasites of a wild raptor population. We show that host siblings carry genetically more similar parasites than unrelated chicks both within and across years. Moreover, chicks of mothers of the same plumage morph carried more similar parasites than nestlings whose mothers were of different morphs, consistent with matrilineal transmission of morph‐specific parasite strains. Ours is the first evidence of an association between host relatedness and parasite genetic similarity, consistent with vector‐mediated parent‐to‐offspring transmission. The conditions for such ‘quasi‐vertical’ transmission may be common and could suppress the evolution of pathogen virulence.     

Genetics of host-parasite interactions

The evolution of host susceptibility or resistance to parasites has important consequences for the evolution of parasite virulence, host sexual selection, population dynamics of both host and parasite populations, and programs of biological control. The general observation of a fraction of Individuals within a population that is not parasitized, and/or the variability in parasite intensity among hosts, may reflect several phenomena acting at different levels of ecological organization. Yet, host-parasite coevolution requires host susceptibility and parasite virulence to be genetically variable. In spite of evolutionary and epidemiological implications of genetic heterogeneities in host-parasite systems, evidence concerning natural populations is still scarce. Here, we wish to emphasize why we need a better knowledge of the genetics of host-parasite interaction in natural populations and to review the evidence concerning the heritability of host susceptibility or resistance to parasites in natural populations of animals.     

The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.     

Parasite strain coexistence in a heterogeneous host population

Heterogeneity in host susceptibility and transmissibility to parasite attack allows a lower transmission rate to sustain an epidemic than is required in homogeneous host populations. However, this heterogeneity can leave some hosts with little susceptibility to disease, and at high transmission rates, epidemic size can be smaller than for diseases where the host population is homogeneous. In a heterogeneous host population, we model natural selection in a parasite population where host heterogeneity is exploited by different strains to varying degrees. This partitioning of the host population allows coexistence of competing parasite strains, with the heterogeneity-exploiting strains infecting the more susceptible hosts, in the absence of physiological tradeoffs and spatial heterogeneity, and even for markedly different transmission rates. In our model, intermediate-strategy parasites were selected against: should coexistence occur, an equilibrium is reached where strains occupied only the extreme ends of trait space, under appropriate conditions selecting for lower R₀.     

Bigger is better: changes in body size explain a maternal effect of food on offspring disease resistance

Maternal effects triggered by changes in the environment (e.g., nutrition or crowding) can influence the outcome of offspring–parasite interactions, with fitness consequences for the host and parasite. Outside of the classic example of antibody transfer in vertebrates, proximate mechanisms have been little studied, and thus, the adaptive significance of maternal effects on infection is not well resolved. We sought to determine why food‐stressed mothers give birth to offspring that show a low rate of infection when the crustacean Daphnia magna is exposed to an orally infective bacterial pathogen. These more‐resistant offspring are also larger at birth and feed at a lower rate. Thus, reduced disease resistance could result from slow‐feeding offspring ingesting fewer bacterial spores or because their larger size allows for greater immune investment. To distinguish between these theories, we performed an experiment in which we measured body size, feeding rate, and susceptibility, and were able to show that body size is the primary mechanism causing altered susceptibility: Larger Daphnia were less likely to become infected. Contrary to our predictions, there was also a trend that fast‐feeding Daphnia were less likely to become infected. Thus, our results explain how a maternal environmental effect can alter offspring disease resistance (though body size), and highlight the potential complexity of relationship between feeding rate and susceptibility in a host that encounters a parasite whilst feeding.     

HERITABILITY OF OVIPOSITION PREFERENCE AND ITS RELATIONSHIP TO OFFSPRING PERFORMANCE WITHIN A SINGLE INSECT POPULATION

Within a population of the butterfly Euphydryas editha that oviposits predominantly on two host species, heritable variation in postalighting oviposition preference was found. In a separate experiment, oviposition preference of adult females was found to be correlated with offspring performance (growth). There was a significant tendency for offspring to perform better on the host species that their female parent preferred. Analysis of the data showed that no single factor, neither maternal preference nor the host species on which the offspring were raised, accounted for any significant variation in larval performance. However, the effect of the interaction between host species and maternal preference on offspring performance was highly significant. These findings imply specialization in both oviposition preference and offspring performance by individuals within a single population. With present evidence, this preference-performance correlation is likely to be genetic. However, as in previous studies, other interpretations cannot be excluded.     

Genotypic vs. condition effects on parasite-driven rare advantage

Models and empirical studies of coevolution assume host resistance and parasite infectivity are genetically based. However, nongenetic physiological or environmental influences could alter host susceptibility even when the relationship is genetically based. In this experiment we examined the influence of host genotype, host condition at the time of infection (age and reproductive status), and their interaction on resistance of the freshwater snail Potamopyrgus antipodarum) to its dominant trematode parasite (Microphallus sp.). We used a laboratory infection experiment of a clonal snail population to determine the susceptibility of juveniles, brooding adult females, and nonbrooding adult females. We found a significant effect of both life-history state and clonal genotype on the prevalence of infection. However, the relative susceptibility of different clonal genotypes was not altered by condition; genotypes that were rare in the natural population were less infected than those that were common for each life-history state. These results suggest that although host condition affects susceptibility, it does not disrupt the specificity of the match between parasites and common clonal genotypes. Hence these findings support the Red Queen hypothesis for the maintenance of sex under genetically based host-parasite interactions.     

Multiple parasites are driving major histocompatibility complex polymorphism in the wild

Parasite mediated selection may result in arms races between host defence and parasite virulence. In particular, simultaneous infections from multiple parasite species should cause diversification (i.e. balancing selection) in resistance genes both at the population and the individual level. Here, we tested these ideas in highly polymorphic major histocompatibility complex (MHC) genes from three-spined sticklebacks (Gasterosteus aculeatus L.). In eight natural populations, parasite diversity (15 different species), and MHC class IIB diversity varied strongly between habitat types (lakes vs. rivers vs. estuaries) with lowest values in rivers. Partial correlation analysis revealed an influence of parasite diversity on MHC class IIB variation whereas general genetic diversity assessed at seven microsatellite loci was not significantly correlated with parasite diversity. Within individual fish, intermediate, rather than maximal allele numbers were associated with minimal parasite load, supporting theoretical models of self-reactive T-cell elimination. The optimal individual diversity matched those values female fish try to achieve in their offspring by mate choice. We thus present correlative evidence supporting the 'allele counting' strategy for optimizing the immunocompetence in stickleback offspring.     

Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (<Emphasis Type="Italic">Danaus plexippus</Emphasis>)

Parasites often produce large numbers of offspring within their hosts. High parasite burdens are thought to be important for parasite transmission, but can also lower host fitness. We studied the protozoan Ophryocystis elektroscirrha, a common parasite of monarch butterflies (Danaus plexippus), to quantify the benefits of high parasite burdens for parasite transmission. This parasite is transmitted vertically when females scatter spores onto eggs and host plant leaves during oviposition; spores can also be transmitted between mating adults. Monarch larvae were experimentally infected and emerging adult females were mated and monitored in individual outdoor field cages. We provided females with fresh host plant material daily and quantified their lifespan and lifetime fecundity. Parasite transmission was measured by counting the numbers of parasite spores transferred to eggs and host plant leaves. We also quantified spores transferred from infected females to their mating partners. Infected monarchs had shorter lifespans and lower lifetime fecundity than uninfected monarchs. Among infected females, those with higher parasite loads transmitted more parasite spores to their eggs and to host plant leaves. There was also a trend for females with greater parasite loads to transmit more spores to their mating partners. These results demonstrate that high parasite loads on infected butterflies confer a strong fitness advantage to the parasite by increasing between-host transmission.     

Sexual showiness and parasite load: correlations without parasite coevolutionary cycles

Hamilton & Zuk (1982, Science 218, 384-387.) produced a model of sexual selection in which coevolutionary cycles of host and parasites generate consistently positive correlations between parent and offspring viability, and that animals choose mates for genetic disease resistance by scrutinizing characters whose full expression is dependent on health and vigour. They predicted a positive correlation between sexual showiness and parasite burden across species, and a negative correlation within a species. First, recent suggestions that interspecific correlations in the opposite direction to that indicated above are consistent with the mechanisms of Hamilton & Zuk's model are discussed. Second, it is shown that the model's predictions can be produced by heritable variation maintained by non-parasite fluctuating selection. In this case, the parasites associated with degree of sexual showiness are those able to amplify any initial heritable differences in vigour. Alternative sources of positive correlation between parent and offspring viability, which include the indirect effects of climatic change and exclude the need for host-parasite coevolutionary cycles, are also proposed.     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

Reproductive Trade-Offs May Moderate the Impact of Gyrodactylus salaris in Warmer Climates

Gyrodactylus salaris is a notifiable freshwater ectoparasite of salmonids. Its primary host is Atlantic salmon (Salmo salar), upon which infections can cause death, and have led to massive declines in salmon numbers in Norway, where the parasite is widespread. Different strains of S. salar vary in their susceptibility, with Atlantic strains (such as those found in Norway) exhibiting no resistance to the parasite, and Baltic strains demonstrating an innate resistance sufficient to regulate parasite numbers on the host causing it to either die out or persist at a low level. In this study, Leslie matrix and compartmental models were used to generate data that demonstrated the population growth of G. salaris on an individual host is dependent on the total number of offspring per parasite, its longevity and the timing of its births. The data demonstrated that the key factor determining the rate of G. salaris population growth is the time at which the parasite first gives birth, with rapid birth rate giving rise to large population size. Furthermore, it was shown that though the parasite can give birth up to four times, only two births are required for the population to persist as long as the first birth occurs before a parasite is three days old. As temperature is known to influence the timing of the parasite''s first birth, greater impact may be predicted if introduced to countries with warmer climates than Norway, such as the UK and Ireland which are currently recognised to be free of G. salaris. However, the outputs from the models developed in this study suggest that temperature induced trade-offs between the total number of offspring the parasite gives birth to and the first birth timing may prevent increased population growth rates over those observed in Norway.     

PARASITE-MEDIATED SELECTION AGAINST INBRED SOAY SHEEP IN A FREE-LIVING ISLAND POPULATON

Parasites are thought to provide a selective force capable of promoting genetic variation in natural populations. One rarely considered pathway for this action is via parasite-mediated selection against inbreeding. If parasites impose a fitness cost on their host and the offspring of close relatives have greater susceptibility to parasites due to the increased homozygosity that results from inbreeding, then parasite-mediated mortality may select against inbred individuals. This hypothesis has not yet been tested within a natural vertebrate population. Here we show that relatively inbred Soay sheep (Ovis aries), as assessed by microsatellite heterozygosity, are more susceptible to parasitism by gastrointestinal nematodes, with interactions indicating greatest susceptibility among adult sheep at high population density. During periods of high overwinter mortality on the island of Hirta, St. Kilda, Scotland, highly parasitised individuals were less likely to survive. More inbred individuals were also less likely to survive, which is due to their increased susceptibility to parasitism, because survival was random with respect to inbreeding among sheep that were experimentally cleared of their gastrointestinal parasite burden by anthelminthic treatment. As a consequence of this selection, average microsatellite heterozygosity increases with age in St. Kildan Soay sheep. We suggest that parasite-mediated selection acts to maintain genetic variation in this small island population by removing less heterozygous individuals.     

Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict?

Parent-offspring conflict may arise because the lifetime reproductive success of the parent is more influenced by its life span than by reproductive success during a particular reproductive event, while the fitness of an offspring depends firstly on its own survival as a juvenile and only subsequently on its own reproductive success. The naive immune system of young animals may allow offspring to be much more affected by parasites than their parents, and thus cause an initial asymmetry in a potential parent-offspring conflict. We investigated this type of conflict by assessing the health status and the immune response of parent and offspring sand martins Riparia riparia infested with manipulated loads of ticks Ixodes lividus (nests either treated with pyrethrin, water, or just visited). The prevalence and the intensity of tick infestations differed among treatments, with low tick loads in nests with the pyrethrin treatment. Ticks reduced the reproductive success of the host and increased offspring wing length. Broods with ticks had higher leukocyte concentrations and concentrations of immunoglobulins. The concentration of immunoglobulins in nestlings was negatively related to brood size and nestling tarsus length. Nestlings receiving the control treatments had a positive association between wing length and the concentration of immunoglobulins and a negative association between tarsus length and immunoglobulins. In contrast, adult sand martins did not respond to the parasite treatment in terms of immune response. Hence, the naive immune system of nestlings may be the crucial factor causing the parent-offspring conflict over costs of parasitism to be resolved to the advantage of parents that may sacrifice nestlings in heavily parasitized nests. Received: 30 March 1998 / Accepted: 5 December 1998     

Host‐specific variation in off‐host performance of a temperate ectoparasite

Antagonistic host–parasite interactions are rarely considered from an ecological perspective of the parasite. We used a blood‐feeding ectoparasite of boreal cervids, the deer ked (Lipoptena cervi L., Hippoboscidae), to study host‐dependent variation in a parasite's ability to cope with an abiotic environment during the free‐living stage(s) in two allopatric Fennoscandian populations. We found that a strongly host‐specific deer ked population in eastern Fennoscandia, exploiting only moose (Alces alces), produced the largest offspring that were the most cold‐tolerant and emerged the earliest as adults, when compared with the western Fennoscandian population that exploited two hosts efficiently. Within the western population, however, offspring produced on roe deer (Capreolus capreolus) were significantly larger, more cold‐tolerant, and had higher survival than those produced on moose in the same area. We discuss potential causes for both host‐specific and geographical differences in off‐host performance: (1) maternal host directly affects the offspring survival prospects; (2) divergent co‐evolution with local main host(s) has shaped the parasite's life history; and/or (3) off‐host performance is shaped by adaptation to the local abiotic environment. In conclusion, this study increases our understanding of the evolution of host–parasite interactions by demonstrating how geographical differences in host exploitation may result in differences in survival prospects outside the host.     

EFFECTS OF A HAEMATOPHAGOUS MITE ON THE BARN SWALLOW (HIRUNDO RUSTICA): A TEST OF THE HAMILTON AND ZUK HYPOTHESIS

I tested three assumptions of the Hamilton and Zuk hypothesis (1982), which suggests that the extravagant male plumage of many bird species allows females to choose mates that are resistant to the parasites exploiting the host population at a given time. By choosing such males as mates, females will rear offspring carrying the genes for resistance. I tested three necessary conditions for the Hamilton and Zuk model: (1) whether parasites affect the fitness of their hosts; (2) whether there is heritable variation in parasite resistance, and (3) whether the expression of the sexual ornament varies with parasite burden. The haematophagous mite Ornithonyssus bursa (Macronyssidae, Gamasida) sucks blood from their Barn Swallow (Hirundo rustica) hosts. Experimental manipulation of mite loads and partial cross-fostering experiments on Barn Swallows, where half of the nestlings in the brood were exchanged with nestlings from another nest, shows that parasite burdens and origin, but not rearing conditions, of Bam Swallow nestlings, affected their adult tarsus length and maximum body weight shortly before fledging. Mite loads of adult Barn Swallows at spring arrival were more similar to mite loads of their own offspring, whether reared in their own or in foster nests inoculated with mites, than to loads of foster offspring. Parent Barn Swallows with long tail ornaments had offspring with smaller mite loads in the partial cross-fostering experiments. The amount of increase in male tail ornaments from one year to another was negatively related to experimentally manipulated mite loads of Barn Swallow nests during the preceding breeding season. In conclusion, the three assumptions of the hypothesis were supported by the experimental tests.