Phylogeny of seven Bulinus species originating from endemic areas in three African countries, in relation to the human blood fluke Schistosoma haematobium

BMC Evolutionary Biology

Gilles Dreyfuss⁴  Tine Huyse²  Bruno Senghor¹  Mustafa Al-Jawhari³  Félicité Flore Djuikwo-Teukeng⁵  Rima Zein-Eddine⁴ 

[1] Institute of Research for Development, URMITE, UM63, CNRS 7278, IRD 198, International Campus of Han, IRD B.P, Dakar, 1386, Senegal;Biology Department, Royal Museum for Central Africa, Leuvensesteenweg, 13, Tervuren, B-3080, Belgium;Laboratory of Microbiology, CNRS UMR 7276, Faculties of Medicine and Pharmacy, 2 Docteur Raymond Marcland Street, Limoges, 87025, France;Institute of Neuroepidemiology and Tropical Parasitology INSERM UMR 1094, Faculties of Medicine and Pharmacy, 2 Docteur Raymond Marcland Street, Limoges, 87025, France;Faculty of Health Sciences, University of Montagnes, Banganté, Cameroon

关键词: Host-parasite interactions;    Genetic diversity;    Phylogeny;    Schistosoma haematobium;    Bulinus species;   

Others  :  1121726
DOI  :  10.1186/s12862-014-0271-3

 received in 2014-06-11, accepted in 2014-12-12,  发布年份 2014

【 摘 要 】

Background

Snails species belonging to the genus Bulinus (Planorbidae) serve as intermediate host for flukes belonging to the genus Schistosoma (Digenea, Platyhelminthes). Despite its importance in the transmission of these parasites, the evolutionary history of this genus is still obscure. In the present study, we used the partial mitochondrial cytochrome oxidase subunit I (cox1) gene, and the nuclear ribosomal ITS, 18S and 28S genes to investigate the haplotype diversity and phylogeny of seven Bulinus species originating from three endemic countries in Africa (Cameroon, Senegal and Egypt).

Results

The cox1 region showed much more variation than the ribosomal markers within Bulinus sequences. High levels of genetic diversity were detected at all loci in the seven studied species, with clear segregation between individuals and appearance of different haplotypes, even within same species from the same locality. Sequences clustered into two lineages; (A) groups Bulinus truncatus, B. tropicus, B. globosus and B. umbilicatus; while (B) groups B. forskalii, B. senegalensis and B. camerunensis. Interesting patterns emerge regarding schistosome susceptibility: Bulinus species with lower genetic diversity are predicted to have higher infection prevalence than those with greater diversity in host susceptibility.

Conclusion

The results reported in this study are very important since a detailed understanding of the population genetic structure of Bulinus is essential to understand the epidemiology of many schistosome parasites.

【 授权许可】

   
2014 Zein-Eddine et al.; licensee BioMed Central.

【 图 表 】

Figure 2.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Tchuem Tchuenté LA, Southgate VR, Jourdane J, Webster BL, Vercruysse J: Schistosoma intercalatum: an endangered species in Cameroon? Trends Parasitol 2003, 19:389-393.
• [2]Van der Werf MJ, Bosompem KM, Vlas SJ: Schistosomiasis control in Ghana: case management and means for diagnosis and treatment within the health system. Trans R Soc Trop Med Hyg 2003, 97:146-152.
• [3]Agatsuma T: Origin and evolution of Schistosoma japonicum. Parasitol Int 2003, 52:335-340.
• [4]Rollinson D, Kaukas A, Johnston D, Simpson A, Tanaka M: Some molecular insights into schistosome evolution. Int J Parasito 1997, 27:11-28.
• [5]Brown DS: Freshwater snails of Africa and their medical importance. In CRC Press. Volume 2. 2nd edition. Edited by Taylor and Françis ltd. London; 1994:208–247.
• [6]Njiokou F, Teukeng E, Bilong Bilong CF, Njiné T, Same Ekobo A: Experimental study of the compatibility between Schistosoma haematobium and two species of Bulinus in Cameroon. Bull Société Pathol Exot 2004, 97:43-46.
• [7]Sène M, Southgate VR, Vercruysse J: Bulinus truncatus, intermediate host of Schistosoma haematobium in the Senegal River Basin (SRB). Bull Société Pathol Exot 2003, 97:29-32.
• [8]Jørgensen A, Madsen H, Nalugwa A, Nyakaana S, Rollinson D, Stothard JR, Kristensen TK: A molecular phylogenetic analysis of Bulinus (Gastropoda: Planorbidae) with conserved nuclear genes. Zool Scr 2011, 40:126-136.
• [9]Kane RA, Stothard JR, Emery AM, Rollinson D: Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasit Vectors 2008, 1:15. BioMed Central Full Text
• [10]Jørgensen A, Kristensen TK, Madsen H: A molecular phylogeny of apple snails (Gastropoda, Caenogastropoda, Ampullariidae) with an emphasis on African species. Zool Scr 2008, 37:245-252.
• [11]Nalugwa A, Jørgensen A, Nyakaana S, Kristensen TK: Molecular phylogeny of Bulinus (Gastropoda: Planorbidae) reveals the presence of three species complexes in the Albertine Rift freshwater bodies. Int J Genet Mol Biol 2010, 2:130-139.
• [12]Jarne P: Resistance genes at the population level. Parasitol Today Pers Ed 1993, 9:216-217.
• [13]Jarne P, Charlesworth D: Hermes meets Aphrodite: an animal perspective. Trends Ecol Evol 1996, 24:35–39.
• [14]Brown DS, Shaw KM: Freshwater snails of the Bulinus truncatus/tropicus complex in Kenya: tetraploid species. J Mollus Stud 1989, 55:509-532.
• [15]Schmid-hempel S: Parasites and flower choice of bumblebees. Anim Behav 1998, 55:819-825.
• [16]Vera C, Mouchet F, Bremond P, Sidiki A, Sellin E, Sellin B: Natural infection of Bulinus senegalensis by Schistosoma haematobium in a temporary pool focus in Niger: characterization by cercarial emergence patterns. Trans R Soc Trop Med Hyg 1992, 86:62.
• [17]Minchella D, LoVerde PT: Laboratory comparison of the relative success of Biophalaria glabrata stoks wiich are susceptible and insusceptible to infection with Schistosoma mansoni. Parasitology 1993, 19:335–344.
• [18]King KC, Lively CM: Does genetic diversity limit disease spread in natural host populations? Heredity 2012, 109:199-203.
• [19]Coltman DW, Smith JA, Bancroft DR, Pilkington J, MacColl AD, Clutton-Brock TH, Pemberton JM: Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. Am Nat 1999, 154:730-746.
• [20]Gow JL, Noble LR, Rollinson D, Mimpfoundi R, Jones CS: Breeding system and demography shape population genetic structure across ecological and climatic zones in the African freshwater snail, Bulinus forskalii (Gastropoda, Pulmonata), intermediate host for schistosomes. Mol Ecol 2004, 13:3561-3573.
• [21]Dazo BC, Hairston NG, Dawood IK: The ecology of Bulinus truncatus and Biomphalaria alexandrina and its implications for the control of bilharziasis in the Egypt-49 project area. Bull World Health Organ 1996, 35:339-356.
• [22]Abdel-Nasser A: Prevalence of urinary schistosomiasis and Infections with Trematode larval stages in Bulinus truncatus Snails from Qena Upper Egypt. J Appl Sci Res 2008, 4:1610-1617.
• [23]El-Khoby T, Galal N, Fenwick A, Baraka R, El-Hawey A, Nooman Z, Habib M, Abdel-Wahab F, Gabr NS, Hammam HM, Hussein MH, Mikhail NN, Cline BL, Strickland GT: The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. Am J Trop Med Hyg 2000, 62:88-99.
• [24]Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, Rollinson D: Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 2009, 5:1000571.
• [25]Kloos H, Thompson K: Schistosomiasis in Africa: an ecological perspective. J Trop Geogr 1979, 48:31-46.
• [26]David R: The paleoepidemiology of schistosomiasis in Ancient Egypt.Soc Hum Eco Soc Humen Ecology 2000, 9:14.
• [27]Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994, 3:294-299.
• [28]Bowles J, Blair D, McManus DP: Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 1992, 54:165-173.
• [29]Kane RA, Rollinson D: Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Mol Biochem Parasitol 1994, 63:153-156.
• [30]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [31]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc Acids Res 1997, 25:4876-4882.
• [32]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinforma Oxf Engl 2009, 25:1451-1452.
• [33]Tamura K, Nei M, Kumar S: Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 2004, 101:11030-11035.
• [34]Morgan JAT, DeJong RJ, Jung Y, Khallaayoune K, Kock S, Mkoji GM, Loker ES: A phylogeny of planorbid snails, with implications for the evolution of Schistosoma parasites. Mol Phylogenet Evol 2002, 25:477-488.