Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing.

Gastropoda co-infections community ecology diagnostics high-throughput amplicon sequencing schistosomiasis

Journal

Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604

Informations de publication

Date de publication:
Feb 2022
Historique:
revised: 19 07 2021
received: 25 09 2020
accepted: 18 08 2021
pubmed: 27 8 2021
medline: 6 1 2022
entrez: 26 8 2021
Statut: ppublish

Résumé

Several methodological issues currently hamper the study of entire trematode communities within populations of their intermediate snail hosts. Here we develop a new workflow using high-throughput amplicon sequencing to simultaneously genotype snail hosts and their infecting trematode parasites. We designed primers to amplify four snail and five trematode markers in a single multiplex PCR. While also applicable to other genera, we focused on medically and economically important snail genera within the superorder Hygrophila and targeted a broad taxonomic range of parasites within the class Trematoda. We tested the workflow using 417 Biomphalaria glabrata specimens experimentally infected with Schistosoma rodhaini, two strains of Schistosoma mansoni and combinations thereof. We evaluated the reliability of infection diagnostics, the robustness of the workflow, its specificity related to host and parasite identification, and the sensitivity to detect co-infections, immature infections and changes of parasite biomass during the infection process. Finally, we investigated its applicability in wild-caught snails of other genera naturally infected with a diverse range of trematodes. After stringent quality control the workflow allows the identification of snails to species level, and of trematodes to taxonomic levels ranging from family to strain. It is sensitive to detect immature infections and changes in parasite biomass described in previous experimental studies. Co-infections were successfully identified, opening the possibility to examine parasite-parasite interactions such as interspecific competition. Together, these results demonstrate that our workflow provides a powerful tool to analyse the processes shaping trematode communities within natural snail populations.

Identifiants

pubmed: 34435445
doi: 10.1111/1755-0998.13492
doi:

Banques de données

GENBANK
['MZ546824', 'MZ546834', 'MZ540237', 'MZ540247', 'MZ600069', 'MZ600118', 'MZ546798', 'MZ546803', 'MZ567152', 'MZ567158', 'MZ558220', 'MZ558244', 'MZ600119', 'MZ600142', 'MZ546812', 'MZ546823', 'MZ546804', 'MZ546811']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

567-586

Subventions

Organisme : Laboratoire d'Excellence (LabEx) TULIP
ID : ANR-10-LABX-41
Organisme : ANR HySWARM
ID : ANR-18-CE35-0001
Organisme : Fonds Européens de Développement Régional
Organisme : BRAIN-be
ID : Pioneer Project BR/165/PI/TRAIL
Organisme : Fonds Wetenschappelijk Onderzoek
ID : Ph.D. Fellowship 11C5219N
Organisme : Agence Nationale de la Recherche
ID : ANR-17-CE02-0015

Informations de copyright

© 2021 John Wiley & Sons Ltd.

Références

Alvarez, I., & Wendel, J. F. (2003). Ribosomal ITS sequences and plant phylogenetic inference. Moleculary Phylogenetics and Evolution, 29, 417-434. https://doi.org/10.1016/s1055-7903(03)00208-2
Alzaylaee, H., Collins, R. A., Shechonge, A., Ngatunga, B. P., Morgan, E. R., & Genner, M. J. (2020). Environmental DNA-based xenomonitoring for determining Schistosoma presence in tropical freshwaters. Parasites & Vectors, 13(1), 63. https://doi.org/10.1186/s13071-020-3941-6
Bakuza, J. S., Denwood, M. J., Nkwengulila, G., & Mable, B. K. (2017). Estimating the prevalence and intensity of Schistosoma mansoni infection among rural communities in Western Tanzania: The influence of sampling strategy and statistical approach. PLOS Neglected Tropical Diseases, 11(9), e0005937. https://doi.org/10.1371/journal.pntd.0005937
Ballenghien, M., Faivre, N., & Galtier, N. (2017). Patterns of cross-contamination in a multispecies population genomic project: Detection, quantification, impact, and solutions. BMC Biology, 15, 25. https://doi.org/10.1186/s12915-017-0366-6
Basch, P., & DiConza, J. (1974). The miracidium-sporocyst transition in Schistosoma mansoni: Surface changes in vitro with ultrastructural correlation. The Journal of Parasitology, 60(6), 935-941. https://doi.org/10.2307/3278518
Blasco-Costa, I., Cutmore, S. C., Miller, T. L., & Nolan, M. J. (2016). Molecular approaches to trematode systematics: 'Best practice' and implications for future study. Systematic Parasitology, 93(3), 295-306. https://doi.org/10.1007/s11230-016-9631-2
Born-Torrijos, A., Poulin, R., Raga, J. A., & Holzer, A. S. (2014). Estimating trematode prevalence in snail hosts using a single-step duplex PCR: How badly does cercarial shedding underestimate infection rates? Parasites and Vectors, 7(1), 243. https://doi.org/10.1186/1756-3305-7-243
Braukmann, T. W. A., Ivanova, N. V., Prosser, S. W. J., Elbrecht, V., Steinke, D., Ratnasingham, S., de Waard, J., Sones, J., Zakharov, E., & Hebert, P. (2019). Metabarcoding a diverse arthropod mock community. Molecular Ecology Resources, 19, 711-727. https://doi.org/10.1111/1755-0998.13008
Brown, D. S. (1994) Freshwater snails of Africa and their medical importance. 2nd edn, Transactions of the Royal Society of Tropical Medicine and Hygiene. UK Taylor & Francis Ltd. https://doi.org/10.1016/0035-9203(81)90097-3
Buddenborg, S. K., Kamel, B., Hanelt, B., Bu, L., Zhang, S. M., Mkoji, G., & Loker, E. (2019). The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from Biomphalaria glabrata. PLOS Neglected Tropical Diseases, 13(9), e0007013. https://doi.org/10.1371/journal.pntd.0007013
Bybee, S. M., Bracken-Grissom, H., Haynes, B. D., Hermansen, R. A., Byers, R. L., Clement, M. J., & Crandall, K. A. (2011). Targeted amplicon sequencing (TAS): A scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biology and Evolution, 3, 1312-1323. https://doi.org/10.1093/gbe/evr106
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. https://doi.org/10.1038/nmeth.3869
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics, 10, 421. https://doi.org/10.1186/1471-2105-10-421
Carolus, H., Muzarabani, K. C., Hammoud, C., Schols, R., Volckaert, F., Barson, M., & Huyse, T. (2019). A cascade of biological invasions and parasite spillback in man-made Lake Kariba. The Science of the Total Environment, 659, 1283-1292. https://doi.org/10.1016/j.scitotenv.2018.12.307
Caron, Y., Righi, S., Lempereur, L., Saegerman, C., & Losson, B. (2011). An optimized DNA extraction and multiplex PCR for the detection of Fasciola sp. in lymnaeid snails. Veterinary Parasitology, 178(1), 93-99. https://doi.org/10.1016/j.vetpar.2010.12.020
Chaudhry, U. N., Ali, Q., Rashid, I., Shabbir, M. Z., Abbas, M. A., Numan, M., Evans, M., Ashraf, K., Morrison, I., Morrison, L. J., & Sargison, N. (2019). Development of a deep amplicon sequencing method to determine the proportional species composition of piroplasm haemoprotozoa as an aid in their control. Ticks and Tick-Borne Diseases, 10(6), 1-7. https://doi.org/10.1016/j.ttbdis.2019.101276
Cooper, C., Keatley, S., Northover, A., Gofton, A. W., Brigg, F., Lymbery, A. J., & Thompson, R. C. A. (2018). Next generation sequencing reveals widespread trypanosome diversity and polyparasitism in marsupials from Western Australia. International Journal for Parasitology: Parasites and Wildlife, 7(1), 58-67. https://doi.org/10.1016/j.ijppaw.2018.01.005
Cruaud, P., Rasplus, J., Rodriguez, L. J., & Cruaud, A. (2017). High throughput sequencing of multiple amplicons for barcoding and integrative taxonomy. Scientific Reports, 7, 1-12. https://doi.org/10.1101/073304
Curtis, J., Sorensen, R. E., & Minchella, D. J. (2002). Schistosome genetic diversity: The implications of population structure as detected with microsatellite markers. Parasitology, 125(Suppl), S51-S59. https://doi.org/10.1017/s0031182002002020
Davison, A. (2000). The inheritance of divergent mitochondria in the land snail, Cepaea nemoralis. Journal of Molluscan Studies, 66(2), 143-147. https://doi.org/10.1093/mollus/66.2.143
Eppert, A., Lewis, F. A., Grzywacz, C., Coura-Filho, P., Caldas, I., & Minchella, D. J. (2002). Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence. The Journal of Parasitology, 88(2), 232-236. https://doi.org/10.1645/0022-3395(2002)088[0232:DOSIIM]2.0.CO;2
Esch, G. W., Barger, M. A., & Fellis, K. J. (2002). The transmission of digenetic trematodes: Style, elegance. Complexity. Integrative and Comparative Biology, 42(2), 304-312.
Esch, G. W., Curtis, L., & Barger, M. (2001). A perspective on the ecology of trematode communities in snails. Parasitology, 123(7), 57-75. https://doi.org/10.1017/S0031182001007697
GNU, P. (2007). Free Software Foundation. Bash (3.2. 48)[Unix shell program].
Gusman, A., Azuelos, C., & Breton, S. (2017). No evidence of sex-linked heteroplasmy or doubly-uniparental inheritance of mtDNA in five snail species. Journal of Molluscan Studies, 83(1), 119-122. https://doi.org/10.1093/mollus/eyw034
Hamburger, J., Hoffman, O., Kariuki, H. C., Muchiri, E. M., Ouma, J. H., Koech, D. K., Sturrock, R. F., & King, C. H. (2004). Large-scale, polymerase chain reaction-based surveillance of Schistosoma haematobium DNA in snails from transmission sites in coastal Kenya: A new tool for studying the dynamics of snail infection. The American Journal of Tropical Medicine and Hygiene, 71(6), 765-773. https://doi.org/10.4269/ajtmh.2004.71.765
Hammoud, C., Mulero, S., Van Bocxlaer, B., Boissier, J., Verschuren, D., Albrecht, C., & Huyse, T. (2020a). Datasets, FASTA files, R and bash scripts for “Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing.” [Data set] Dryad data, https://doi.org/10.5061/dryad.qnk98sfg1
Hammoud, C., Mulero, S., Van Bocxlaer, B., Boissier, J., Verschuren, D., Albrecht, C., & Huyse, T. (2020b). Raw sequencing reads from "Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing". [Data set] NCBI SRAI: PRJNA743924.
Hammoud, C., Mulero, S., Van Bocxlaer, B., Boissier, J., Verschuren, D., Albrecht, C., & Huyse, T. (2020c). Processed Amplicon Sequence Variants from " Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing." [Data set] NCBI GenBank, Genbank accessions: MZ546824 - MZ546834 (COI1_snail); MZ540237 - MZ540247 (COI2_snail); MZ600069 - MZ600118 (ITS1_snail); MZ546798 - MZ546803 (NAD1_snail); MZ567152 - MZ567158 (COI1_trematode); MZ558220 - MZ558244 (COI2_trematode); MZ600119 - MZ600142 (ITS2_trematode); MZ546812 - MZ546823 (cytb_trematode); MZ546804 - MZ546811 (NAD1_trematode).
Harris, D. J., & Crandall, K. A. (2000). Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): Implications for phylogenetic and microsatellite studies. Molecular Biology and Evolution, 17(2), 284-291. https://doi.org/10.1093/oxfordjournals.molbev.a026308
Herbold, C. W., Pelikan, C., Kuzyk, O., Hausmann, B., Angel, R., Berry, D., & Loy, A. (2015). A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Frontiers in Microbiology, 6, 731. https://doi.org/10.3389/fmicb.2015.00731
Hopkins, S. R., Ocampo, J. M., Wojdak, J. M., & Belden, L. K. (2016). Host community composition and defensive symbionts determine trematode parasite abundance in host communities. Ecosphere, 7(3), e01278. https://doi.org/10.1002/ecs2.1278
Hotez, P. J., Alvarado, M., Basáñez, M. G., Bolliger, I., Bourne, R., Boussinesq, M., Brooker, S. J., Brown, A. S., Buckle, G., Budke, C. M., Carabin, H., Coffeng, L. E., Fèvre, E. M., Fürst, T., Halasa, Y. A., Jasrasaria, R., Johns, N. E., Keiser, J., King, C. H., … Naghavi, M. (2014). The global burden of disease study 2010: Interpretation and implications for the neglected tropical diseases. PLOS Neglected Tropical Diseases, 8(7). 1-9. https://doi.org/10.1371/journal.pntd.0002865
Jannotti-Passos, L., Magalhães, K., Carvalho, O., & Vidigal, T. (2006). Multiplex PCR for both identification of Brazilian Biomphalaria species (Snaila: Planorbidae) and diagnosis of infection by Schistosoma mansoni (Trematoda: Schistosomatidae). The Journal of Parasitology, 92(2), 401-403. https://doi.org/10.1645/GE-593R1.1
Jusino, M. A., Banik, M. T., Palmer, J. M., Wray, A. K., Xiao, L., Pelton, E., Barber, J. R., Kawahara, A. Y., Gratton, C., Peery, M. Z., & Lindner, D. L. (2019). An improved method for utilizing high-throughput amplicon sequencing to determine the diets of insectivorous animals. Molecular Ecology Resources, 19(1), 176-190. https://doi.org/10.1111/1755-0998.12951
Kamel, B., Laidemitt, M. R., Lu, L., Babbitt, C., Weinbaum, O. L., Mkoji, G. M., & Loker, E. S. (2021). Detecting and identifying Schistosoma infections in snails and aquatic habitats: A systematic review. PLOS Neglected Tropical Diseases, 15(3), e0009175. https://doi.org/10.1371/journal.pntd.0009175
Karstens, L., Asquith, M., Davin, S., Fair, D., Gregory, W. T., Wolfe, A. J., Braun, J., & McWeeney, S. (2019). Controlling for contaminants in low-biomass 16S rRNA gene sequencing experiments. mSystems 4, e00290-19. https://doi.org/10.1128/mSystems.00290-19
Laidemitt, M. R., Anderson, L. C., Wearing, H. J., Mutuku, M. W., Mkoji, G. M., & Loker, E. S. (2019). Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis. eLife, 8, 1-17. https://doi.org/10.7554/eLife.50095
Le Clecʼh, W., Diaz, R., Chevalier, F. D., McDew-White, M., & Anderson, T. (2019). Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations. Parasites & Vectors, 12(1), 485. https://doi.org/10.1186/s13071-019-3741-z
Lerch, A., Koepfli, C., Hofmann, N. E., Messerli, C., Wilcox, S., Kattenberg, J., Betuela, I., O’Connor, L., Mueller, I., & Felger, I. (2017). Development of amplicon deep sequencing markers and data analysis pipeline for genotyping multi-clonal malaria infections. BMC Genomics, 18(1), 864. https://doi.org/10.1186/s12864-017-4260-y
Lockyer, A. E., Jones, C. S., Noble, L. R., & Rollinson, D. (2004). Trematodes and snails: An intimate association. Canadian Journal of Zoology/Revue Canadien De Zoologie, 82(2), 251-269. https://doi.org/10.1139/z03-215
Loker, E. S., Moyo, H. G., & Gardner, S. L. (1981). Trematode-snail associations in nine non-lacustrine habitats in the Mwanza region of Tanzania. Parasitology, 83(2), 381-399. https://doi.org/10.1017/S0031182000085383
Lopez, J. V., Yuhki, N., Masuda, R., Modi, W., & O’Brien, S. J. (1994). Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution, 39(2), 174-190. https://doi.org/10.1007/bf00163806
Lusk, R. W. (2014). Diverse and widespread contamination evident in the unmapped depths of high throughput sequencing data. PLoS One, 9(10), e110808. https://doi.org/10.1371/journal.pone.0110808
MacConaill, L. E., Burns, R. T., Nag, A., Coleman, H. A., Slevin, M. K., Giorda, K., Light, M., Lai, K., Jarosz, M., McNeill, M. S., Ducar, M. D., Meyerson, M., & Thorner, A. R. (2018). Unique, dual-indexed sequencing adapters with UMIs effectively eliminate index cross-talk and significantly improve sensitivity of massively parallel sequencing. BMC Genomics, 19(1), 30. https://doi.org/10.1186/s12864-017-4428-5
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal, 17(1), 10-12. https://doi.org/10.14806/ej.17.1.200
Mesquita, S. G., Rodrigues-Luiz, G. F., Reis-Cunha, J. L., Cardoso, M. S., De Mendonça, C., Bueno, L. L., Fujiwara, R. T., Pinto, H. A., Caldeira, R. L., & Bartholomeu, D. C. (2020). A multiplex PCR protocol for rapid differential identification of four families of trematodes with medical and veterinary importance transmitted by Biomphalaria Preston, 1910 snails. Acta Tropica, 211, 105655. https://doi.org/10.1016/j.actatropica.2020.105655
Minchella, D., Sollenberger, K., & Pereira De Souza, C. (1995). Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology, 111(2), 217-220. https://doi.org/10.1017/S0031182000064970
Moszczyńska, A., Locke, S. A., McLaughlin, J. D., Marcogliese, D. J., & Crease, T. J. (2009). Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources, 9(Suppl s1), 75-82. https://doi.org/10.1111/j.1755-0998.2009.02634.x
Mulero, S., Boissier, J., Allienne, J.-F., Quilichini, Y., Foata, J., Pointier, J.-P., & Rey, O. (2020). Environmental DNA for detecting Bulinus truncatus: A new environmental surveillance tool for schistosomiasis emergence risk assessment. Environmental DNA, 2, 161-174. https://doi.org/10.1002/edn3.53
Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of trematode species. Advances in Parasitology, 60, 101-163. https://doi.org/10.1016/S0065-308X(05)60002-4
Norton, A., Rollinson, D., Richards, L., & Webster, J. (2008). Simultaneous infection of Schistosoma mansoni and S. rodhaini in Biomphalaria glabrata: Impact on chronobiology and cercarial behaviour. Parasites and Vectors, 1(1), 43. https://doi.org/10.1186/1756-3305-1-43
Pages, J.-R., & Théron, A. (1990). Analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium, S. intercalatum, S. bovis, and their hybrid progeny. International Journal for Parasitology, 20(2), 193-197. https://doi.org/10.1016/0020-7519(90)90100-2
Palmer, J. M., Jusino, M. A., Banik, M. T., & Lindner, D. L. (2018). Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data. PeerJ, 6, e4925. https://doi.org/10.7717/peerj.4925
Parakatselaki, M. E., Saavedra, C., & Ladoukakis, E. D. (2016). Searching for doubly uniparental inheritance of mtDNA in the apple snail Pomacea diffusa. Mitochondrial DNA, 27(6), 4000-4002. https://doi.org/10.3109/19401736.2014.989521
Parkin, E. J., & Butlin, R. K. (2004). Within- and between-individual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. Molecular Biology and Evolution, 21(8), 1595-1601. https://doi.org/10.1093/molbev/msh163
Pennance, T., Archer, J., Lugli, E. B., Rostron, P., Llanwarne, F., Ali, S. M., Amour, A. K., Suleiman, K. R., Li, S., Rollinson, D., Cable, J., Knopp, S., Allan, F., Ame, S. M., & Webster, B. L. (2020). Development of a molecular snail xenomonitoring assay to detect Schistosoma haematobium and Schistosoma bovis infections in their Bulinus snail hosts. Molecules, 25(17), 4011. https://doi.org/10.3390/molecules25174011
Pinaud, S., Portela, J., Duval, D., Nowacki, F. C., Olive, M. A., Allienne, J. F., Galinier, R., Dheilly, N. M., Kieffer-Jaquinod, S., Mitta, G., Théron, A., & Gourbal, B. (2016). A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathogens, 12(1), e1005361. https://doi.org/10.1371/journal.ppat.1005361
Pitchford, R. J., Meyling, A. H., Meyling, J., & Du Toit, J. F. (1969). Cercarial shedding patterns of various schistosome species under outdoor conditions in the Transvaal. Annals of Tropical Medicine & Parasitology, 63(3), 359-371. https://doi.org/10.1080/00034983.1969.11686637
Portela, J., Duval, D., Rognon, A., Galinier, R., Boissier, J., Coustau, C., Mitta, G., Theron, A., & Gourbal, B. (2013). Evidence for specific genotype-dependent immune priming in the lophotrochozoan Biomphalaria glabrata snail. Journal of Innate Immunity, 5(3), 261-276. https://doi.org/10.1159/000345909
Portet, A., Pinaud, S., Chaparro, C., Galinier, R., Dheilly, N. M., Portela, J., Charriere, G., Allienne, J. F., Duval, D., & Gourbal, B. (2019). Sympatric versus allopatric evolutionary contexts shape differential immune response in Biomphalaria / Schistosoma interaction. PLoS Path, 15(3), e1007647. https://doi.org/10.1371/journal.ppat.1007647
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/
Rodriguez-Lanetty, M., & Hoegh-Guldberg, O. (2002). The phylogeography and connectivity of the latitudinally widespread scleractinian coral Plesiastrea versipora in the Western Pacific. Molecular Ecology, 11(7), 1177-1189. https://doi.org/10.1046/j.1365-294X.2002.01511.x
Schols, R., Carolus, H., Hammoud, C., Mulero, S., Mudavanhu, A., & Huyse, T. (2019). A rapid diagnostic multiplex PCR approach for xenomonitoring of human and animal schistosomiasis in a ‘One Health’ context. Transactions of the Royal Society of Tropical Medicine and Hygiene, 113(11), 722-729. https://doi.org/10.1093/trstmh/trz067
Schols, R., Mudavanhu, A., Carolus, H., Hammoud, C., Muzarabani, K. C., Barson, M., & Huyse, T. (2020). Exposing the barcoding void: An integrative approach to study snail-borne parasites in a one health context. Frontiers in Veterinary Science, 7, 605280. https://doi.org/10.3389/fvets.2020.605280
Schwanbek, A., Becker, W., & Rupprecht, H. (1986). Quantification of parasite development in the host-parasite system Biomphalaria glabrata and Schistosoma mansoni. Zeitschrift für Parasitenkunde Parasitology Research, 72(3), 365-373. https://doi.org/10.1007/BF00928747
Soldánová, M., Faltýnková, A., Scholz, T., & Kostadinova, A. (2011). Parasites in a man-made landscape: Contrasting patterns of trematode flow in a fishpond area in Central Europe. Parasitology, 138(6), 789-807. https://doi.org/10.1017/S0031182011000291
Soldánová, M., Kuris, A. M., Scholz, T., & Lafferty, K. D. (2012). The role of spatial and temporal heterogeneity and competition in structuring trematode communities in the great pond snail, Lymnaea stagnalis (L.). The Journal of Parasitology, 98(3), 460-471. https://doi.org/10.1645/GE-2964.1
Steinauer, M. L., Hanelt, B., Agola, L. E., Mkoji, G. M., & Loker, E. S. (2009). Genetic structure of Schistosoma mansoni in western Kenya: The effects of geography and host sharing. International Journal for Parasitology, 39(12), 1353-1362. https://doi.org/10.1016/j.ijpara.2009.04.010
Steinauer, M. L., Hanelt, B., Mwangi, I. N., Maina, G. M., Agola, L. E., Kinuthia, J. M., Mutuku, M. W., Mungai, B. N., Wilson, W. D., Mkoji, G. M., & Loker, E. S. (2008). Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Molecular Ecology, 17(23), 5062-5074. https://doi.org/10.1111/j.1365-294X.2008.03957.x
Stothard, J. R., Brémond, P., Andriamaro, L., Loxton, N. J., Sellin, B., Sellin, E., & Rollinson, D. (2000). Molecular characterization of the freshwater snail Lymnaea natalensis (Gastropoda: Lymnaeidae) on Madagascar with an observation of an unusual polymorphism in ribosomal small subunit genes. Journal of Zoology, 252, 303-315. https://doi.org/10.1111/j.1469-7998.2000.tb00625.x
Sword, G. A., Senior, L. B., Gaskin, J. F., & Joern, A. (2007). Double trouble for grasshopper molecular systematics: Intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acrididae). Systematic Entomology, 32(3), 420-428. https://doi.org/10.1111/j.1365-3113.2007.00385.x
Théron, A., Gérard, C., & Moné, H. (1992). Early enhanced growth of the digestive gland of Biomphalaria glabrata infected with Schistosoma mansoni: Side effect or parasite manipulation? Parasitology Research, 78(5), 445-450. https://doi.org/10.1007/BF00931703
Théron, A., Rognon, A., Gourbal, B., & Mitta, G. (2014). Multi-parasite host susceptibility and multi-host parasite infectivity: A new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 26, 80-88. https://doi.org/10.1016/j.meegid.2014.04.025
Théron, A., & Touassem, R. (1989). Schistosoma rodhaini: Intramolluscan larval development, migration and replication processes of daughter sporocysts. Acta Tropica, 46(1), 39-45. https://doi.org/10.1016/0001-706X(89)90014-4
Thiele, E. A., & Minchella, D. J. (2013). Molecular assessment of trematode co-infection and intraspecific competition in molluscan intermediate hosts. Molecular and Biochemical Parasitology, 187(1), 52-59. https://doi.org/10.1016/j.molbiopara.2012.12.003
Thomaz, D., Guiller, A., & Clarke, B. C. (1996). Extreme divergence of mitochondrial DNA within species of pulmonate land snails. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263(1368), 363-368. https://doi.org/10.1098/rspb.1996.0056
Toledo, R., & Fried, B. (2014) Digenetic trematodes, Advances in experimental medicine and biology. (pp. 21-23). Springer. https://doi.org/10.1007/978-1-4939-0915-5
Van den Broeck, F., Geldof, S., Polman, K., Volckaert, F. A. M., & Huyse, T. (2011). Optimal sample storage and extraction procotols for reliable multilocus genotyping of the human parasite Schistosoma mansoni. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 11(6), 1413-1418. https://doi.org/10.1016/j.meegid.2011.05.006
Vanhove, M. P., Tessens, B., Schoelinck, C., Jondelius, U., Littlewood, D. T., Artois, T., & Huyse, T. (2013). Problematic barcoding in flatworms: A case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys, 365, 355-379. https://doi.org/10.3897/zookeys.365.5776
Vierna, J., Martínez-Lage, A., & González-Tizón, A. M. (2009). Analysis of ITS1 and ITS2 sequences in Ensis razor shells: Suitability as molecular markers at the population and species levels, and evolution of these ribosomal DNA spacers. Genome, 53(1), 23-34. https://doi.org/10.1139/G09-080
World Health Organization (2017). Integrating neglected tropical diseases into global health and development: Fourth WHO report on neglected tropical diseases. Geneva. Licence: CC BY-NC-SA 3.0 IGO.
World Health Organization (2020). Ending the neglect to attain the Sustainable Development Goals - A road map for neglected tropical diseases 2021-2030. Geneva: Licence: CC BY-NC-SA 3.0 IGO.
Xu, J., Zhang, Q., Xu, X., Wang, Z., & Qi, J. (2009). Intragenomic variability and pseudogenes of ribosomal DNA in stone flounder Kareius bicoloratus. Molecular Phylogenetics and Evolution, 52(1), 157-166. https://doi.org/10.1016/j.ympev.2009.03.031

Auteurs

Cyril Hammoud (C)

Limnology Unit, Department of Biology, Ghent University, Gent, Belgium.
Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium.

Stephen Mulero (S)

IHPE, Univ. Montpellier, CNRS, Univ. Perpignan Via Domitia, IFREMER, Perpignan, France.

Bert Van Bocxlaer (B)

Limnology Unit, Department of Biology, Ghent University, Gent, Belgium.
Univ. Lille, UMR 8198 Evo-Eco-Paleo, CNRS, Lille, France.

Jérôme Boissier (J)

IHPE, Univ. Montpellier, CNRS, Univ. Perpignan Via Domitia, IFREMER, Perpignan, France.

Dirk Verschuren (D)

Limnology Unit, Department of Biology, Ghent University, Gent, Belgium.

Christian Albrecht (C)

Systematics & Biodiversity Lab, Department of Animal Ecology & Systematics, Justus Liebig University, Giessen, Germany.

Tine Huyse (T)

Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium.
Laboratory of Biodiversity and Evolutionary Genomics, University of Leuven, Leuven, Belgium.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH