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Oncomelania Hupensis Robertsoni in an Historically Endemic Schistosomiasis Area

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Oncomelania Hupensis Robertsoni in an Historically Endemic Schistosomiasis Area UC Berkeley UC Berkeley Previously Published Works Title Stirred, not shaken: genetic structure of the intermediate snail host Oncomelania hupensis robertsoni in an historically endemic schistosomiasis area. Permalink https://escholarship.org/uc/item/91p744wc Journal Parasites & vectors, 4(1) ISSN 1756-3305 Authors Hauswald, Anne-Kathrin Remais, Justin V Xiao, Ning et al. Publication Date 2011-10-26 DOI 10.1186/1756-3305-4-206 License https://creativecommons.org/licenses/by-nc-sa/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Hauswald et al. Parasites & Vectors 2011, 4:206 http://www.parasitesandvectors.com/content/4/1/206 RESEARCH Open Access Stirred, not shaken: genetic structure of the intermediate snail host Oncomelania hupensis robertsoni in an historically endemic schistosomiasis area Anne-Kathrin Hauswald1, Justin V Remais2,3, Ning Xiao4, George M Davis5, Ding Lu4, Margaret J Bale2 and Thomas Wilke1* Abstract Background: Oncomelania hupensis robertsoni is the sole intermediate host for Schistosoma japonicum in western China. Given the close co-evolutionary relationships between snail host and parasite, there is interest in understanding the distribution of distinct snail phylogroups as well as regional population structures. Therefore, this study focuses on these aspects in a re-emergent schistosomiasis area known to harbour representatives of two phylogroups - the Deyang-Mianyang area in Sichuan Province, China. Based on a combination of mitochondrial and nuclear DNA, the following questions were addressed: 1) the phylogeography of the two O. h. robertsoni phylogroups, 2) regional and local population structure in space and time, and 3) patterns of local dispersal under different isolation-by-distance scenarios. Results: The phylogenetic analyses confirmed the existence of two distinct phylogroups within O. h. robertsoni.In the study area, phylogroups appear to be separated by a mountain range. Local specimens belonging to the respective phylogroups form monophyletic clades, indicating a high degree of lineage endemicity. Molecular clock estimations reveal that local lineages are at least 0.69-1.58 million years (My) old and phylogeographical analyses demonstrate that local, watershed and regional effects contribute to population structure. For example, Analyses of Molecular Variances (AMOVAs) show that medium-scale watersheds are well reflected in population structures and Mantel tests indicate isolation-by-distance effects along waterways. Conclusions: The analyses revealed a deep, complex and hierarchical structure in O. h. robertsoni, likely reflecting a long and diverse evolutionary history. The findings have implications for understanding disease transmission. From a co-evolutionary standpoint, the divergence of the two phylogroups raises species level questions in O. h. robertsoni and also argues for future studies relative to the distinctness of the respective parasites. The endemicity of snail lineages at the regional level supports the concept of endemic schistosomiasis areas and calls for future geospatial analyses for a better understanding of respective boundaries. Finally, local snail dispersal mainly occurs along waterways and can be best described by using cost distance, thus potentially enabling a more precise modelling of snail, and therefore, parasite dispersal. Keywords: China, Sichuan Province, Oncomelania hupensis robertsoni, schistosomiasis japonica, coevolution, AFLP, cytochrome c oxidase subunit I (COI), phylogeny, phylogeography, watersheds * Correspondence: [email protected] 1Department of Animal Ecology & Systematics, Justus Liebig University, Heinrich-Buff-Ring 26-32 IFZ, D-35392 Giessen, Germany Full list of author information is available at the end of the article © 2011 Hauswald et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Hauswald et al. Parasites & Vectors 2011, 4:206 Page 2 of 18 http://www.parasitesandvectors.com/content/4/1/206 Background and Yunnan Provinces above the Three Gorges. The parasite species of the trematode genus Schistosoma However, subspecies validityandassignmentremains cause human schistosomiasis, one of the most prevalent controversial [24,25], including the western subspecies parasitic diseases in the world, infecting more than 200 O. h. robertsoni. Genetically, it is highly distinct from all million people and leading toasubstantialburdenof other known subspecies of O. hupensis [16,22,26,27], disease [1]. Schistosoma japonicum, the causal agent of raising questions about whether it deserves full species the disease common in East and Southeast Asia, remains status. Moreover, based on mitochondrial (mt) DNA a public health threat for millions of people living in the sequence data, the existence of at least two major phy- tropical and subtropical zones of China [2]. Though logroups within O. h. robertsoni was demonstrated, with overall prevalence and intensity of infection have pairwise K2P-distances for two mtDNA genes of up to decreased greatly in recent decades [3], cases of re- 0.12 (= 12%) [26]. Because such a high divergence typi- emergence remain of concern [4,5]. The considerable cally reflects genus-level relationships within the snail medical importance of S. japonicum has spurred numer- superfamily Rissooidea [28], it was initially not clear ous parasitological, ecological and genetic studies. whether the patterns observed are due to the presumed Genetic variation between strains of S. japonicum from long evolutionary history of this subspecies [16] or are widely separated geographical areas, for example, have simply artefacts. Note that O. hupensis is a dioecious been reported based on allozyme, nucleotide sequence, species (i.e., an individual specimen is distinctly male or microsatellite and single nucleotide polymorphism ana- female). Thus selfing cannot explain the overall high lyses [6-15]. Indeed, the genetic distance between some diversity within this species either. S. japonicum populations is so immense as to indicate Only recently, an independent study based on DNA that they represent distinct taxa [10]. In particular, sequencing data of a nuclear (nc) gene confirmed the researchers consider that parasites from Sichuan Pro- existence of two phylogroups [27]. However, the regio- vince, which are transmitted by the nominal snail sub- nal distribution of these groups is not well understood. species Oncomelania hupensis robertsoni, possibly Moreover, possible co-evolutionary implications of these belong to a separate strain [10-12]. two genetically and sexually isolated snail host taxa for Given the demonstrated close co-evolutionary rela- the genetic structure of S. japonicum remain unknown. tionships between S. japonicum and its intermediate At the same time, little knowledge exists about smaller- snail host O. hupensis ssp. [16], there is an increased scale population structures in O. h. robertsoni,suchas interest in understanding snail phylogenetics and popu- those within schistosomiasis transmission areas. As a lation structure. The importance of the snail host for consequence, local effects of barriers (such as watershed comprehending disease transmission is further rein- boundaries or mountain ranges) and means of dispersal forced by three principal findings: (such as along water networks or bird-mediated) on 1) Oncomelania hupensis is the sole intermediate host snail and thus parasite distributions are poorly under- for Schistosoma japonicum:unlikeS. mansoni and S. stood. Given these knowledge gaps, there is a need for haematobium, host switching does not appear to occur. better understanding of the phylogroup distribution in 2) Given the close genetic interactions between snail O. h. robertsoni and regional population structures in and parasite in terms of co-evolutionary relationships, a time and space. snail population likely reflects population genetic para- This study focused on these aspects in a formerly ende- meters of the parasite and vice versa [17,18]. mic schistosomiasis area previously reported to harbour 3) Genetically diverse snail populations appear to be representatives of two distinct phylogroups [26] - the more susceptible to infection with S. japonicum than Deyang-Mianyang area in Sichuan Province (Figure 1). homogeneous populations [19]. Based on a combination of mtDNA and genome-wide Molecular and morphological analyses, together with ncDNA, we studied: breeding experiments and biogeographic studies of O. 1)ThephylogeographyofthetwoO. h. robertsoni hupensis indicate that there are three subspecies on the phylogroups, with an interest in understanding how mainland of China [16,20-22]. Oncomelania h. hupensis these groups are distributed on a micro-scale, e.g., primarily occurs in the Yangtze River drainage below whether they occur in sympatry. the Three Gorges; it has spread to Guangxi Province via 2) Regional and local population structures in space the Grand Canal from Hunan (note that some authors and time, focusing on the degree of population admixing consider the latter populations to belong to a distinct as well as the potential correlation of population struc- subspecies, O. h. guangxiensis [23,24]). Oncomelania h. ture with physical barriers. Our working hypothesis
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