Stirred, not shaken: genetic structure of the intermediate snail host Oncomelania hupensis robertsoniin an historically endemic schistosomiasis area

Hauswald Anne-Kathrin, Remais, Xiao Ning, Davis, Lu Ding, Bale, Wilke, Wilke Thomas

Description

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.

Sujets

• China
• Coévolution
• AFLP
• Phylogenetics
• Phylogeography
• Watershed

Informations

• Publié par: biomed
• Publié le: 01 janvier 2011
• Nombre de lectures: 83
• Langue: English
• Poids de l'ouvrage: 9 Mo

Extrait

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
1 2,3 4 5 4 2Anne-Kathrin Hauswald , Justin V Remais , Ning Xiao , George M Davis , Ding Lu , Margaret J Bale and
1*Thomas Wilke
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: [e-mail]
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
and Yunnan Provinces above the Three Gorges.Background
However, subspecies validityandassignmentremainsThe parasite species of the trematode genus Schistosoma
controversial [24,25], including the western subspeciescause human schistosomiasis, one of the most prevalent
O. h. robertsoni. Genetically, it is highly distinct from allparasitic diseases in the world, infecting more than 200
other known subspecies of O. hupensis [16,22,26,27],million people and leading toasubstantialburdenof
raising questions about whether it deserves full speciesdisease [1]. Schistosoma japonicum, the causal agent of
status. Moreover, based on mitochondrial (mt) DNAthe disease common in East and Southeast Asia, remains
sequence data, the existence of at least two major phy-a public health threat for millions of people living in the
logroups within O. h. robertsoni was demonstrated, withtropical and subtropical zones of China [2]. Though
pairwise K2P-distances for two mtDNA genes of up tooverall prevalence and intensity of infection have
0.12 (= 12%) [26]. Because such a high divergence typi-decreased greatly in recent decades [3], cases of re-
cally reflects genus-level relationships within the snailemergence remain of concern [4,5]. The considerable
superfamily Rissooidea [28], it was initially not clearmedical importance of S. japonicum has spurred numer-
whether the patterns observed are due to the presumedous parasitological, ecological and genetic studies.
long evolutionary history of this subspecies [16] or areGenetic variation between strains of S. japonicum from
simply artefacts. Note that O. hupensis is a dioeciouswidely separated geographical areas, for example, have
species (i.e., an individual specimen is distinctly male orbeen reported based on allozyme, nucleotide sequence,
female). Thus selfing cannot explain the overall highmicrosatellite and single nucleotide polymorphism ana-
diversity within this species either.lyses [6-15]. Indeed, the genetic distance between some
Only recently, an independent study based on DNAS. japonicum populations is so immense as to indicate
sequencing data of a nuclear (nc) gene confirmed thethat they represent distinct taxa [10]. In particular,
existence of two phylogroups [27]. However, the regio-researchers consider that parasites from Sichuan Pro-
nal distribution of these groups is not well understood.vince, which are transmitted by the nominal snail sub-
Moreover, possible co-evolutionary implications of thesespecies Oncomelania hupensis robertsoni, possibly
two genetically and sexually isolated snail host taxa forbelong to a separate strain [10-12].
the genetic structure of S. japonicum remain unknown.Given the demonstrated close co-evolutionary rela-
At the same time, little knowledge exists about smaller-tionships between S. japonicum and its intermediate
scale population structures in O. h. robertsoni,suchassnail host O. hupensis ssp. [16], there is an increased
those within schistosomiasis transmission areas. As ainterest in understanding snail phylogenetics and popu-
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
(such as along water networks or bird-mediated) onforced by three principal findings:
snail and thus parasite distributions are poorly under-1) Oncomelania hupensis is the sole intermediate host
stood. Given these knowledge gaps, there is a need forfor Schistosoma japonicum:unlike S. mansoni and S.
better understanding of the phylogroup distribution inhaematobium, host switching does not appear to occur.
O. h. robertsoni and regional population structures in2) Given the close genetic interactions between snail
time and space.and parasite in terms of co-evolutionary relationships, a
This study focused on these aspects in a formerly ende-snail population likely reflects population genetic para-
mic schistosomiasis area previously reported to harbourmeters of the parasite and vice versa [17,18].
representatives of two distinct phylogroups [26] - the3) Genetically diverse snail populations appear to be
Deyang-Mianyang area in Sichuan Province (Figure 1).more susceptible to infection with S. japonicum than
Based on a combination of mtDNA and genome-widehomogeneous populations [19].
ncDNA, we studied:Molecular and morphological analyses, together with
1)Thephylogeographyofthetwo O. h. robertsonibreeding experiments and biogeographic studies of O.
phylogroups, with an interest in understanding howhupensis indicate that there are three subspecies on the
these groups are distributed on a micro-scale, e.g.,mainland of China [16,20-22]. Oncomelania h. hupensis
whether they occur in sympatry.primarily occurs in the Yangtze River drainage below
2) Regional and local population structures in spacethe Three Gorges; it has spread to Guangxi Province via
and time, focusing on the degree of population admixingthe Grand Canal from Hunan (note that some authors
as well as the potential correlation of population struc-consider the latter populations to belong to a distinct
ture with physical barriers. Our working hypothesis issubspecies, O. h. guangxiensis [23,24]). Oncomelania h.
tangi is restricted to Fujian Province along the coast, that strong habitat fragmentation in the study area,
and O. h. robertsoni has a patchy distribution in Sichuan together with the long evolutionary history of theHauswald et al. Parasites & Vectors 2011, 4:206 Page 3 of 18
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structure of the intermediate snail host affects suscept-
ibility to schistosome infections, the means of snail, and
thus parasite, dispersal, and phylogenetic tracking in
S