Epidemiology of a Daphnia 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 bacteriu

A meta-analysis of how parasites affect host consumption rates

Parasites are known to mediate trophic interactions and can, for example, modify how consumers acquire resources. These modifications of host feeding behaviour can be imposed through three interconnected mechanisms affecting: 1) host food acquisition, 2) host food digestion or 3) host energy budgets. As a result, infected hosts may consume more, less or the same amount of food compared to their uninfected conspecifics. It is commonly assumed that infected hosts have lower consumption rates than uninfected hosts, but a comprehensive quantitative synthesis investigating the effects of parasites on host consumption rate has been lacking thus far. To fill this knowledge gap, we systematically searched for experimental studies that evaluated changes in consumption rate of infected vs uninfected hosts. In total, we extracted 158 effect sizes from 68 studies. We then performed meta-analyses of mean differences in host consumption rates and their variation. The analyses were carried out for all taxonomic groups as well as separately for vertebrate and invertebrate hosts. The main-effects meta-analyses confirmed a generally negative effect of parasites on host consumption rates; infected hosts consumed on average 25% less food than their uninfected conspecifics. In addition, there was a significant increase in the variability in host consumption rate, on average by 25%, indicating that parasites can have variable effects on the foraging behaviour of their hosts. The meta-regression models revealed that several moderator variables related to host and parasite characteristics influence host consumption rate. Experimental infection had a stronger influence on variance effects than natural infection. Parasitic infections reduced consumption rate of vertebrate hosts by 28% and thus more strongly than those of invertebrates, which were reduced by 22%. We conclude with recommendations to facilitate future ecological research syntheses on host-parasite interactions and beyond

Hatching with the enemy: Daphnia diapausing eggs hatch in the presence of fish kairomones

Summary.: Infochemicals are known to play a key role in mediating predator-prey interactions, both in aquatic and terrestrial communities. However, state-dependent variation may exist in how effectively individuals can use this information, depending on genotype, life stage and experience. For our study, we used the predator-prey model system fish-waterflea Daphnia magna Straus (Cladocera, Daphniidae). Adult Daphnia use fish-derived infochemicals, so-called kairomones, as indicators of predation risk, and exhibit a spectrum of morphological, behavioural and life-history responses to the presence of fish kairomones. Here, we investigate whether diapausing eggs, an embryonic resting stage in the life cycle of D. magna, also use fish kairomones and tune their hatching to the risk of fish predation, as reported for diapausing stages of dinoflagellates. In two laboratory experiments, we studied hatching proportion and time until hatching of D. magna diapausing eggs in the absence and presence of fish kairomones. D. magna families differed significantly in their response to the presence of fish kairomones; some families reduced hatching proportion, whereas others increased it. Our results imply genotype-dependent differences in the hatching reactions to fish kairomones as observed for other traits in adult Daphni

The establishment of hybrids of the Daphnia longispina complex explained by a mathematical model incorporating different overwintering life history strategies

Interspecific hybridization (i.e. mating between species) occurs frequently in animals. Among cyclical parthenogens, hybrids can proliferate and establish through parthenogenetic reproduction, even if their sexual reproduction is impaired. In water fleas of the Daphnia longispina species complex, interspecific hybrids hatch from sexually produced dormant eggs. However, fewer hybrid genotypes contribute to the dormant egg bank and their hatching rate from dormant eggs is reduced, compared to eggs resulting from intraspecific crosses. Therefore, Daphnia hybrids would benefit from adaptations that increase their survival over winter as parthenogenetic lineages, avoiding the need to re-establish populations after winter from sexually produced dormant eggs. Here, we constructed a mathematical model to examine the conditions that could explain the frequently observed establishment of hybrids in the D. longispina species complex. Specifically, we compared the outcome of hybrid and parental taxa competition given a reduced contribution of hybrids to hatchlings from the sexually produced dormant egg bank, but their increased ability to survive winter as parthenogenetic lineages. In addition, different growth rates of parental species and differences in average annual temperatures were evaluated for their influence on hybrid production and establishment. Our model shows that increased overwinter performance as parthenogenetic females can compensate for reduced success in sexual reproduction, across all tested scenarios for varying relative growth rates of parental species. This pattern holds true for lower annual temperatures, but at higher temperatures hybrids were less successful. Consequently, hybrids might become less abundant as temperatures rise due to climate change, resulting in reduced diversity and faster differentiation of the parental species

Adaptation of a chytrid parasite to Its cyanobacterial host Is hampered by host intraspecific diversity

Experimental evolution can be used to test for and characterize parasite and pathogen adaptation. We undertook a serial-passage experiment in which a single parasite population of the obligate fungal (chytrid) parasite Rhizophydium megarrhizum was maintained over a period of 200 days under different mono- and multiclonal compositions of its phytoplankton host, the bloom-forming cyanobacterium Planktothrix. Despite initially inferior performance, parasite populations under sustained exposure to novel monoclonal hosts experienced rapid fitness increases evidenced by increased transmission rates. This demonstrates rapid adaptation of chytrids to novel hosts and highlights their high evolutionary potential. In contrast, increased fitness was not detected in parasites exposed to multiclonal host mixtures, indicating that cyanobacterial intraspecific diversity hampers parasites adaptation. Significant increases in intensity of infection were observed in monoclonal and multiclonal treatments, suggesting high evolvability of traits involved in parasite attachment onto hosts (i.e., encystment). A comparison of the performance of evolved and unevolved (control) parasite populations against their common ancestral host did not reveal parasite attenuation. Our results exemplify the ability of chytrid parasites to adapt rapidly to new hosts, while providing experimental evidence that genetic diversity in host populations grants increased resistance to disease by hindering parasite adaptation

Light intensity and spectral distribution affect chytrid infection of cyanobacteriaviamodulation of host fitness

Light gradients are an inherent feature in aquatic ecosystems and play a key role in shaping the biology of phytoplankton. Parasitism by chytrid fungi is gaining increasing attention as a major control agent of phytoplankton due to its previously overlooked ubiquity, and profound ecological and evolutionary consequences. Despite this interest, if and how light conditions modulate phytoplankton chytridiomycosis remains poorly studied. We investigated life-history traits of a chytrid parasite,Rhizophydium megarrhizum, under different light intensities and spectral compositions when infecting two closely related planktonic cyanobacteria with different light-harvesting strategies:Planktothrix rubescensandP. agardhii. In general, parasite transmission was highest under light conditions (both intensity and quality) that maximized growth rates for uninfected cyanobacteria. Chytrid encystment on hosts was significantly affected by light intensity and host strain identity. This likely resulted from higher irradiances stimulating the increased discharge of photosynthetic by-products, which drive parasite chemotaxis, and from strain-specific differences at the cell-surface. Comparisons of parasite transmission and host growth rates under different light conditions suggest the potential for epidemic development at higher irradiances, whereas host and parasite could coexist without epidemic outbreaks at lower light levels. These results illustrate the close relationship between parasite transmission and host fitness, which is ultimately modulated by the external environment

Fine-scale temporal and spatial variation of taxon and clonal structure in the Daphnia longispina hybrid complex in heterogeneous environments

Background: Cyclical parthenogenetic water fleas of the genus Daphnia have become a prominent model organism in ecology and evolution. In the past, analyses of their population structure have been limited by the prevailing use of allozyme markers, which in general do not allow for the distinction of individual clones. In this study, we used 10 microsatellite markers to track changes in the taxonomic and clonal composition of Daphnia populations, and traced the abundance of the most common clones in two European reservoirs. One of the localities was inhabited by a single species of the Daphnia longispina complex (D. galeata), the other by two parental species (D. galeata and D. longispina) and their interspecific hybrids. The study took place during the transition from summer stratification to autumn mixing, representing a period of major environmental change within lake habitats. Results: In both reservoirs, we observed temporal (generation-to-generation) and spatial (along the heterogeneous reservoir environment) changes in Daphnia community structure. In the single-species reservoir, the clonal diversity of D. galeata increased with time, as a few dominant clones were replaced by a higher number of less common clones. A loss in selective advantage for the dominant clones may have been due to gradual changes in the environment, or due to selection acting in a negative frequency-dependent manner. In the multispecies reservoir, there were no apparent temporal trends in clonal diversity but we observed significantly lower clonal diversity in the interspecific hybrids than in the coexisting parental species, supporting the existence of reproductive barriers between the parental genomes. Conclusions: Our study, tracing clonal lineages of Daphnia in time and space by the fine-resolution markers, contributes to the understanding of how clonal reproduction impacts community structure in cyclically parthenogenetic organisms

Fighting parasites and predators: How to deal with multiple threats?

Background: Although inducible defences have been studied extensively, only little is known about how the presence of parasites might interfere with these anti-predator adaptations. Both parasites and predators are important factors shaping community structure and species composition of ecosystems. Here, we simultaneously exposed Daphnia magna to predator cues (released by the tadpole shrimp, Triops, or by a fish) and spores of the yeast parasite Metschnikowia sp. to determine how life history and morphological inducible defences against these two contrasting types of predators are affected by infection. Results: The parasite suppressed some Triops-induced defences: Daphnia lost the ability to produce a greater number of larger offspring, a life-history adaptation to Triops predation. In contrast, the parasite did not suppress inducible defences against fish: induction (resulting in smaller body length of the mothers as well as of their offspring) and infection acted additively on the measured traits. Thus, fish-induced defences may be less costly than inducible defences against small invertebrate predators like Triops; the latter defences could no longer be expressed when the host had already invested in fighting off the parasite. Conclusions: In summary, our study suggests that as specific inducible defences differ in their costs, some might be suppressed if a target prey is additionally infected. Therefore, adding parasite pressure to predator-prey systems can help to elucidate the costs of inducible defences

Polystyrene nanoplastics differentially influence the outcome of infection by two microparasites of the host Daphnia magna

The accumulation of micro- and nanoplastic particles in freshwater bodies has given rise to much concern regarding their potential adverse effects on aquatic biota. Beyond their known effects on single species, recent experimental evidence suggests that host–parasite interactions can also be affected by environmental concentrations of micro- and nanoplastics. However, investigating the effects of contaminants in simplified infection settings (i.e. one host, one parasite) may understate their ecological relevance, considering that co-infections are common in nature. We exposed the cladoceran Daphnia magna to a fungal parasite of the haemolymph (Metschnikowia bicuspidata) and a gut microsporidium (Ordospora colligata), either in single or co-infection. In addition, Daphnia were raised individually in culture media containing 0, 5 or 50 mg l−1 of polystyrene nanoplastic beads (100 nm). Only few infections were successful at the higher nanoplastic concentration, due to increased mortality of the host. While no significant effect of the low concentration was detected on the microsporidium, the proportion of hosts infected by the fungal parasite increased dramatically, leading to more frequent co-infections under nanoplastic exposure. These results indicate that nanoplastics can affect the performance of distinct pathogens in diverging ways, with the potential to favour parasite coexistence in a common zooplanktonic host

Hybridizing Daphnia communities from ten neighbouring lakes: spatio-temporal dynamics, local processes, gene flow and invasiveness

Background In natural communities of cyclical parthenogens, rapid response to environmental change is enabled by switching between two reproduction modes. While long periods of asexual reproduction allow some clones to outcompete others, and may result in “clonal erosion”, sexual reproduction restores genetic variation in such systems. Moreover, sexual reproduction may result in the formation of interspecific hybrids. These hybrids can then reach high abundances, through asexual clonal reproduction. In the present study, we explored genetic variation in water fleas of the genus Daphnia. The focus was on the short-term dynamics within several clonal assemblages from the hybridizing Daphnia longispina complex and the impact of gene flow at small spatial scales. Results Daphnia individuals belonged either to the parental species D. galeata and D. longispina, or to different hybrid classes, as identified by 15 microsatellite markers. The distribution and genotypic structure of parental species, but not hybrids, corresponded well with the geographical positions of the lakes. Within parental species, the genetic distance among populations of D. galeata was lower than among populations of D. longispina. Moreover, D. galeata dominance was associated with higher phosphorous load. Finally, there was no evidence for clonal erosion. Conclusions Our results suggest that the contemporary structure of hybridizing Daphnia communities from ten nearby lakes is influenced by colonization events from neighbouring habitats as well as by environmental factors. Unlike the parental species, however, there was little evidence for successful dispersal of hybrids, which seem to be produced locally. Finally, in contrast to temporary Daphnia populations, in which a decrease in clonal diversity was sometimes detectable over a single growing season, the high clonal diversity and lack of clonal erosion observed here might result from repeated hatching of sexually produced offspring. Overall, our study provides insights into spatio-temporal dynamics in a hybridizing Daphnia species complex in a recently established lake system, and relates genetic similarities of populations to a scenario of secondary invasion enhanced by environmental factors