Identifying sources of variation in parasite aggregation.

Aggregation of macroparasites among hosts is a near-universal pattern, and has important consequences for the stability of host-parasite associations and the impacts of disease. Identifying which potential drivers are contributing to levels of aggregation observed in parasite-host associations is challenging, particularly for observational studies. We apply beta regressions in a Bayesian framework to determine predictors of aggregation, quantified using Poulin's index of discrepancy (D), for 13 species of parasites infecting Icelandic Rock Ptarmigan (Lagopus muta) collected over 12 years. 1,140 ptarmigan were collected using sampling protocols maximizing consistency of sample sizes and of composition of host ages and sexes represented across years from 2006-2017. Parasite species, taxonomic group (insect, mite, coccidian, or nematode), and whether the parasite was an ecto- or endoparasite were tested as predictors of aggregation, either alone or by modulating an effect of parasite mean abundance on D. Parasite species was an important predictor of aggregation in models. Despite variation in D across samples and years, relatively consistent aggregation was demonstrated for each specific host-parasite association, but not for broader taxonomic groups, after taking sample mean abundance into account. Furthermore, sample mean abundance was consistently and inversely related to aggregation among the nine ectoparasites, however no relationship between mean abundance and aggregation was observed among the four endoparasites. We discuss sources of variation in observed aggregation, sources both statistical and biological in nature, and show that aggregation is predictable, and distinguishable, among infecting species. We propose explanations for observed patterns and call for the review and re-analysis of parasite and other symbiont distributions using beta regression to identify important drivers of aggregation-both broad and association-specific.

Metabarcoding prey DNA from fecal samples of adult dragonflies shows no predicted sex differences, and substantial inter-individual variation, in diets.

Sexes often differ in foraging and diet, which is associated with sex differences in size, trophic morphology, use of habitats, and/or life history tactics. Herein, strikingly similar diets were found for adult sexes of a dragonfly (Leucorrhinia intacta), based on comparing 141 dietary taxa identified from the metabarcoding of mitochondrial DNA archived in feces. Arthropods in > 5% of samples included five species of dipterans, two hemipterans, two spider species and one parasitic mite. The mite was not traditional prey as its presence was likely due to DNA contamination of samples arising through parasitism or possibly via accidental consumption during grooming, and therefore the mite was excluded from diet characterizations. Common prey species were found with statistically indistinguishable frequencies in male and female diets, with one exception of an aphid more often found in male diets, although this pattern was not robust to corrections for multiple statistical tests. While rare prey species were often found in diets of only one sex, instances of this were more frequent in the more oft-sampled females, suggesting sampling artefact. Sexes did not differ in the mean prey species richness in their diets. Overall, sexes showed statistically indistinguishable diets both on a prey species-by-species basis and in terms of multivariate characterizations of diet composition, derived from presence-absence data of prey species analyzed via PERMANOVA and accumulation curves. Males and females may have similar diets by being both opportunistic and generalist predators of arthropods, using the same foraging habitats and having similar sizes and flight agilities. Notably, similarities in diet between sexes occur alongside large interindividual differences in diet, within sexes. Researchers intending on explaining adaptive sex differences in diet should consider characteristics of species whose sexes show similar diets.

Threats from the air: Damselfly predation on diverse prey taxa.

To understand the diversity and strength of predation in natural communities, researchers must quantify the total amount of prey species in the diet of predators. Metabarcoding approaches have allowed widespread characterization of predator diets with high taxonomic resolution. To determine the wider impacts of predators, researchers should combine DNA techniques with estimates of population size of predators using mark-release-recapture (MRR) methods, and with accurate metrics of food consumption by individuals. Herein, we estimate the scale of predation exerted by four damselfly species on diverse prey taxa within a well-defined 12-ha study area, resolving the prey species of individual damselflies, to what extent the diets of predatory species overlap, and which fraction of the main prey populations are consumed. We identify the taxonomic composition of diets using DNA metabarcoding and quantify damselfly population sizes by MRR. We also use predator-specific estimates of consumption rates, and independent data on prey emergence rates to estimate the collective predation pressure summed over all prey taxa and specific to their main prey (non-biting midges or chironomids) of the four damselfly species. The four damselfly species collectively consumed a prey mass equivalent to roughly 870 (95% CL 410-1,800) g, over 2 months. Each individual consumed 29%-66% (95% CL 9.4-123) of its body weight during its relatively short life span (2.1-4.7 days; 95% CL 0.74-7.9) in the focal population. This predation pressure was widely distributed across the local invertebrate prey community, including 4 classes, 19 orders and c. 140 genera. Different predator species showed extensive overlap in diets, with an average of 30% of prey shared by at least two predator species. Of the available prey individuals in the widely consumed family Chironomidae, only a relatively small proportion (0.76%; 95% CL 0.35%-1.61%) were consumed. Our synthesis of population sizes, per-capita consumption rates and taxonomic distribution of diets identifies damselflies as a comparatively minor predator group of aerial insects. As the next step, we should add estimates of predation by larger odonate species, and experimental removal of odonates, thereby establishing the full impact of odonate predation on prey communities.

Negative covariance between water mite and gregarine parasitism for adult dragonflies, Leucorrhinia intacta (Hagen): an age-related pattern?

Studies on parasite-mediated selection often focus on single parasite taxa infecting single species of hosts. However, host populations experience infections by multiple parasite taxa simultaneously; coinfection is expected to influence how host- and/or parasite-related factors affect host exposure and susceptibility to various parasites, and the resulting patterns of infection. We sampled adult dragonflies from a population of Leucorrhinia intacta (Hagen) in eastern Ontario, Canada. Dragonflies were exposed to parasitism by both water mites (Arrenuridae) and gregarines (Eugregarinidae). We tested for covariation between these ecto- and endoparasites, while considering potential sex and age biases in host sampling and patterns of infection. Mite parasitism differed dramatically between host sexes: nearly all collected males were parasitized, whereas only half of females were infested. This was likely due to differences in age distributions between sexes in sampled dragonflies. Water mite and gregarine parasitism showed strong, negative covariation, and coinfection occurred far less often than expected by chance, although these patterns were restricted to samples of females which, unlike male samples, likely included many old and young dragonflies. We report the first observation of negative covariation between internal and external parasite taxa in an anisopteran host and suggest this relationship between water mites and gregarines may be more widespread among Odonata and perhaps other insects than previously surmised. We advance hypotheses based on host age-parasitism relationships as well as variable parasite-mediated selection to help explain the sex specificity of observed coinfection patterns in our samples.

Host species exploitation and discrimination by animal parasites.

Parasite species often show differential fitness on different host species. We developed an equation-based model to explore conditions favouring host species exploitation and discrimination. In our model, diploid infective stages randomly encountered hosts of two species; the parasite's relative fitness in exploiting each host species, and its ability to discriminate between them, was determined by the parasite's genotype at two independent diallelic loci. Relative host species frequency determined allele frequencies at the exploitation locus, whereas differential fitness and combined host density determined frequency of discrimination alleles. The model predicts instances where populations contain mixes of discriminatory and non-discriminatory infective stages. Also, non-discriminatory parasites should evolve when differential fitness is low to moderate and when combined host densities are low, but not so low as to cause parasite extinction. A corollary is that parasite discrimination (and host-specificity) increases with higher combined host densities. Instances in nature where parasites fail to discriminate when differential fitness is extreme could be explained by one host species evolving resistance, following from earlier selection for parasite non-discrimination. Similar results overall were obtained for haploid extensions of the model. Our model emulates multi-host associations and has implications for understanding broadening of host species ranges by parasites.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Explaining parasite aggregation: more than one parasite species at a time.

Studies generally have neglected parasite-centric views in explorations of whether the oft-seen patterns of parasite aggregation are adaptive. Using simulation models, we explored the effects of aggregation on coinfection with hetero- or conspecific parasite species characterised by different mean abundances. Increasing aggregation increased the probability of conspecific co-occurrence for parasites with low mean abundances, and increased median numbers of conspecifics for all species. In comparison, increasing aggregation generally decreased the probability, intensity and diversity of heterospecific co-occurrence, irrespective of mean abundance. Researchers should weigh the respective costs and benefits of increasing co-occurrence with conspecifics and decreasing coinfection with heterospecifics in explaining aggregation.

Lesser snow goose helminths show recurring and positive parasite infection-diversity relations.

The patterns and mechanisms by which biological diversity is associated with parasite infection risk are important to study because of their potential implications for wildlife population's conservation and management. Almost all research in this area has focused on host species diversity and has neglected parasite diversity, despite evidence that parasites are important drivers of community structure and ecosystem processes. Here, we assessed whether presence or abundance of each of nine helminth species parasitizing lesser snow geese (Chen caerulescens) was associated with indices of parasite diversity (i.e. species richness and Shannon's Diversity Index). We found repeated instances of focal parasite presence and abundance having significant positive co-variation with diversity measures of other parasites. These results occurred both within individual samples and for combinations of all samples. Whereas host condition and parasite facilitation could be drivers of the patterns we observed, other host- or parasite-level effects, such as age or sex class of host or taxon of parasite, were discounted as explanatory variables. Our findings of recurring and positive associations between focal parasite abundance and diversity underscore the importance of moving beyond pairwise species interactions and contexts, and of including the oft-neglected parasite species diversity in infection-diversity studies.

Aggregation of Infective Stages of Parasites as an Adaptation and Its Implications for the Study of Parasite-Host Interactions.

The causes and consequences of aggregation among conspecifics have received much attention. For infecting macroparasites, causes include variation among hosts in susceptibility and whether infective stages are aggregated in the environment. Here, we link these two phenomena and explore whether aggregation of infective stages in the environment is adaptive to parasites encountering host condition-linked defenses and what effect such aggregations have for parasite-host interactions. Using simulation models, we show that parasite fitness is increased by aggregates attacking a host, particularly when investment into defenses is high. The fitness benefit of aggregation remains despite inclusion of factors that should curb the benefits of aggregation, namely, mortality of low-condition hosts (those hosts expected to be most susceptible to parasitism) and costs of high coinfection. For sample sizes common in studies, aggregation of infective stages reduces the likelihood of detecting host condition-parasitism relations, even when host condition is the only other factor in models affecting parasitism. Thus, it is not surprising that the expected inverse relations between host condition and parasitism, commonly a premise in studies of parasite-host interactions, are inconsistently found. An understanding of how parasites encounter hosts is thus needed for developing theory for parasite-host ecological and evolutionary interactions.

Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation.

Parasite aggregation is viewed as a natural law in parasite-host ecology but is a paradox insofar as parasites should follow the Poisson distribution if hosts are encountered randomly. Much research has focused on whether parasite aggregation in or on hosts is explained by aggregation of infective parasite stages in the environment, or by heterogeneity within host samples in terms of host responses to infection (e.g., through representation of different age classes of hosts). In this paper, we argue that the typically aggregated distributions of parasites may be explained simply. We propose that aggregated distributions can be derived from parasites encountering hosts randomly, but subsequently by parasites being 'lost' from hosts based on condition-linked escape or immunity of hosts. Host condition should be a normally distributed trait even among otherwise homogeneous sets of hosts. Our model shows that mean host condition and variation in host condition have different effects on the different metrics of parasite aggregation. Our model further predicts that as host condition increases, parasites become more aggregated but numbers of attending parasites are reduced overall and this is important for parasite population dynamics. The effects of deviation from random encounter are discussed with respect to the relationship between host condition and final parasite numbers.