PhD Candidate, University of Alberta, School of Public Health
I study ecological, host-parasite interactions important to disease transmission.
Freshwater snails are an important host for tens of thousands of parasites called trematodes. Trematodes are flatworms that have complex life cycles, meaning they use more than one host during their life time. Snails are the host in which they complete the first stage of their larval development, and where they amplify their numbers to increase their chances of reaching the next host in their life cycle. Trematodes, in their adult worm form, can be found to infect nearly every animal group, including humans. Certain species of trematode are known to cause the allergic condition, commonly called swimmer’s itch. This is a rash commonly contracted by swimmers in freshwater lakes, when avian trematode larvae emerge from snails and penetrate human skin. Though historically swimmer’s itch has been in Canada (and worldwide) for a very long time, there has not been much research dedicated to understanding transmission of this condition. My research aims to look at the relationship between snails and their invading trematode parasites within freshwater ecosystems to better understand when and where peaks in transmission may occur. Rather than looking at only the species that cause swimmer’s itch, I am adopting a community-based approach to incorporate the interactions among all trematode and snail species present. I am also measuring environmental variables that may have an affect on species presence and persistence. This information will be used to inform swimmer’s itch control methods in Alberta, but will also broadly contribute to our general understanding of trematode communities among their snail hosts. This will hopefully provide important insight for researchers working on trematode diseases that go beyond the skin and cause true disease in humans, such as Schistosomiasis in sub-Saharan Africa; a disease caused by a closely related trematode species to that which causes swimmer’s itch.
Abstract: Community genetics aims at understanding how within-species variation, species diversity and environmental factors interact to shape community assembly. An approach that emerged a few years ago has been to quantify the correlation between the neutral genetic diversity of a focal species and species diversity of the surrounding community (species–genetic diversity correlations, or SGDCs). We here review this approach and discuss its interpretative framework in a community ecology context. First, we show that the case for mostly positive SGDCs is probably overstated due to publication bias – only 11% are significantly positive, a fraction comparable to the significantly negative ones. This suggests that variation in area and connectivity among habitat patches, theoretically leading to positive SGDCs, is not the only factor affecting SGDCs. Second, building upon previous contributions, we propose a general framework to identify the multiple factors underpinning SGDCs, and argue that it will help deepen our understanding of community assembly, especially with regard to the ecological factors playing at metacommunity scale. Our framework distinguishes between site and community factors which can affect SGDCs either positively or negatively, depending on whether the focal species and the rest of the community are similar or dissimilar, in terms of realized niches and dispersal abilities. Empirical studies should thus go beyond simply computing SGDCs, and we provide statistical methods (e.g. structural equation modelling) to decompose SGDCs into the multiple contributions of site and community factors. As an example, we use a published dataset (freshwater snail metacommunity), and show how the role of focal population size on SGDCs had hitherto not been detected. We further discuss how considering several focal species and various delimitations of the community may help one to identify clusters of ecologically similar species. We eventually highlight the benefit that SGDC studies would get from integrating β-diversities.
Pub.: 15 Feb '17, Pinned: 01 Sep '17
Abstract: Cryptic parasite diversity is a major issue for taxonomy and systematics, and for attempts to control diseases of humans, domestic animals and wildlife. Here, we re-examine an earlier report that, after correcting for sampling effort, more cryptic species of trematodes are found per published study than for other helminth taxa. We performed a meta-analysis of 110 studies that used DNA sequences to search for cryptic species in parasitic helminth taxa. After correcting for study effort and accounting for the biogeographical region of origins, we found that more cryptic species tend to be uncovered among trematodes, and fewer among cestodes and animal-parasitic nematodes, than in other helminth groups. However, this pattern was only apparent when we included only studies using nuclear markers in the analysis; it was not seen in a separate analysis based only on mitochondrial markers. We propose that the greater occurrence of cryptic diversity among trematodes may be due to some of their unique features, such as their mode of reproduction or frequent lack of hard morphological structures, or to the way in which trematode species are described. Whatever the reason, the high frequency of cryptic species among trematodes has huge implications for estimates of parasite diversity and for future taxonomic research.
Pub.: 07 Mar '17, Pinned: 01 Sep '17
Abstract: For many parasites, the full set of hosts that are susceptible to infection is not known, and this could lead to a bias in estimates of transmission. We used counts of individual adult parasites from historical parasitology studies in southern Africa to map a bipartite network of the nematode parasites of herbivore hosts that occur in Botswana. Bipartite networks are used in community ecology to represent interactions across trophic levels. We used a Bayesian hierarchical model to predict the full set of host-parasite interactions from existing data on parasitic gastrointestinal nematodes of wild and domestic ungulates given assumptions about the distribution of parasite counts within hosts, while accounting for the relative uncertainty of less sampled species. We used network metrics to assess the difference between the observed and predicted networks, and to explore the connections between hosts via their shared parasites using a host-host unipartite network projected from the bipartite network. The model predicts a large number of missing links and identifies red hartebeest, giraffe and steenbok as the hosts that have the most uncertainty in parasite diversity. Further, the unipartite network reveals clusters of herbivores that have a high degree of parasite sharing, and these clusters correspond closely with phylogenetic distance rather than with the wild/domestic boundary. These results provide a basis for predicting the risk of cross-species transmission of nematode parasites in areas where livestock and wildlife share grazing land.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.
Pub.: 16 Mar '17, Pinned: 01 Sep '17
Abstract: To identify trematode diversity and life-cycles in the sub-Arctic Lake Takvatn, Norway, we characterised 120 trematode isolates from mollusc first intermediate hosts, metacercariae from second intermediate host fishes and invertebrates, and adults from fish and invertebrate definitive hosts, using molecular techniques. Phylogenies based on nuclear and/or mtDNA revealed high species richness (24 species or species-level genetic lineages), and uncovered trematode diversity (16 putative new species) from five families typical in lake ecosystems (Allocreadiidae, Diplostomidae, Plagiorchiidae, Schistosomatidae and Strigeidae). Sampling potential invertebrate hosts allowed matching of sequence data for different stages, thus achieving molecular elucidation of trematode life-cycles and exploration of host-parasite interactions. Phylogenetic analyses also helped identify three major mollusc intermediate hosts (Radix balthica, Pisidium casertanum and Sphaerium sp.) in the lake. Our findings increase the known trematode diversity at the sub-Arctic Lake Takvatn, showing that digenean diversity is high in this otherwise depauperate sub-Arctic freshwater ecosystem, and indicating that sub-Arctic and Arctic ecosystems may be characterised by unique trematode assemblages.
Pub.: 21 Mar '17, Pinned: 01 Sep '17
Abstract: Community ecology aims to understand what factors determine the assembly and dynamics of species assemblages at different spatiotemporal scales. To facilitate the integration between conceptual and statistical approaches in community ecology, we propose Hierarchical Modelling of Species Communities (HMSC) as a general, flexible framework for modern analysis of community data. While non-manipulative data allow for only correlative and not causal inference, this framework facilitates the formulation of data-driven hypotheses regarding the processes that structure communities. We model environmental filtering by variation and covariation in the responses of individual species to the characteristics of their environment, with potential contingencies on species traits and phylogenetic relationships. We capture biotic assembly rules by species-to-species association matrices, which may be estimated at multiple spatial or temporal scales. We operationalise the HMSC framework as a hierarchical Bayesian joint species distribution model, and implement it as R- and Matlab-packages which enable computationally efficient analyses of large data sets. Armed with this tool, community ecologists can make sense of many types of data, including spatially explicit data and time-series data. We illustrate the use of this framework through a series of diverse ecological examples.
Pub.: 20 Mar '17, Pinned: 01 Sep '17
Abstract: Understanding temporal variation of host-pathogen dynamics can be important for predicting disease risks and anticipating how disease systems may change in response to natural or human disturbances. Seasonal changes in weather, especially those associated with changes in temperature or precipitation, are often a key component of temporal changes in infection risk and can have important impacts on disease systems. However, these patterns can be difficult to track due to interannual variation and the need for longer-term, multi-year surveillance efforts. We assessed seasonal and annual changes in the trematode component community of first-intermediate host stream snails, Elimia (= Oxytrema = Goniobasis) proxima, across 5 streams in the southern Appalachian Mountains. Over 3 yr, we found no evidence of consistent seasonal peaks of trematode infection in E. proxima. There was some across site consistency in infection prevalence over 4 yr, as high prevalence sites tended to maintain higher prevalence from year to year, relative to lower prevalence sites. Additionally, we examined the relationship between prevalence of first-intermediate host infection, weather variables and site-level factors, including snail density and water quality metrics. Trematode prevalence was negatively related to total precipitation, which may have been due to the movement of infectious parasite stages and hosts downstream during high flows. We found no strong relationships between trematode prevalence and snail density or any of the water quality metrics examined in this study, indicating that snail infection may be driven primarily by definitive host activity.
Pub.: 30 Mar '17, Pinned: 01 Sep '17
Abstract: Macroecological models for predicting species distributions usually only include abiotic environmental conditions as explanatory variables, despite knowledge from community ecology that all species are linked to other species through biotic interactions. This disconnect is largely due to the different spatial scales considered by the two sub-disciplines: macroecologists study patterns at large extents and coarse resolutions, while community ecologists focus on small extents and fine resolutions. A general framework for including biotic interactions in macroecological models would help bridge this divide, as it would allow for rigorous testing of the role that biotic interactions play in determining species ranges. Here, we present an approach that combines species distribution models with Bayesian networks, which enables the direct and indirect effects of biotic interactions to be modelled as propagating conditional dependencies among species' presences. We show that including biotic interactions in distribution models for species from a California grassland community results in better range predictions across the western USA. This new approach will be important for improving estimates of species distributions and their dynamics under environmental change.
Pub.: 22 Apr '17, Pinned: 01 Sep '17
Abstract: Reciprocal coevolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population- or genotype-specific evolutionary change. These host-parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of coevolving host-parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its coevolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus-infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population-level coevolution is leading to population-specific host-parasite interactions and evolutionary trajectories. We also used an FST -based approach to identify a set of loci that represent promising candidates for targets of parasite-mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population-specific responses to coevolving infection in the P. antipodarum-Microphallus interaction and provide new insights into the genomic basis of coevolutionary interactions in nature. This article is protected by copyright. All rights reserved.
Pub.: 22 Apr '17, Pinned: 01 Sep '17
Abstract: Factors that drive parasite specificity and differences in infection dynamics among alternative host species are important for ecology and evolution of host-parasite interactions, but still often poorly known in natural systems. Here, we investigated spatiotemporal dynamics of infection, host susceptibility and parasite-induced changes in host phenotype in a rarely explored host-parasite system, the Australapatemon sp. trematode infecting two sympatric species of freshwater leeches, Erpobdella octoculata and Helobdella stagnalis. We show significant variation in infection abundance between the host species in both space and time. Using experimental infections, we also show that most of this variation likely comes from interspecific differences in exposure rather than susceptibility. Moreover, we demonstrate that the hiding behaviour of E. octoculata, but not that of H. stagnalis, was impaired by the infection irrespective of the parasite abundance. This may increase susceptibility of E. octoculata to predation by the final avian host. We conclude that differences in patterns of infection and in behavioural alterations among alternative sympatric host species may arise in narrow spatial scales, which emphasises the importance of local infection and transmission dynamics for parasite life cycles.
Pub.: 16 May '17, Pinned: 01 Sep '17
Abstract: Most species aggregate in local patches. High host density in patches increases contact rate between hosts and parasites, increasing parasite transmission success. At the same time, for environmentally-transmitted parasites, high host density can decrease infection risk to individual hosts, because infective stages are divided among all hosts in a patch, leading to safety in numbers. We tested these predictions using the California horn snail, Cerithideopsis californica (=Cerithidea californica), which is the first intermediate host for at least 19 digenean trematode species in California estuaries. Snails become infected by ingesting trematode eggs or through penetration by free-swimming miracidia that hatch from trematode eggs deposited with final-host (bird or mammal) feces. This complex life cycle decouples infective-stage production from transmission, raising the possibility of an inverse relationship between host density and infection risk. In a field survey, higher snail density was associated with increased trematode (infected snail) density, but decreased trematode prevalence, consistent with either safety in numbers, parasitic castration, or both. To determine the extent to which safety in numbers drove the negative snail density-trematode prevalence association, we manipulated uninfected snail density in 83 cages at eight sites within Carpinteria Salt Marsh (CA, USA). At each site, we quantified snail density and used data on final-host (bird and raccoon) distributions to control for between-site variation in infective-stage supply. After three months, overall trematode infections per cage increased with snail-biomass density. For egg-transmitted trematodes, per-snail infection risk decreased with snail-biomass density in the cage and surrounding area, whereas per-snail infection risk did not decrease for miracidium-transmitted trematodes. Furthermore, both trematode recruitment and infection risk increased with infective-stage input, but this was significant only for miracidium-transmitted species. A model parameterized with our experimental results and snail densities from 524 field transects estimated that safety in numbers, when combined with host aggregation, halved per-capita infection risk in this snail population. We conclude that, depending on transmission mode, host density can enhance parasite recruitment and reduce per-capita infection risk. This article is protected by copyright. All rights reserved.
Pub.: 19 May '17, Pinned: 01 Sep '17
Abstract: Community assembly processes is the primary focus of community ecology. Using phylogenetic-based and functional trait-based methods jointly to explore these processes along environmental gradients are useful ways to explain the change of assembly mechanisms under changing world. Our study combined these methods to test assembly processes in wide range gradients of elevation and other habitat environmental factors. We collected our data at 40 plots in Taibai Mountain, China, with more than 2,300 m altitude difference in study area and then measured traits and environmental factors. Variance partitioning was used to distinguish the main environment factors leading to phylogeny and traits change among 40 plots. Principal component analysis (PCA) was applied to colligate other environment factors. Community assembly patterns along environmental gradients based on phylogenetic and functional methods were studied for exploring assembly mechanisms. Phylogenetic signal was calculated for each community along environmental gradients in order to detect the variation of trait performance on phylogeny. Elevation showed a better explanatory power than other environment factors for phylogenetic and most traits’ variance. Phylogenetic and several functional structure clustered at high elevation while some conserved traits overdispersed. Convergent tendency which might be caused by filtering or competition along elevation was detected based on functional traits. Leaf dry matter content (LDMC) and leaf nitrogen content along PCA 1 axis showed conflicting patterns comparing to patterns showed on elevation. LDMC exhibited the strongest phylogenetic signal. Only the phylogenetic signal of maximum plant height showed explicable change along environmental gradients. Synthesis. Elevation is the best environment factors for predicting phylogeny and traits change. Plant's phylogenetic and some functional structures show environmental filtering in alpine region while it shows different assembly processes in middle- and low-altitude region by different trait/phylogeny. The results highlight deterministic processes dominate community assembly in large-scale environmental gradients. Performance of phylogeny and traits along gradients may be independent with each other. The novel method for calculating functional structure which we used in this study and the focus of phylogenetic signal change along gradients may provide more useful ways to detect community assembly mechanisms.
Pub.: 02 Jun '17, Pinned: 01 Sep '17
Abstract: Large quantities of road salts are used for de-icing in temperate climates but often leach into aquatic ecosystems where they can cause harm to inhabitants, including reduced growth and survival. However, the implications of road salt exposure for aquatic animal susceptibility to pathogens and parasites have not yet been examined even though infectious diseases can significantly contribute to wildlife population declines. Through a field survey, we found a range of NaCl concentrations (50-560mg/L) in ponds known to contain larval amphibians, with lower levels found in sites close to gravel- rather than hard-surfaced roads. We then investigated how chronic exposure to environmentally-realistic levels of road salt (up to 1140mg/L) affected susceptibility to infection by trematode parasites (helminths) in larval stages of two amphibian species (Lithobates sylvaticus - wood frogs, and L. pipiens - northern leopard frogs) by considering effects on host anti-parasite behavior and white blood cell profiles. Wood frogs exposed to road salt had higher parasite loads, and also exhibited reduced anti-parasite behavior in these conditions. In contrast, infection intensity in northern leopard frogs had a non-monotonic response to road salts even though lymphocytes were only elevated at the highest concentration. Our results indicate the potential for chronic road salt exposure to affect larval amphibian susceptibility to pathogenic parasites through alterations of behavior and immunocompetence, with further studies needed at higher concentrations, as well as that of road salts on free-living parasite infectious stages.
Pub.: 06 Jun '17, Pinned: 01 Sep '17
Abstract: Parasites competing over limited host resources are faced with a tradeoff between reproductive success and host overexploitation jeopardizing survival. Surprisingly little is known about the outcome of such competitive scenarios, and we therefore aimed at elucidating interactions between the trematodes Himasthla elongata and Renicola roscovita coinfecting the periwinkle first intermediate host. The results show that the success of Himasthla colonies (rediae) in terms of cercarial emission is unaffected by Renicola competition (sporocysts), whereas deteriating host condition decreases fitness. Furthermore, double infection has no bearing on Himasthla's colony size but elevated the proportion of non-reproductive rediae that play a decisive role in colony defence. Opposite, the development of the Renicola colony (size/maturity), and in turn fitness, is markedly reduced in presence of Himasthla, whereas the nutritional state of the host appears less important. Hence, the intramolluscan competition between Himasthla and Renicola is asymmetrical, Himasthla being the superior competitor. Himasthla not only adjusts its virulence according to the hosts immediate nutritional state, it also nullifies the negative impact of a heterospecific competitor on own fitness. The latter is argued to follow in part from direct predation on the competitor, for which purpose more defensive non-reproductive rediae are strategically produced.
Pub.: 28 Jun '17, Pinned: 01 Sep '17
Abstract: Parasite distributions are constantly changing due to climate change, local and global movement of animals and humans, as well as land use and habitat change. The trematode Dicrocoelium dendriticum is a relatively recent invader of Canada, being first reported in eastern Canada in the 1930s and western Canada in the 1970s. However, historical records are scarce and its emergence is poorly understood. The establishment of this parasite in Canada provides an interesting opportunity to explore the use of population genetic approaches to help elucidate the invasion history of a relatively recently established helminth parasite. In this study, we compare the genetic diversity and population structure of a number of D. dendriticum populations from western and eastern Canada, and compare these with much longer established European populations. Two independent genetic marker systems were used; a microsatellite marker panel and a cytochrome c oxidase 1 (cox1) mitochondrial (mt)DNA sequence marker. We found distinct differences in both genetic diversity and population structure of the different Canadian populations that provide insights into their invasion histories compared with the European populations. Two populations from British Columbia, Canada - Salt Spring and Vancouver Islands - are of low diversity, show evidence of a population bottleneck and are closely related to each other, suggesting a shared recent history of establishment. These west coast populations are otherwise most closely related to those from eastern Canada and western Europe, and in contrast are genetically divergent from those in Cypress Hills, Alberta, Canada. Although the Alberta parasite population is the most recently reported in Canada, being first identified there in the early 1990s, it was the most genetically diverse of those examined and showed a strong pattern of admixture of genotypes present in western and eastern Europe. Overall, our results are consistent with a model in which western Europe is likely the source of flukes on the east coast of Canada, which were then subsequently translocated to the west coast of Canada. The most recently reported D. dendriticum population in Canada appears to have a different history and likely has multiple origins.
Pub.: 03 Jul '17, Pinned: 01 Sep '17
Abstract: Rapid losses of biodiversity due to the changing landscape have spurred increased interest in the role of species diversity and disease risk. A leading hypothesis for the importance of biodiversity in disease reduction is the dilution effect, which suggests that increasing species diversity within a system decreases the risk of disease among the organisms inhabiting it. The role of species diversity in trematode infection was investigated using field studies from sites across the U.S. to examine the impact of snail diversity in the infection dynamics of both first and second intermediate larval stages of Echinostoma spp. parasites. The prevalence of Echinostoma spp. sporocysts/rediae infection was not affected by increases in snail diversity, but significant negative correlations in metacercariae prevalence and intensity with snail diversity were observed. Additionally, varying effectiveness of the diluting hosts was found, i.e., snail species that were incompatible first intermediate hosts for Echinostoma spp. were more successful at diluting the echinostome parasites in the focal species, while H. trivolvis, a snail species that can harbor the first intermediate larval stages, amplified infection. These findings have important implications not only on the role of species diversity in reducing disease risk, but the success of the parasites in completing their life cycles and maintaining their abundance within an aquatic system.
Pub.: 07 Jul '17, Pinned: 01 Sep '17
Abstract: Digenean trematode distributions, compatibility profiles with their snail hosts, and complete life cycles remain mysteries in many parts of the world. Surveys of digenean biology and ecology provide further insight and perspective into just how incredibly diverse and important helminth parasites are in shaping local ecosystems. Past surveys have provided substantial characterizations of adult digeneans within their definitive hosts, and many now have contributed toward furthering our understanding of larval digeneans within their intermediate host communities. However, much information about the diversity of digeneans and their relationships with their snail intermediate hosts are lacking in many locations across the globe. This is certainly true in Canada, where few records related to digenean-snail relationships exist. Currently, there is a need for more information about the presence and distribution of digeneans across Canada, and how this compares to other parts of North America and beyond. To address this diversity gap in Western Canada, six lakes within central Alberta were surveyed for the presence of snails and larval digenean species and their associations. This investigation into the diversity of digeneans utilized a combined approach of morphological and molecular tools to identify 39 digenean species among five snail host species, from biweekly collections, taken over the course of 2 years (2013-2014). Here, digenean-snail combinations, presence, and distribution across sampling sites and lakes are reported. Overall, this survey contributes new information toward digenean-snail compatibility, life cycles, and distribution in Northern lake ecosystems within North America.
Pub.: 02 Jun '16, Pinned: 23 Aug '17
Abstract: Zygocercous (aggregating) cercarial larvae were recently discovered emerging from a physid snail during a molecular survey of cercariae from molluscs in lakes in central Alberta, Canada. This manuscript delves into the characterization of these cercariae through morphological and molecular techniques and provides the first genetic information for a zygocercous larval trematode. Analyses of cytochrome c oxidase I of mitochondrial DNA and two partial regions of nuclear ribosomal DNA sequences revealed the zygocercous cercariae to belong to the genus Australapatemon Sudarikov, 1959. Further analyses of sequences of Australapatemon burti (Miller, 1923), from cercariae and adults collected from across North America, indicate a complex of nine genetically-distinct lineages within this species, a surprising level of diversity. The zygocercous cercariae, along with adult worms collected from ducks in Manitoba, Canada, and from Mexico, represent one of these lineages, and are herein described as Australapatemon mclaughlini n. sp. Seven lineages cannot yet be identified, but one is tentatively identified as Australapatemon burti.
Pub.: 18 Jun '17, Pinned: 23 Aug '17
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