Project

Global spread of parasites at the human - domestic animal - wildlife interface

Goal: We study patterns of parasite sharing between domestic animals and wildlife to better understand how anthropogenic change will impact parasite spread and disease emergence. Our work focuses on a number of host-parasite systems, including mammalian helminths, arthropod ectoparasites and avian malaria.

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Konstans Wells
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Emerging infectious diseases arising from pathogen spillover from mammals to humans constitute a substantial health threat. Tracing virus origin and predicting the most likely host species for future spillover events are major objectives in One Health disciplines. We assessed patterns of virus sharing among a large diversity of mammals, including humans and domestic species. We used network centrality analysis and trait‐based Bayesian hierarchical models to explore patterns of virus sharing among mammals. We analysed a global database that compiled the associations between 1,785 virus species and 725 mammalian host species as sourced from automatic screening of meta‐data accompanying published nucleotide sequences between 1950 and 2019. We show that based on current evidence, domesticated mammals hold the most central positions in networks of known mammal–virus associations. Among entire host–virus networks, Carnivora and Chiroptera hold central positions for mainly sharing RNA viruses, whereas ungulates hold central positions for sharing both RNA and DNA viruses with other host species. We revealed strong evidence that DNA viruses were phylogenetically more host specific than RNA viruses. RNA viruses exhibited low functional host specificity despite an overall tendency to infect phylogenetically related species, signifying high potential to shift across hosts with different ecological niches. The frequencies of sharing viruses among hosts and the proportion of zoonotic viruses in hosts were larger for RNA than for DNA viruses. Acknowledging the role of domestic species in addition to host and virus traits in patterns of virus sharing is necessary to improve our understanding of virus spread and spillover in times of global change. Understanding multi‐host virus‐sharing pathways adds focus to curtail disease spread.
Konstans Wells
added a research item
Host specificity encompasses the range and diversity of host species that a parasite is capable of infecting and is considered a crucial measure of a parasite’s potential to shift hosts and trigger disease emergence. Yet empirical studies rarely consider that regional observations only reflect a parasite’s ‘realized’ host range under particular conditions: the true ‘fundamental’ range of host specificity is typically not approached. We provide an overview of challenges and directions in modelling host specificity under variable environmental conditions. Combining tractable modelling frameworks with multiple data sources that account for the strong interplay between a parasite's evolutionary history, transmission mode, and environmental filters that shape host–parasite interactions will improve efforts to quantify emerging disease risk in times of global change.
Nicholas Clark
added a research item
The cat flea (Ctenocephalides felis) is the most common parasite of domestic cats and dogs worldwide. Due to the morphological ambiguity of C. felis and a lack of — particularly largescale — phylogenetic data, we do not know whether global C. felis populations are morphologically and genetically conserved, or whether human-mediated migration of domestic cats and dogs has resulted in homogenous global populations. To determine the ancestral origin of the species and to understand the level of global pervasion of the cat flea and related taxa, our study aimed to document the distribution and phylogenetic relationships of Ctenocephalides fleas found on cats and dogs worldwide. We investigated the potential drivers behind the establishment of regional cat flea populations using a global collection of fleas from cats and dogs across six continents. We morphologically and molecularly evaluated six out of the 14 known taxa comprising genus Ctenocephalides, including the four original C. felis subspecies (Ctenocephalides felis felis, Ctenocephalides felis strongylus, Ctenocephalides felis orientis and Ctenocephalides felis damarensis), the cosmopolitan species Ctenocephalides canis and the African species Ctenocephalides connatus. We confirm the ubiquity of the cat flea, representing 85% of all fleas collected (4357/5123). Using a multigene approach combining two mitochondrial (cox1 and cox2) and two nuclear (Histone H3 and EF-1α) gene markers, as well as a cox1 survey of 516 fleas across 56 countries, we demonstrate out-of-Africa origins for the genus Ctenocephalides and high levels of genetic diversity within C. felis. We define four bioclimatically limited C. felis clusters (Temperate, Tropical I, Tropical II and African) using maximum entropy modelling. This study defines the global distribution, African origin and phylogenetic relationships of global Ctenocephalides fleas, whilst resolving the taxonomy of the C. felis subspecies and related taxa. We show that humans have inadvertently precipitated the expansion of C. felis throughout the world, promoting diverse population structure and bioclimatic plasticity. By demonstrating the link between the global cat flea communities and their affinity for specific bioclimatic niches, we reveal the drivers behind the establishment and success of the cat flea as a global parasite.
Nicholas Clark
added a research item
Biogeographic patterns of parasite diversity are useful for determining how host-parasite interactions can influence speciation. However, variation in methodologies and sampling effort can skew diversity estimates. Avian haemosporidians are vector-transmitted blood parasites represented by over 1300 unique genetic lineages spread across over 40 countries. We used a global database of lineage distributions for two avian haemosporidian genera, Plasmodium and Haemoproteus, to test for congruence of diversity among haemosporidians and their avian hosts across 13 geographic regions. We demonstrated that avian haemosporidians exhibit similar diversity patterns to their avian hosts; however, specific patterns differ between genera. Haemoproteus spp. diversity estimates were significantly higher than those of Plasmodium spp. in all areas where the genera co-occurred, apart from the Plasmodium spp.-rich region of South America. The geographic distributions of parasite genera also differed, with Haemoproteus spp. absent from the majority of oceanic regions while Plasmodium spp. were cosmopolitan. These findings suggest fundamental differences in the way avian haemosporidians diverge and colonise new communities. Nevertheless, a review of the literature suggests that accurate estimates of avian haemosporidian diversity patterns are limited by (i) a concentration of sampling towards passerines from Europe and North America, (ii) a frequent failure to include microscopic techniques together with molecular screening and (iii) a paucity of studies investigating distributions across vector hosts.
Konstans Wells
added an update
New research investigating global patterns in helminth host specificity just accepted in Ecography:
Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter
Host specificity has a major influence on a parasite’s ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world’s most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4-10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo-Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hydatigera taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host-parasite systems and will provide key insights into parasite invasion potential at regional and global scales.
 
Nicholas Clark
added a research item
Aim Characterizing macroecological patterns in biodiversity is key to improve our understanding of community assembly. Global biodiversity for many taxa follows a latitudinal gradient, with increased diversity in tropical latitudes. Less is known about global parasite biodiversity, inhibiting our ability to predict how global change will impact parasitic disease emergence. Using distribution and phylogenetic data for 2,386 avian haemosporidian blood parasites (genera Plasmodium, Haemoproteus and Leucocytozoon), I assessed how contemporary and historical drivers influence the composition of parasite communities worldwide. Location Global. Time period Current. Major taxa studied Haemosporidian blood parasites. Methods Parasite distribution and cytochrome b sequence data were accessed from an open‐source database. Bayesian phylogenetic tree distributions were constructed for each parasite genus using two substitution models to capture uncertainty. Hierarchical regressions assessed effects of environmental variation, latitude and phylogenetic β‐diversity (βdiv; a proxy for phylogenetic uniqueness) on the diversity and asymmetry of parasite communities around the globe. Results I uncovered biodiversity hotspots and identified broad variation in global diversity patterns among parasite genera. Community diversity increased with increasing phylogenetic uniqueness for all three parasite genera; however, these diverse and unique regions did not consistently occur in the tropics. I found no evidence of a latitudinal diversity gradient, and support for a latitudinal gradient in community phylogenetic asymmetry was weak. Main conclusions Global variation in avian haemosporidian phylogenetic diversity does not reflect a latitudinal gradient. Instead, parasite biogeography may reflect fundamental differences in host‐switching tendencies or the timing of avian evolutionary radiations. Examining the interplay between shared evolutionary history and phylogenetic diversity can provide important insights into the drivers of parasite biodiversity at global scales.
Konstans Wells
added a research item
Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the strength of biotic and biogeographical factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite (Nematoda, Cestoda, Trematoda) sharing between mammalian wildlife species and domestic mammal hosts (including humans) using >24,000 unique country-level records of host–parasite associations. We used hierarchical modelling and species trait data to determine possible drivers of the level of parasite sharing between wildlife species and either humans or domestic animal hosts. We found the diet of wildlife species to be a strong predictor of levels of helminth parasite sharing with humans and domestic animals, followed by a moderate effect of zoogeographical region and minor effects of species’ habitat and climatic niches. Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species (including humans). These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species. If the dietary profile and position in the trophic chain of a wildlife species largely drives its level of helminth parasite sharing with humans/domestic animals, future range shifts of host species that result in novel trophic interactions may likely increase parasite host shifting and have important ramifications for human and animal health.
Nicholas Clark
added an update
A nice and descriptive news article covering our research on the spread of fleas from pets / feral animals to wildlife has just been published in The Conversation. Have a read here to find out more:
 
Konstans Wells
added an update
New research studying “Global spread of helminth parasites at the human – domestic animal – wildlife interface” just accepted in Global Change Biology.
“Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite sharing between mammalian wildlife species and domestic mammal hosts (including humans). Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species. These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species.”
Details and full text links to follow soon!
 
Nicholas Clark
added 2 research items
Tracing the temporal dynamics of pathogens is crucial for developing strategies to detect and limit disease emergence. Canine parvovirus (CPV-2) is an enteric virus causing morbidity and mortality in dogs around the globe. Previous work in Australia reported that the majority of cases were associated with the CPV-2a subtype, an unexpected finding since CPV-2a was rapidly replaced by another subtype (CPV-2b) in many countries. Using a nine-year dataset of CPV-2 infections from 396 dogs sampled across Australia, we assessed the population dynamics and molecular epidemiology of circulating CPV-2 subtypes. Bayesian phylogenetic Skygrid models and logistic regressions were used to trace the temporal dynamics of CPV-2 infections in dogs sampled from 2007 to 2016. Phylogenetic models indicated that CPV-2a likely emerged in Australia between 1973 and 1988, while CPV-2b likely emerged between 1985 and 1998. Sequences from both subtypes were found in dogs across continental Australia and Tasmania, with no apparent effect of climate variability on subtype occurrence. Both variant subtypes exhibited a classical disease emergence pattern of relatively high rates of evolution during early emergence followed by subsequent decreases in evolutionary rates over time. However, the CPV-2b subtype maintained higher mutation rates than CPV-2a and continued to expand, resulting in an increase in the probability that dogs will carry this subtype over time. Ongoing monitoring programs that provide molecular epidemiology surveillance will be necessary to detect emergence of new variants and make informed recommendations to develop reliable detection and vaccine methods.
[Background] Spillover of parasites at the domestic animal - wildlife interface is a pervasive threat to animal health. Cat and dog fleas (Ctenocephalides felis and C. canis) are among the world’s most invasive and economically important ectoparasites. Although both species are presumed to infest a diversity of host species across the globe, knowledge on their distributions in wildlife is poor. We built a global dataset of wild mammal host associations for cat and dog fleas, and used Bayesian hierarchical models to identify traits that predict wildlife infestation probability. We complemented this by calculating functional-phylogenetic host specificity to assess whether fleas are restricted to hosts with similar evolutionary histories, diet or habitat niches. [Results] Over 130 wildlife species have been found to harbour cat fleas, representing nearly 20% of all mammal species sampled for fleas. Phylogenetic models indicate cat fleas are capable of infesting a broad diversity of wild mammal species through ecological fitting. Those that use anthropogenic habitats are at highest risk. Dog fleas, by contrast, have been recorded in 31 mammal species that are primarily restricted to certain phylogenetic clades, including canids, felids and murids. Both flea species are commonly reported infesting mammals that are feral (free-roaming cats and dogs) or introduced (red foxes, black rats and brown rats), suggesting the breakdown of barriers between wildlife and invasive reservoir species will increase spillover at the domestic animal - wildlife interface. [Conclusions] Our empirical evidence shows that cat fleas are incredibly host-generalist, likely exhibiting a host range that is among the broadest of all ectoparasites. Reducing wild species’ contact rates with domestic animals across natural and anthropogenic habitats, together with mitigating impacts of invasive reservoir hosts, will be crucial for reducing invasive flea infestations in wild mammals.
Nicholas Clark
added an update
New research investigating patterns of host-specificity and geographic spread of domestic fleas just accepted in Parasites & Vectors. Watch this space for details and full text links
 
Nicholas Clark
added a project goal
We study patterns of parasite sharing between domestic animals and wildlife to better understand how anthropogenic change will impact parasite spread and disease emergence. Our work focuses on a number of host-parasite systems, including mammalian helminths, arthropod ectoparasites and avian malaria.
 
Nicholas Clark
added 2 research items
Pathogens can influence the success of invaders. The Enemy Release Hypothesis predicts invaders encounter reduced pathogen abundance and diversity, while the Novel Weapons Hypothesis predicts invaders carry novel pathogens that spill over to competitors. We tested these hypotheses using avian malaria (haemosporidian) infections in the invasive myna (Acridotheres tristis), which was introduced to southeastern Australia from India and was secondarily expanded to the eastern Australian coast. Mynas and and native Australian birds were screened in the secondary introduction range for haemosporidians (Plasmodium and Haemoproteus spp.) and results were combined with published data from the myna's primary introduction and native ranges. We compared malaria prevalence and diversity across myna populations to test for Enemy Release and used phylogeographic analyses to test for exotic strains acting as Novel Weapons. Introduced mynas carried significantly lower parasite diversity than native mynas and significantly lower Haemoproteus prevalence than native Australian birds. Despite commonly infecting native species that directly co-occur with mynas, Haemoproteus spp. were only recorded in introduced mynas in the primary introduction range and were apparently lost during secondary expansion. In contrast, Plasmodium infections were common in all ranges and prevalence was significantly higher in both introduced and native mynas than in native Australian birds. Introduced mynas carried several exotic Plasmodium lineages that were shared with native mynas, some of which also infected native Australian birds and two of which are highly invasive in other bioregions. Our results suggest that introduced mynas may benefit through escape from Haemoproteus spp. while acting as important reservoirs for Plasmodium spp., some of which are known exotic lineages.
Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly. Australasia and Oceania. We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition. Parasites were more locally distinct (co-occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co-occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance. Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co-occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.
Konstans Wells
added 2 research items
Rickettsioses and bartonelloses are arthropod-borne diseases of mammals with widespread geographical distributions. Yet their occurrence in specific regions, their association with different vectors and hosts and the infection rate of arthropod-vectors with these agents remain poorly studied in South-east Asia. We conducted entomological field surveys in the Lao PDR (Laos) and Borneo, Malaysia by surveying fleas, ticks, and lice from domestic dogs and collected additional samples from domestic cows and pigs in Laos. Rickettsia felis was detected by real-time PCR with similar overall flea infection rate in Laos (76.6%, 69/90) and Borneo (74.4%, 268/360). Both of the encountered flea vectors Ctenocephalides orientis and Ctenocephalides felis felis were infected with R. felis. The degrees of similarity of partial gltA and ompA genes with recognized species indicate the rickettsia detected in two Boophilus spp. ticks collected from a cow in Laos may be a new species. Isolation and further characterization will be necessary to specify it as a new species. Bartonella clarridgeiae was detected in 3/90 (3.3%) and 2/360 (0.6%) of examined fleas from Laos and Borneo, respectively. Two fleas collected in Laos and one flea collected in Borneo were co-infected with both R. felis and B. clarridgeiae. Further investigations are needed in order to isolate these agents and to determine their epidemiology and aetiological role in unknown fever in patients from these areas.
AimGeographic spread and range expansion of species into novel environments may merge originally separated species assemblages, yet the possible drivers of geographic heterogeneity in host-parasite associations remain poorly understood. Here, we examine global patterns in the parasite assemblages of two rat species and explore the role of parasite acquisition from local pools of host species.LocationGlobal.Methods We compiled a global data set of helminth parasites (n = 241 species) from two rat species (Rattus rattus species complex, R. norvegicus) and, concomitantly, from all other mammal species known to be infected by the same parasites. We used an inverse Bayesian modelling approach to explicitly link species-level to community-level infestation probabilities at different geographic scales and alleviate the shortcoming of sampling bias.ResultsPatterns of species richness and turnover of parasites in the two focal rat species revealed clear biogeographic structure with lowest species richness and most distinct assemblages in Madagascar and highest species richness and least distinct assemblages in the Palaearctic region. Parasite species richness and turnover across regions were correlated for the two focal hosts, although they were associated with distinct assemblages within regions. Infection probability of a focal host with any given parasite was clearly related to infection probability of the local species pool of wildlife hosts with that same parasite. Infection probability of other mammal species infected with these parasite species, in turn, decreased with their taxonomic distance to the genus Rattus.Main conclusionsOur study demonstrates the importance of spillover of parasites from local wildlife hosts to invasive rats on global patterns of host-parasite associations. Considering both changes in local pools of host species and the global distributions of parasite and pathogen diversity in consistent model frameworks may therefore advance the forecasting of species-level infestation patterns and the possible risk of disease emergence from local to global scale.