Snail-Schistosoma, Paragonimus interactions in China: Population ecology, genetic diversity, coevolution and emerging diseases

This paper focuses on two snail-borne helminths in China infecting man, Sch istosoma and Paragonimus, but primarily on Schistosoma (Asian caenogastropo d-transmitted). Of concern are 1) the direction and timing of the evolution of the snail family Pomatiopsidae and the pattern of coevolution of Schist osoma and Paragonimus with defined clades within the Pomatiopsidae, 2) the question of monophyly of the Pomatiopsidae and its two subfamilies Pomatiop sinae and Triculinae, 3) the amount of genetic diversity within Oncomelania throughout China as revealed by allozymes and DNA sequences, 4) Oncomelani a ecology and genetics with regard to different modes of transmission of Sc histosoma japonicum, 5) the implications of the Three Gorges dam across the Yangtze River on emerging diseases. Allozyme and COI gene sequence data confirm the monophyly of the Pomatiopsi dae with its two subfamilies. The timing and direction of evolution of the Pomatiopsidae in Asia are congruent with area cladograms based on geologica l-paleontological events and evolving river systems (Yangtze, Mekong, Red) from about the end of the Miocene. The two subfamilies are highly divergent on the basis of morphology and ecology but less so on the basis of molecul ar genetics. The Pomatiopsidae are in a clade distinctly divergent from the Hydrobiidae, a family that has been used in China to classify the Pomatiop sinae and Triculinae. Figs. 2 and 3 show the relationships of the two paras ite genera with the morphology-based clades of those caenogastropod familie s transmitting Schistosoma and Paragonimus throughout the world (excluding Africa for which too little is known). Two caenogastropod superfamilies are involved (Ceritheacea and Rissoacea); Only Paragonimus has evolved with ta xa of the Thiaridae, Pleuroceridae, Hydrobiidae; both parasite genera have evolved with various pomatiopsid taxa of both subfamilies. While all data a vailable (reviewed in Davis, 1980, 1992) show that Schistosoma is tightly l inked genetically in a coevolved system with its snail host, such a close l inked genetic coevolved system operating at the population to genus level i n Paragonimus is in doubt. Erhaia (Pomatiopsinae) and Tricula (Triculinae) were found in sympatry in Fujian Province, both reported transmitting putat ive Paragonimus skrjabini. P. skrjabini has been reported from at least 22 species of pomatiopsine and triculine snails in China. The evidence suggest s that species of Paragonimus can switch hosts between different snail subf amilies and genera. The higher classification of Erhaia is in doubt. Should Erhaia be found not to be a pomatiopsid snail, then host switching can occ ur between some families (at least of the Rissoacea). Based on COI and allozyme data there are three geographically isolated subs pecies of Oncomelania on the mainland of China: O. h robertsoni in Yunnan a nd Sichuan, O. h. tangi in Fujian Province, O. h. hupensis throughout the Y angtze drainage below the Three Gorges of the Yangtze River as well as part s of Guangxi and Zhejiang Provinces. Within O. h. hupensis there is conside rable genetic diversity. Nei's minimum genetic distance among populations i s 0.204 +/- 0.085. We conclude, on the basis of allozyme data from Miao Riv er populations of O. h. hupensis in Hubei Province, that ribbed and smooth- shelled populations (shell with varix; shell growth with the same allometry ) are the same species. Ribbing is found in populations affected by annual floods, especially the annual flooding of the Yangtze River. Smooth-shelled populations are upstream, above the effects of flooding. Thus, smooth-shel led O. fausti and O. h. guangxiensis, nominal taxa used by some authors, ar e synonyms of O. h. hupensis. Using allozyme population genetics and COI gene sequence data we have found that there is considerable genetic instability in what one would initially presume to be a population. Duringflooding, snails are swept from flood pl ains and islands, float down the Yangtze, and are deposited in diverse loca tions or are swept into canals and become deposited along canals. These agg regates of snails derived from various places do not exhibit Hardy-Weinberg equilibrium for polymorphic loci. Haplotypes of the COI gene are shown to be most useful for demonstrating genetic instability. Data are presented fr om six "populations" from around Dong Ting Lake of Hunan Province. Sequence data were obtained from 10 individuals taken from each site. In a stable p opulation, one expects 0 to 0.5% nucleotide differences within a population (0-3 nucleotide differences), or one to two haplotypes per 10 individuals. One such population was found at low elevation beyond effects of flooding. The other sites were around the edge of the lake and are flooded annually. Snails from these lowland localities had 6 to 10 haplotypes per 10 individ uals (3.5 to 3.9% polymorphic sites), i.e. they were genetically unstable a ggregates. The diversity of haplotypes enables us to map gene flow and patt erns of intermixing of snails among localities. Four different modes of transmission of Schistosoma japonicum are discussed . Differences are based on genetically differentiated subspecies, whether o r not the populations are affected by annual flooding, life expectancy, pop ulation genetic stability, biogeography, and whether or not cattle play a d ominant role in transmission of the disease. The implications of the Three Gorges Dam across the Yangtze River is discussed both in terms of the poten tial for snail transport into the vast reservoir but also of the impact on Poyang Lake, the largest lake in China and a major endemic area for schisto somiasis. A remote sensing image is used in conjunction with GIS technology to discuss snail-schistosome interactions and epidemiology on Poyang Lake marshlands.