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.     

Food stoichiometry affects the outcome of Daphnia–parasite interaction

Phosphorus (P) is an essential nutrient for growth in consumers. P‐limitation and parasite infection comprise one of the most common stressor pairs consumers confront in nature. We conducted a life‐table study using a Daphnia–microsporidian parasite model, feeding uninfected or infected Daphnia with either P‐sufficient or P‐limited algae, and assessed the impact of the two stressors on life‐history traits of the host. Both infection and P‐limitation negatively affected some life‐history traits tested. However, under P‐limitation, infected animals had higher juvenile growth rate as compared with uninfected animals. All P‐limited individuals died before maturation, regardless of infection. The numbers of spore clusters of the microsporidian parasite did not differ in P‐limited or P‐sufficient hosts. P‐limitation, but not infection, decreased body phosphorus content and ingestion rates of Daphnia tested in separate experiments. As parasite spore production did not suffer even under extreme P‐limitation, our results suggest that parasite was less limited by P than the host. We discuss possible interpretations concerning the stoichiometrical demands of parasite and suggest that our results are explained by parasite‐driven changes in carbon (C) allocation of the hosts. We conclude that the impact of nutrient starvation and parasite infection on consumers depends not only on the stoichiometric demands of host but also those of the parasite.     

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

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.     

The neonate nutrition hypothesis: early feeding affects the body stoichiometry of Daphnia offspring

相似文献   

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.     

Parasites driving host diversity: Incidence of disease correlated with Daphnia clonal turnover*

According to the Red Queen hypothesis, clonal diversity in asexual populations could be maintained by negative frequency‐dependant selection by coevolving parasites. If common clones are selected against and rare clones gain a concomitant advantage, we expect that clonal turnover should be faster during parasite epidemics than between them. We tested this hypothesis exploring field data of the Daphnia–Caullerya host–parasite system. The clonal make‐up and turnover of the Daphnia host population was tracked with high temporal resolution from 1998 until 2013, using first allozyme and later microsatellite markers. Significant differences in the clonal composition between random and infected subsamples of Daphnia populations were detected on six of seven tested occasions, confirming genetic specificity of the host–parasite interaction in this system. We used time series analysis to compare the rates of host clonal turnover to the incidence of parasitism, and found that Caullerya prevalence was significantly associated with microsatellite‐based clonal turnover. As alternate hypotheses, we further tested whether turnover was related to a variety of biotic, abiotic, and host demographic parameters. Other significant correlates of turnover were cyanobacterial biomass and (weakly) temperature. Overall, parasitism seems to be a strong driver of host clonal turnover, in support of the Red Queen hypothesis.     

Context dependency of infectious disease: the cyanobacterium Microcystis aeruginosa decreases white bacterial disease in Daphnia magna

相似文献   

Maternal Effects of Photoperiod and Food Level on Life History Characteristics of the Cladoceran Daphnia Pulicaria Forbes

The response of various life-history characteristics of Daphnia pulicaria to photoperiod and food concentration was measured in 16 combinations of maternal and offspring environments (long vs. short day, high vs. low food) in flow-through experiments. Response variables in offspring were time and survival to release of first offspring, clutch size and neonate mass in the first brood, mass of adult females after 30days and somatic growth rate during the course of the experiment. Most of these parameters were directly controlled by food concentration in the offspring environment, but maternal effects frequently modified the response. A long day length in the maternal environment resulted in a prolongation of the time to first clutch release in offspring similar to the direct effect of low food. Likewise, survival to maturation and female mass were affected by maternal photoperiod. Somatic growth rate and clutch size responded to combined effects of maternal food conditions and photoperiod. The laboratory results were used to predict the seasonal change of fecundity of Daphnia in the field. When data on clutch size are ordered in a sequence as the different combinations of maternal and offspring environment occur during the seasonal succession in a temperate lake, they show a bimodal distribution with a high peak in spring and a lower peak in fall. This pattern is consistent with field observations. We conclude that photoperiod and maternal effects are important factors influencing life history and population dynamics of Daphnia.     

Diet quality determines interspecific parasite interactions in host populations

The widespread occurrence of multiple infections and the often vast range of nutritional resources for their hosts allow that interspecific parasite interactions in natural host populations might be determined by host diet quality. Nevertheless, the role of diet quality with respect to multispecies parasite interactions on host population level is not clear. We here tested the effect of host population diet quality on the parasite community in an experimental study using Daphnia populations. We studied the effect of diet quality on Daphnia population demography and the interactions in multispecies parasite infections of this freshwater crustacean host. The results of our experiment show that the fitness of a low‐virulent microsporidian parasite decreased in low, but not in high‐host‐diet quality conditions. Interestingly, infections with the microsporidium protected Daphnia populations against a more virulent bacterial parasite. The observed interspecific parasite interactions are discussed with respect to the role of diet quality‐dependent changes in host fecundity. This study reflects that exploitation competition in multispecies parasite infections is environmentally dependent, more in particular it shows that diet quality affects interspecific parasite competition within a single host and that this can be mediated by host population‐level effects.     

Higher parasite resistance in Daphnia populations with recent epidemics

Natural populations often show genetic variation in parasite resistance, forming the basis for evolutionary response to selection imposed by parasitism. We investigated whether previous epidemics selected for higher resistance to novel parasite isolates in a Daphnia galeata–microparasite system by comparing susceptibility of host clones from populations with varying epidemic history. We manipulated resource availability to evaluate whether diet influences Daphnia susceptibility as epidemics are common in nutrient‐rich lakes. Exposing clones from 10 lakes under two food treatments to an allopatric protozoan parasite, we found that Daphnia originating from lakes (mainly nutrient rich) with previous epidemics better resist infection. Despite this result, there was a tendency of higher susceptibility in the low food treatment, suggesting that higher resistance of clones from populations with epidemic background is not directly caused by lake nutrient level. Rather, our results imply that host populations respond to parasite‐mediated selection by evolving higher parasite resistance.     

Size‐dependent reproductive success of wild zebrafish Danio rerio in the laboratory

Size‐dependent reproductive success of wild zebrafish Danio rerio was studied under controlled conditions in the laboratory to further understand the influence of spawner body size on reproductive output and egg and larval traits. Three different spawner size categories attained by size‐selective harvesting of the F₁‐offspring of wild D. rerio were established and their reproductive performance compared during a 5 day period. As to be expected, large females spawned more frequently and had significantly greater clutch sizes than small females. Contrary to expectations, small females produced larger eggs when measured as egg diameter with similar amounts of yolk compared to eggs spawned by large spawners. Eggs from small fish, however, suffered from higher egg mortality than the eggs of large individuals. Embryos from small‐sized spawners also hatched later than offspring from eggs laid by large females. Larval standard length (L_S)‐at‐hatch did not differ between the size categories, but the offspring of the large fish had significantly larger area‐at‐hatch and greater yolk‐sac volume indicating better condition. Offspring growth rates were generally similar between offspring from all size categories, but they were significantly higher for offspring spawned by small females in terms of L_S between days 60 and 90 post‐fertilization. Despite temporarily higher growth rates among the small fish offspring, the smaller energy reserves at hatching translated into lower condition later in ontogeny. It appeared that the influence of spawner body size on egg and larval traits was relatively pronounced early in development and seemed to remain in terms of condition, but not in growth, after the onset of exogenous feeding. Further studies are needed to explore the mechanisms behind the differences in offspring quality between large‐ and small‐sized spawners by disentangling size‐dependent maternal and paternal effects on reproductive variables in D. rerio.     

Microparasite transmission to <Emphasis Type="Italic">Daphnia magna</Emphasis> decreases in the presence of conspecifics

Single parasite species often have a range of different hosts which vary in their ability to sustain the parasite. When foraging for food, alternative hosts with similar feeding modes may compete for the infective stages of trophically transmitted parasites. If some of the infective stages end up in unsuitable hosts, transmission of the parasite to the focal host is decreased. I studied whether the presence of conspecifics alters the probability of an uninfected susceptible recipient Daphnia becoming infected by a microparasite and if this effect depends on whether the added conspecifics themselves are susceptible or resistant to infection. The presence of both susceptible and resistant conspecifics decreased the probability of infection in recipients. This effect was dependent on the density of the conspecifics but was not found to be related to their size. In addition, when Daphnia were placed in medium derived from crowded Daphnia populations, the probability of infection in recipients decreased as compared to that in standard medium. This implies that decreases in transmission probability are not caused by dilution of spores through food competition only, but also by indirect interference mediated through infochemicals released by Daphnia. Since Daphnia have been found to respond to crowding by decreasing their filtering rate, the decrease in transmission is probably caused by decreased intake of spores in crowded conditions. The presence of conspecifics can thus decrease microparasite transmission in Daphnia which may have important consequences for epidemiology and evolution of Daphnia parasites.     

Maternal food quantity affects offspring feeding rate in Daphnia magna

Maternal effects have wide-ranging effects on life-history traits. Here, using the crustacean Daphnia magna, we document a new effect: maternal food quantity affects offspring feeding rate, with low quantities of food triggering mothers to produce slow-feeding offspring. Such a change in the rate of resource acquisition has broad implications for population growth or dynamics and for interactions with, for instance, predators and parasites. This maternal effect can also explain the previously puzzling situation that the offspring of well-fed mothers, despite being smaller, grow and reproduce better than the offspring of food-starved mothers. As an additional source of variation in resource acquisition, this maternal effect may also influence relationships between life-history traits, i.e. trade-offs, and thus constraints on adaptation. Maternal nutrition has long-lasting effects on health and particularly diet-related traits in humans; finding an effect of maternal nutrition on offspring feeding rate in Daphnia highlights the utility of this organism as a powerful experimental model for exploring the relationship between maternal diet and offspring fitness.     

Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction

Abstract. 1. Hosts experiencing frequent variation in density are thought to benefit from allocating more resources to parasite defence when density is high (‘density‐dependent prophylaxis’). However, high density conditions can increase intra‐specific competition and induce physiological stress, hence increasing host susceptibility to infection (‘crowding‐stress hypothesis’). 2. We studied monarch butterflies (Danaus plexippus) and quantified the effects of larval rearing density on susceptibility to the protozoan parasite Ophryocystis elektroscirrha. Larvae were inoculated with parasite spores and reared at three density treatments: low, moderate, and high. We examined the effects of larval density on parasite loads, host survival, development rates, body size, and wing melanism. 3. Results showed an increase in infection probability with greater larval density. Monarchs in the moderate and high density treatments also suffered the greatest negative effects of parasite infection on body size, development rate, and adult longevity. 4. We observed greater body sizes and shorter development times for monarchs reared at moderate densities, and this was true for both unparasitised and parasite‐treated monarchs. We hypothesise that this effect could result from greater larval feeding rates at moderate densities, combined with greater physiological stress at the highest densities. 5. Although monarch larvae are assumed to occur at very low densities in the wild, an analysis of continent‐wide monarch larval abundance data showed that larval densities can reach high levels in year‐round resident populations and during the late phase of the breeding season. Treatment levels used in our experiment captured ecologically‐relevant variation in larval density observed in the wild.     

Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara)

We studied the effect of maternal ectoparasite load (measured at parturition) on the life-history traits of the offspring of the host Lacerta vivipara, the European common lizard. The ectoparasite, a mite belonging to the family Laelapidae, had a detrimental effect on its host: parasite load was associated with increased host mortality, and was negatively correlated with host body mass. Parasite load was persistent over time, suggesting that parasite load can be predictable. Offspring of highly parasitised mothers had higher values of several fitness components early in life than offspring of parasite-free mothers or lightly infested mothers. This was expressed in terms of increased F₁ yearling growth rate, and reproductive investment at first reproduction (measured as F₂ hatchling mass). These results are interpreted as a host adaptation to attenuate the impact of parasites. Indeed, if high parasite loads arise from long exposure time to a constant population of parasites, and if the negative effects of parasites are additive over time, hosts could reduce the impact of parasites simply by investing more during the earlier stages of life. Naturally, having better performance early in life should lead to higher mortality rates and/or lower fecundity later in life.     

Effects of maternal and grandmaternal flea infestation on offspring quality and quantity in a desert rodent: evidence for parasite-mediated transgenerational phenotypic plasticity

Parasites can cause a broad range of sublethal fitness effects across a wide variety of host taxa. However, a host’s efforts to compensate for possible parasite-induced fitness effects are less well-known. Parental effects may beneficially alter the offspring phenotype if parental environments sufficiently predict the offspring environment. Parasitism is a common stressor across generations; therefore, parental infestation could reliably predict the likelihood of infestation for offspring. However, little is known about relationships between parasitism and transgenerational phenotypic plasticity. Thus, we investigated how maternal and grandmaternal infestation with fleas (Xenopsylla ramesis) affected offspring quality and quantity in a desert rodent (Meriones crassus). We used a fully-crossed design with control and infested treatments to examine litter size, pup body mass at birth, and pup mass gain before weaning for combinations of maternal and grandmaternal infestation status. No effect of treatment on litter size or pup body mass at birth was found. However, maternal and grandmaternal infestation status significantly affected pre-weaning body mass gain, a proxy for the rate of maturation, in male pups. Pups gained significantly more weight before weaning if maternal and grandmaternal infestation statuses matched, regardless of the treatment. Thus, pups whose mothers and grandmothers experienced similar risks of parasitism, either both non-parasitized or both infested, would reach sexual maturity more quickly than those pups whose mothers’ infestation status did not match that of their grandmothers. These results support the contention that parents can receive external cues such as the risk of parasitism, that prompt them to alter offspring provisioning. Therefore, parasites could be a mediator of environmentally-induced maternal effects and could affect host reproductive fitness across multiple generations.     

Trait-mediated indirect effects, predators, and disease: test of a size-based model

Increasing prevalence of wildlife disease accentuates the need to uncover drivers of epidemics. Predators can directly influence disease prevalence via density-mediated effects (e.g., culling infected hosts leading to reduced disease prevalence). However, trait-mediated indirect effects (TMIEs) of predators can also strongly influence disease—but predicting a priori whether TMIEs should increase or decrease disease prevalence can be challenging, especially since a single predator may elicit responses that have opposing effects on disease prevalence. Here, we pair laboratory experiments with a mechanistic, size-based model of TMIEs in a zooplankton host, fungal parasite, multiple predator system. Kairomones can either increase or decrease body size of the host Daphnia, depending on the predator. These changes in size could influence key traits of fungal disease, since infection risk and spore yield increase with body size. For six host genotypes, we measured five traits that determine an index of disease spread (R ₀). Although host size and disease traits did not respond to kairomones produced by the invertebrate predator Chaoborus, cues from fish reduced body size and birth rate of uninfected hosts and spore yield from infected hosts. These results support the size model for fish; the birth and spore yield responses should depress disease spread. However, infection risk did not decrease with fish kairomones, thus contradicting predictions of the size model. Exposure to kairomones increased per spore susceptibility of hosts, countering size-driven decreases in exposure to spores. Consequently, synthesizing among the relevant traits, there was no net effect of fish kairomones on the R ₀ metric. This result accentuates the need to integrate the TMIE-based response to predators among all key traits involved in disease spread.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.