Phylogeography Of Biomphalaria Glabrata And B. Pfeifferi, Important Intermediate Hosts Of Schistosoma Mansoni In The New And Old World Tropics

The historical phylogeography of the two most important intermediate host species of the human blood fluke Schistosoma mansoni, B. glabrata in the New World, and B. pfeifferi in the Old World, was investigated using partial 16S and ND1 sequences from the mitochondrial genome. Nuclear sequences of an actin intron and internal transcribed spacer (ITS)-1 were also obtained, but they were uninformative for the relationships among populations. Phylogenetic analyses based on mtDNA revealed six well-differentiated clades within B. glabrata: the Greater Antilles, Venezuela and the Lesser Antilles, and four geographically overlapping Brazilian clades. Application of a Biomphalaria-specific mutation rate gives an estimate of the early Pleistocene for their divergence. The Brazilian clades were inferred to be the result of fragmentation, due possibly to climate oscillations, with subsequent range expansion producing the overlapping ranges. Within the Venezuela and Lesser Antilles clade, lineages from each of these areas were estimated to have separated approximately 740 000 years ago. Compared to B. glabrata, mitochondrial sequences of B. pfeifferi are about 4x lower in diversity, reflecting a much younger age for the species, with the most recent common ancestor of all haplotypes estimated to have existed 880 000 years ago. The oldest B. pfeifferi haplotypes occurred in southern Africa, suggesting it may have been a refugium during dry periods. A recent range expansion was inferred for eastern Africa less than 100 000 years ago. Several putative species and subspecies, B. arabica, B. gaudi, B. rhodesiensis and B. stanleyi, are shown to be undifferentiated from other B. pfeifferi populations.121130413056Akaike, H., A new look at the statistical model identification (1974) Transactions on Automatic Control, 19, pp. 716-723. , Institute of Electrical and Electronics EngineersAngers, B., Charbonnel, N., Galtier, N., Jarne, P., The influence of demography, population structure and selection on molecular diversity in the selfing freshwater snail Biomphalaria pfeifferi (2003) Genetical Research, 81, pp. 193-204Arctander, P., Johansen, C., Coutellec-Vreto, M.-A., Phylogeography of three closely related African bovids (Tribe Alcelaphini) (1999) Molecular Ecology, 16, pp. 1724-1739Bandoni, S.M., Mulvey, M., Koech, D., Loker, E.S., Genetic structure of Kenyan populations of Biomphalaria pfeifferi (Gastropoda: Planorbidae) (1990) Journal of Molluscan Studies, 56, pp. 383-391Bandoni, S.M., Mulvey, M., Loker, E.S., Phylogenetic analysis of eleven species of Biomphalaria Preston, 1910 (Gastropoda: Planorbidae) based on comparisons of allozymes (1995) Biological Journal of the Linnaean Society, 54, pp. 1-27Bandoni, S.M., Mulvey, M., Loker, E.S., Intraspecific and interspecific patterns of allozyme variation among species of Biomphalaria Preston 1910 (Gastropoda: Planorbidae) (1995) Biochemical Systematics and Ecology, 23, pp. 593-616Brown, D.S., (1994) Freshwater Snails of Africa and Their Medical Importance, 2nd Edn., , Taylor & Francis Ltd, LondonBrown, D.D., Wensink, P.C., Jordan, E., A comparison of the ribosomal DNAs of Xenopus leavis and Xenopus mulleri: The evolution of tandem genes (1972) Journal of Molecular Biology, 63, pp. 57-73Campbell, G., Jones, C.S., Lockyer, A.E., Molecular evidence supports an African affinity of the Neotropical freshwater gastropod, Biomphalaria glabrata, Say 1818, an intermediate host for Schistosoma mansoni (2000) Proceedings of the Royal Society of London Series B, 267, pp. 2351-2358Carvalho, Od.S., Nunes, I.M., Caldeira, R.L., First report of Biomphalaria glabrata in the state of Rio Grande do Sul, Brazil (1998) Memórias do Instituto Oswaldo Cruz, 93, pp. 39-40Charbonnel, N., Angers, B., Rasatavonjizay, R., The influence of mating system, demography, parasites and colonization on the population dynamics of Biomphalaria pfeifferi. Madagascar (2002) Molecular Ecology, 11, pp. 2213-2228Charbonnel, N., Angers, B., Rasatavonjizay, R., Brémond, P., Jarne, P., Evolutionary aspects of the metapopulation dynamics of Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni (2002) Journal of Evolutionary Biology, 15, pp. 248-261Charbonnel, N., Quesnoit, M., Razatavonjizay, R., Brémond, P., Jarne, P., A spatial and temporal approach to microevolutionary forces affecting population biology in the freshwater snail Biomphalaria pfeifferi (2002) American Naturalist, 160, pp. 741-755Chevillon, C., Raymond, M., Guillemaud, T., Lenormand, T., Pasteur, N., Population genetics of insecticide resistance in the mosquito Culex pipiens (1999) Biological Journal of the Linnaean Society, 68, pp. 147-157Clement, M., Posada, D., Crandall, K.A., TCS: A computer program to estimate gene genealogies (2000) Molecular Ecology, 9, pp. 1657-1660Cox, A.J., Hebert, P.D.N., Colonization, extinction, and phylogeographic patterning in a freshwater crustacean (2001) Molecular Ecology, 10, pp. 371-386Crompton, D.W.T., How much human helminthiasis is there in the world? (1999) Journal of Parasitology, 85, pp. 397-403De Meester, L., Gómez, A., Okamura, B., Schwenk, K., The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms (2002) Acta Oecologica, 23, pp. 121-135DeJong, R.J., Morgan, J.A.T., Paraense, W.L., Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni (2001) Molecular Biology and Evolution, 18, pp. 2225-2239Després, L., Imbert-Establet, D., Monnerot, M., Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America (1995) Molecular and Biochemical Parasitology, 60, pp. 221-230Donnelly, M.J., Licht, M.C., Lehmann, T., Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae (2001) Molecular Biology and Evolution, 18, pp. 1353-1364Doumenge, J., Mott, K.E., Cheung, C., (1987) Centre d'Etude de Géographie Tropicale/WHO Atlas of Global Distribution of Schistosomiasis, , Presses Universitaires de Bordeaux, BordeauxEdwards, S.V., Beerli, P.B., Perspective: Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies (2000) Evolution, 54, pp. 1839-1854Failloux, A.B., Vazeille, M., Rodhain, F., Geographic genetic variation in populations of the dengue virus vector Aedes aegypti (2002) Journal of Molecular Evolution, 55, pp. 653-663Felsenstein, J., Phylogenies from molecular sequences: Inference and reliability (1988) Annual Review of Genetics, 22, pp. 521-565Fletcher, M., LoVerde, P.T., Woodruff, D.S., Genetic variation in Schistosoma mansoni enzyme polymorphisms in populations from Africa, Southwest Asia, South America and the West Indies (1981) American Journal of Tropical Medicine and Hygiene, 30, pp. 406-421Gandolfi, A., Bonilauri, P., Rossi, V., Menozzi, P., Intraindividual and intraspecies variability of ITS1 sequences in the ancient asexual Darwinula stevensoni (Crustacea: Ostracoda) (2001) Heredity, 87, pp. 449-455Harris, D.J., Crandall, K.A., Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): Implications for phylogenetic and microsatellite studies (2000) Molecular Biology and Evolution, 17, pp. 284-291Hubendick, B., Viewpoints on species discrimination with special attention to medically important snails (1954) Proceedings of the Malacological Society of London, 31, pp. 6-11Jarne, P., Théron, A., Genetic structure in natural populations of flukes and snails: A practical approach and review (2001) Parasitology, 123, pp. S27-S40Knight, M., Brindley, P.J., Richards, C.S., Lewis, F.A., Schistosoma mansoni: Use of a cloned ribosomal RNa gene probe to detect restriction fragment length polymorphism in the intermediate host Biomphalaria glabrata (1991) Experimental Parasitology, 78, pp. 285-294Kuhner, M.K., Yamato, J., Felsenstein, J., Maximum likelihood estimation of population growth rates based on the coalescent (1998) Genetics, 149, pp. 429-434Lancaster, I.N., Evidence for a widespread late Pleistocene humid period in the Kalahari (1979) Nature, 279, pp. 145-146Lehmann, T., Hawley, W.A., Grebert, H., The rift valley complex as a barrier to gene flow for Anopheles gambiae. Kenya (1999) Journal of Heredity, 90, pp. 613-621Lima, L.C., Biomphalaria aff. glabrata do Pleistocene de Janaúba, Minas Gerais (1984) Memórias do Instituto Oswaldo Cruz, 79, pp. 55-58Lima, L.C., Ocorrência de Planorbídeos Pleistocênicos no município de Jacobina, Bahia (1987) Memôrias Do Instituto Oswaldo Cruz, 82, pp. 71-72Lima, L.C., Alexandre, M.A., Biomphalaria aff. tenagophila do sítio arqueológico do corondó, São Pedro da Aldeia, RJ (1985) Memórias Do Instituto Oswaldo Cruz, 79, pp. 491-495Lima, L.C., De Oliveira, M.P., Pleistocene gastropods from Toca da Esperança, municipality of Central, state of Bahia, Brazil (1992) Memórias do Instituto Oswaldo Cruz, 87, pp. 423-427Lockhart, P.J., Steel, M.H., Hendy, M.D., Penny, D., Recovering evolutionary trees under a more realistic model of sequence evolution (1994) Molecular Biology and Evolution, 11, pp. 605-612Malek, E.A., (1985) Snail Hosts of Schistosomiasis and Other Snail-Transmitted Diseases in Tropical America: A Manual, , Scientific Publication no. 478. Pan American Health Organization, WashingtonMalek, E.A., File, S.K., Electrophoretic studies on the digestive gland esterases of some biomphalarid and lymnaeid snails (1971) Bulletin of the World Health Organization, 45, pp. 819-825Mavárez, J., Amarista, M., Pointier, J.P., Jarne, P., Fine-scale population structure and dispersal in Biomphalaria glabrata, the intermediate snail host of Schistosoma mansoni, in Venezuela (2002) Molecular Ecology, 11, pp. 879-889Mavárez, J., Pointier, J.-P., David, P., Delay, B., Jarne, P., Genetic differentiation, dispersal, and mating system in the schistosome-transmitting freshwater snail Biomphalaria glabrata (2002) Heredity, 89, pp. 258-265Mavârez, J., Steiner, C., Pointier, J.P., Jarne, P., Evolutionary history and phylogeography of the schistosome-vector freshwater snail Biomphalaria glabrata based on nuclear and mitochondrial DNA sequences (2002) Heredity, 89, pp. 266-272McDonald, J.H., Kreitman, M., Adaptive protein evolution at the ADH locus in Drosophila (1991) Nature, 351, pp. 652-654Meunier, C., Tirard, C., Hurtrez-Boussès, S., Lack of molluscan diversity and the transmission of an emerging parasitic disease in Bolivia (2001) Molecular Ecology, 10, pp. 1333-1340Mimpfoundi, R., Greer, G.J., Allozyme variation among populations of Biomphalaria pfeifferi (Krauss, 1848) (Gastropoda, Planorbidae) in Cameroon (1990) Journal of Molluscan Studies, 56, pp. 461-467Monteiro, F.A., Barrett, T.V., Fitzpatrick, S., Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus (2003) Molecular Ecology, 12, pp. 997-1006Mulvey, M., Bandoni, S.M., Genetic variability in the M-line stock of Biomphalaria glabrata (Mollusca, Planorbidae) (1994) Journal of the Helminthological Society of Washington, 61, pp. 103-108Mulvey, M., Newman, M.C., Woodruff, D.S., Genetic differentiation among West Indian populations of the schistosome transmitting snail Biomphalaria glabrata (1988) Malacologia, 29, pp. 309-317Mulvey, M., Vrijenhoek, R.C., Genetic variation among laboratory strains of the planorbid snail Biomphalaria glabrata (1981) Biochemical Genetics, 19, pp. 1169-1182Mulvey, M., Vrijenhoek, R.C., Population structure in Biomphalaria glabrata. Examination of an hypothesis for the patchy distribution of susceptibility to schistosomes (1982) American Journal of Tropical Medicine and Hygiene, 31, pp. 1195-1200Nei, M., Li, W.-H., Mathematical model for studying genetic variation in terms of restriction endonucleases (1979) Proceedings of the National Academy of Sciences USA, 76, pp. 5269-5273Nersting, L.G., Arctander, P., Phylogeography and conservation of impala and greater kudu (2001) Molecular Ecology, 10, pp. 711-719Newton, W.L., The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus (1953) Experimental Parasitology, 21, pp. 72-74Newton, W.L., The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility with Schistosoma mansoni (1955) Journal of Parasitology, 41, pp. 526-528Nicholas, K.B., Nicholas Jr., H.B., (1997) GENEDOC: A Tool for Editing and Annotating Multiple Sequence Alignments, , Distributed by the authorNyakanna, S., Arctander, P., Siegismund, H.R., Population structure of the African savannah elephant inferred from mitochondrial control region sequences and nuclear microsatellite loci (2002) Heredity, 89, pp. 90-98Palumbi, S.R., Nucleic acids II: The polymerase chain reaction (1996) Molecular Systematics, pp. 205-248. , eds Hillis DM, Moritz C, Mable BK. Sinauer, Sunderland, MAParaense, W.L., Self and cross-fertilization in Australorbis glabratus (1955) Memórias Do Instituto Oswaldo Cruz, 53, pp. 285-291Paraense, W.L., A genetic approach to the systematics of planorbid molluscs (1956) Evolution, 10, pp. 403-407Paraense, W.L., One-sided reproductive isolation between geographically remote populations of a planorbid snail (1959) American Naturalist, 93, pp. 93-101Paraense, W.L., Corrêa, L.R., Variation in susceptibility of populations of Australorbis glabratus to a strain of Schistosoma mansoni (1963) Review of the Institute of Tropical Medicine São Paulo, 5, pp. 15-22Parodiz, J.J., The Tertiary non-marine Mollusca of South America (1969) Annals of the Carnegie Museum, 40, pp. 1-242Partridge, T., Warming phases in Southern Africa during the last 150,000 yearsan overview (1993) Palaeogeography, Palaeoclimatology, Palaeoecology, 101, pp. 237-244Pereira De Souza, C.P., Lima, L.C., (1997) Moluscos de Interesse Parasitológico de Brasil, , Serie de Equistossomase n. 1. FIOCRUZ/CPqRR. Belo Horizonte, BrazilPointier, J.-P., Invading freshwater gastropods: Some conflicting aspects for public health (1999) Malacologia, 41, pp. 403-411Posada, D., Crandall, K.A., MODELTEST: Testing the model of DNA substitution (1998) Bioinformatics, 14, pp. 817-818Posada, D., Crandall, K.A., Intraspecific gene genealogies: Trees grafting into networks (2001) Trends in Ecology and Evolution, 16, pp. 37-45Qiu, W.G., Dykhuizen, D.E., Acosta, M.S., Luft, B.J., Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States (2002) Genetics, 160, pp. 833-849Reader, J., (1998) Africa: A Biography of the Continent, , Alfred A Knopf, Inc., New YorkRibera, I., Bilton, D.T., Vogler, A.P., Mitochondrial DNA phylogeography and population history of Meladema diving beetles on the Atlantic Islands and in the Mediterranean basin (Coleoptera, Dytiscidae) (2003) Molecular Ecology, 12, pp. 153-167Richards, C.S., Merritt Jr., J.W., Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection (1972) American Journal of Tropical Medicine and Hygiene, 21, pp. 425-434Rogers, A.R., Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences (1992) Molecular Biology and Evolution, 9, pp. 552-569Rozas, J., Rozas, R., DNASP, version 3: An integrated program for molecular population genetics and molecular evolution analysis (1999) Bioinformatics, 15, pp. 174-175Schneider, S., Excoffier, L., Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: Application to human mitochondrial DNA (1999) Genetics, 152, pp. 1079-1089Schneider, S., Roessli, D., Excoffier, L., (2000) ARLEQUIN, Version 2.000: A Software for Population Genetics Data Analysis, , Genetics and Biometry Laboratory, University of Geneva, GenevaStädler, T., Jarne, P., Population biology, genetic structure, and mating system parameters in freshwater snails (1997) Evolutionary Ecology of Freshwater Animals, pp. 231-262. , eds Streit B, Städler T, Lively CM. Birkhäuser-Verlag, BaselSwofford, D.L., (2001) PAUP* Phylogenetic Analysis Using Parsimony (*and other Methods), Version 4 0b10, , Sinauer, Sunderland, MATajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism (1989) Genetics, 123, pp. 585-595Tchuem Tchuenté, L.A., Southgate, V.R., Théron, A., Compatibility of Schistosoma mansoni and Biomphalaria pfeifferi, Northern Senegal (1999) Parasitology, 118, pp. 595-603Templeton, A.R., Crandall, K.A., Sing, C.F., A cladistic analysis of phenotypic associations inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation (1992) Genetics, 132, pp. 619-633Truett, G.E., Heeger, P., Mynatt, R.L., Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT) (2000) Biotechniques, 29, pp. 52-54Van Andel, T.H., Tzedakis, P.C., Paleolithic landscapes of Europe and environs: 150 000-25 000 Years ago: An overview (1996) Quaternary Science Reviews, 15, pp. 481-500Van Herwerden, L., Blair, D., Agatsuma, T., Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: Implications for phylogenetic studies (1999) Molecular Phylogenetics and Evolution, 12, pp. 67-73Verheyan, E., Rüber, L., Snoeks, J., Meyer, A., Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations in Lake Tanganyika, Africa (1996) Philosophical Transactions of the Royal Society of London, Series B, 351, pp. 797-805Vianey-Liaud, M., La reproduction chez un mollusque hermaphrodite simultané, la planorbe Biomphalaria glabrata (Say, 1818) (Gastéropode, Pulmoné) (1997) Haliotis, 27, pp. 67-114Viard, F., Justy, F., Jarne, P., Population dynamics inferred from temporal variation at microsatellite loci in the selfing snail Bulinus truncatus (1997) Genetics, 146, pp. 973-982Vidigal, T.H.D.A., Kissinger, J.C., Caldeira, R.L., Phylogenetic relationships among Brazilian Biomphalaria species (Mollusca: Planorbidae) based upon analysis of ribosomal ITS2 sequences (2000) Parasitology, 121, pp. 611-620Vidigal, T.H.D.A., Neto, E.D., Carvahlo, O.D., Simpson, A.J.G., Biomphalaria glabrata - Extensive variation in Brazilian isolates revealed by random amplified polymorphic DNA analysis (1994) Experimental Parasitology, 79, pp. 187-194Wares, J.P., Biogeography of Asterias: North Atlantic climate change and speciation (2001) Biological Bulletin, 201, pp. 95-103Wares, J.P., Cunningham, C.W., Phylogeography and historical ecology of the North Atlantic intertidal (2001) Evolution, 55, pp. 2455-2469Wesselingh, F.P., Cadée, G.C., Renema, W., Flying high: On the airborne dispersal of aquatic organisms as illustrated by the distribution histories of the gastropod genera Tryonia and Planorbarius (1999) Geologie en Mijnbouw, 78, pp. 165-174Winograd, I.J., Landwehr, J.M., Ludwig, K.R., Coplan, T.B., Riggs, A.C., Duration and structure of the past four interglaciations (1997) Quaternary Review, 48, pp. 141-154Woodruff, D.S., Mulvey, M., Neotropical schistosomiasis: African affinities of the host snail Biomphalaria glabrata (Gastropoda: Planorbidae) (1997) Biological Journal of the Linnean Society, 60, pp. 505-516Young, A.M., Torres, C., Mack, J.E., Cunningham, C.W., Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus (2002) Marine Biology, 140, pp. 1059-106