Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements.

Schistosomatidae Stiles and Hassall 1898 is a medically significant family of digenetic trematodes (Trematoda: Digenea), members of which infect mammals or birds as definitive hosts and aquatic or amphibious gastropods as intermediate hosts. Currently, there are 17 named genera, for many of which evolutionary interrelationships remain unresolved. The lack of a resolved phylogeny has encumbered our understanding of schistosomatid evolution, specifically patterns of host-use and the role of host-switching in diversification. Here, we used targeted sequence capture of ultra-conserved elements (UCEs) from representatives of 13 of the 17 named genera and 11 undescribed lineages that are presumed to represent either novel genera or species to generate a phylogenomic dataset for the estimation of schistosomatid interrelationships. This study represents the largest phylogenetic effort within the Schistosomatidae in both the number of loci and breadth of taxon sampling. We present a near-comprehensive family-level phylogeny providing resolution to several clades of long-standing uncertainty within Schistosomatidae, including resolution for the placement of the North American mammalian schistosomes, implying a second separate capture of mammalian hosts. Additionally, we present evidence for the placement of Macrobilharzia at the base of the Schistosoma + Bivitellobilharzia radiation. Patterns of definitive and intermediate host use and a strong role for intermediate host-switching are discussed relative to schistosomatid diversification.

An outbreak of canine schistosomiasis in Utah: Acquisition of a new snail host (Galba humilis) by Heterobilharzia americana, a pathogenic parasite on the move.

Parasites with complex life cycles engaging multiple host species living among different environments well-exemplify the value of a cross-cutting One Health approach to understanding fundamental concerns like disease emergence or spread. Here we provide new information regarding a pathogenic schistosome trematode parasite of both wild and domestic mammals that has recently expanded its known range from mesic/wet environments of the southeastern United States to the arid southwest. In 2018, 12 dogs living near a man-made pond in Moab, Utah, were found positive for Heterobilharzia americana, the most westerly report of this endemic North American schistosome, and the first from Utah. Raccoon scats collected near the pond were positive for H. americana eggs, and snails living near the pond's water line identified as Galba humilis shed H. americana cercariae, the first indication of natural infections in this widespread North American snail species. The susceptibility of G. humilis to H. americana was confirmed experimentally. Our studies support the existence of two variants of H. americana and emphasize the need for further investigations of lymnaeids and their compatibility with H. americana, to better define the future potential for its spread. Capture of a new species of intermediate host vector snail and construction of man-made habitats suitable for this snail have created the potential for a much more widespread animal health problem, especially for dogs and horses. H. americana will prove difficult to control because of the role of raccoons in maintaining transmission and the amphibious habits of the snail hosts of this pathogenic schistosome.

Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes.

BACKGROUND: Physa acuta is a globally invasive freshwater snail native to North America. Prior studies have led to conflicting views of how P. acuta populations are connected and genetic diversity is partitioned globally. This study aims to characterize phylogeographic and population genetic structure within the native range of P. acuta, elucidate its invasion history and assess global patterns of genetic diversity. Further, using meta-analytic methods, we test the 'Enemy-Release hypothesis' within the P. acuta - digenetic trematode system. The 'Enemy-Release hypothesis' refers to the loss of native parasites following establishment of their host within an invasive range. Population genetic data is combined with surveys of trematode infections to map range-wide trematode species richness associated with P. acuta, and to identify relevant host-population parameters important in modeling host-parasite invasion. RESULTS: Phylogenetic analyses using mtDNA uncovered two major clades (A & B). Clade A occurs globally while clade B was only recovered from the Western USA. All invasive populations sampled grouped within Clade A, where multiple independent source populations were identified from across North America. Significant population genetic structure was found within the native range of P. acuta, with some evidence for contemporary geographic barriers between western and eastern populations. Mito-nuclear discordance was found suggesting historical isolation with secondary contact between the two mitochondrial clades. Trematode species richness was found to differ significantly between native and invasive populations, in concordance with the 'Enemy-Release hypothesis'. Further, our data suggests a positive relationship between nucleotide diversity of invasive populations and trematode prevalence and richness. CONCLUSIONS: This study includes a wider geographic sampling of P. acuta within its native range that provides insight into phylogeographic and population genetic structure, range-wide genetic diversity and estimation of the invasion history. Meta-analysis of P. acuta - trematode surveys globally is consistent with the 'Enemy-Release hypothesis'. Additionally, results from this study suggest that host demographic parameters, namely genetic diversity as a proxy for population size, may play an essential role in how parasite communities assemble within invasive host populations. This knowledge can be used to begin to construct a framework to model host-parasite invasion dynamics over time.

Schistosomes with wings: how host phylogeny and ecology shape the global distribution of Trichobilharzia querquedulae (Schistosomatidae).

Migratory waterfowl play an important role in the maintenance and spread of zoonotic diseases worldwide. An example is cercarial dermatitis, caused when larval stages of schistosomes that normally develop in birds penetrate human skin. Members of the genus Trichobilharzia (Schistosomatidae), transmitted mainly by ducks, are considered to be major etiological agents of cercarial dermatitis globally. To better understand the diversity and distribution of Trichobilharzia spp., we surveyed ducks from the United States, eastern Canada, Argentina, South Africa and New Zealand. To aid in species identification of the Trichobilharzia worms recovered, regions of the Cox1, ND4 and ITS1 were sequenced. Furthermore, we provide molecular phylogenetic evidence for the cosmopolitan distribution and trans-hemispheric gene flow for one species, Trichobilharzia querquedulae, previously thought to be restricted to North America. These new samples from endemic non-migratory duck species indicate that T. querquedulae transmission occurs within each of the regions we sampled and that it is specific to the blue-winged+silver teal duck clade. Prevalence within this host group is >95% across the known range of T. querquedulae, indicating that transmission is common. Genetic divergence is evenly distributed among continents, and no phylogenetic structure associated with geography was observed. The results provide strong support for the global distribution and transmission of T. querquedulae and represent, to our knowledge, the first report of a cosmopolitan schistosome confirmed by genetic data. These data are the first known to support trans-hemispheric genetic exchange in a species responsible for causing cercarial dermatitis, indicating that the epidemiology of this group of poorly known zoonotic parasites is more complex than previously expected.