Spatio-temporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape.

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogeneous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing prolonged dormancy yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, we investigated the extent to which parasite survival within snails is diminished. We conducted an investigation of seasonal snail schistosome dynamics in 109 ponds of variable ephemerality in Tanzania from August 2021 to July 2022. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and observed cercariae, though of lower magnitude in the fully desiccating than non-desiccating ponds. Second, we evaluated total yearly schistosome prevalence across an ephemerality gradient, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

Spatiotemporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape.

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogenous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing dormancy for up to seven months yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, parasite survival within snails is greatly diminished. We conducted a year-round investigation of seasonal snail-schistosome dynamics in 109 ponds of variable ephemerality in Tanzania. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and cercariae release, though of lower magnitude in the fully desiccating ponds than non-desiccating ponds. Second, we evaluated total yearly prevalence across a gradient of an ephemerality, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

Coinfection rates of avian blood parasites increase with latitude in parapatric host species.

Animals are frequently coinfected with multiple parasites concurrently, and advances in our sampling of these complex intra-host parasite communities have revealed important ecological impacts on their hosts. However, the spatial distributions and environmental determinants of parasite coinfection remain infrequently studied. Here, we investigated the drivers of haemosporidian blood parasite coinfection in the Bicknell's thrush (Catharus bicknelli) and grey-cheeked thrush (Catharus minimus), parapatric sister species that occur across a broad latitudinal range in northern North America. Using 298 samples from across the distributions of these species, we found high overall infection (86%) and coinfection (41%) rates within host populations. Coinfection rates within populations were highly variable across sampling sites, ranging from 7 to 75%. Latitude was a more important predictor of coinfection frequency than host species identity, with coinfections becoming more abundant at higher latitudes. The 2 host species exhibited similar parasite faunas, and an analysis of the co-occurrence patterns among haemosporidians showed that host species identity was largely not a factor in structuring which parasites were found within coinfections. To our knowledge, this is the first study to illustrate a reverse latitudinal gradient in coinfection frequency in a eukaryotic parasite system. Further work is necessary to determine whether vector ecology or some other factor is the primary proximate driver of this pattern.

Snail juvenile growth rate as a rapid predictor of the transmission potential of parasitizing human schistosomes.

Host and parasite traits that are sensitive to environmental perturbations merit special attention in the mitigation of diseases. While life table experiments allow a practical evaluation of variability of these traits with environmental change, they are cost and resource intensive. Here, we use a model snail host-trematode parasite system to test the efficacy of an expeditious alternative. Rapidly changing host traits (such as juvenile growth rate) can be used as effective predictors of parasite transmission potential across a range of environmental factors. This approach can be applied to anticipate epidemiological changes under diverse environmental scenarios.

Cascading impacts of host seasonal adaptation on parasitism.

The persistence of parasite populations through harsh seasonal bouts is often critical to circannual disease outbreaks. Parasites have a diverse repertoire of phenotypes for persistence, ranging from transitioning to a different life stage better suited to within-host dormancy to utilizing weather-hardy structures external to hosts. While these adaptive traits allow parasite species to survive through harsh seasons, it is often at survival rates that threaten population persistence. We argue that these periods of parasite (and vector) population busts could be ideal targets for disease intervention. As climate change portends abbreviated host dormancy and extended transmission periods in many host-parasite systems, it is essential to identify novel pathways to shore up current disease-intervention strategies.

Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts.

Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.

Drivers of community turnover differ between avian hemoparasite genera along a North American latitudinal gradient.

The latitudinal diversity gradient (LDG) is an established macroecological pattern, but is poorly studied in microbial organisms, particularly parasites. In this study, we tested whether latitude, elevation, and host species predicted patterns of prevalence, alpha diversity, and community turnover of hemosporidian parasites. We expected parasite diversity to decrease with latitude, alongside the diversity of their hosts and vectors. Similarly, we expected infection prevalence to decrease with latitude as vector abundances decrease. Lastly, we expected parasite community turnover to increase with latitudinal distance and to be higher between rather than within host species. We tested these hypotheses by screening blood and tissue samples of three closely related avian species in a clade of North American songbirds (Turdidae: Catharus, n = 466) across 17.5° of latitude. We used a nested PCR approach to identify parasites in hemosporidian genera that are transmitted by different dipteran vectors. Then, we implemented linear-mixed effects and generalized dissimilarity models to evaluate the effects of latitude, elevation, and host species on parasite metrics. We found high diversity of hemosporidian parasites in Catharus thrushes (n = 44 lineages) but no evidence of latitudinal gradients in alpha diversity or prevalence. Parasites in the genus Leucocytozoon were most prevalent and lineage rich in this study system; however, there was limited turnover with latitude and host species. Contrastingly, Plasmodium parasites were less prevalent and diverse than Leucocytozoon parasites, yet communities turned over at a higher rate with latitude and host species. Leucocytozoon communities were skewed by the dominance of one or two highly prevalent lineages with broad latitudinal distributions. The few studies that evaluate the hemosporidian LDG do not find consistent patterns of prevalence and diversity, which makes it challenging to predict how they will respond to global climate change.