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Genetic connectivity of trypanosomes between tsetse-infested and tsetse-free areas of Kenya

Published online by Cambridge University Press:  28 October 2021

Naomi N. Kimenyi ,
Kelvin M. Kimenyi ,
Nelson O. Amugune  and
Merid N. Getahun Open the ORCID record for Merid N. Getahun [Opens in a new window]
Naomi N. Kimenyi
Affiliation:
International Center for Insect Physiology and Ecology (icipe), P. O. Box 30772, Nairobi 00100, Kenya School of Biological Sciences, The University of Nairobi, Nairobi, Kenya
Kelvin M. Kimenyi
Affiliation:
Center for Biotechnology and Bioinformatics (CEBIB), The University of Nairobi, Nairobi, Kenya
Nelson O. Amugune
Affiliation:
School of Biological Sciences, The University of Nairobi, Nairobi, Kenya
Merid N. Getahun*
Affiliation:
International Center for Insect Physiology and Ecology (icipe), P. O. Box 30772, Nairobi 00100, Kenya
*
Author for correspondence: Merid N. Getahun, E-mail: [email protected]
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Abstract

The prevalence rates of trypanosomes, including those that require cyclical transmission by tsetse flies, are widely distributed in Africa. Trypanosoma brucei and Trypanosoma congolense are actively maintained in regions where there are no tsetse flies although at low frequencies. Whether this could be due to an independent evolutionary origin or multiple introduction of trypanosomes due to continuous movement of livestock between tsetse-free and -infested areas is not known. Thus, the aim of the study was to carry out microsatellite genotyping to explore intra-specific genetic diversity between T. (Trypanozoon), T. congolense and Trypanosoma vivax from the two regions: tsetse infested and tsetse free. Microsatellite genotyping showed geographical origin-based structuring among T. (Trypanozoon) isolates. There was a clear separation between isolates from the two regions signalling the potential of microsatellite markers as diagnostic markers for T. brucei and Trypanosoma evansi isolates. Trypanosoma vivax isolates also clustered largely based on the sampling location with a significant differentiation between the two locations. However, our results revealed that T. congolense isolates from Northern Kenya are not genetically separated from those from Coastal Kenya. Therefore, these isolates are likely introduced in the region through animal movement. Our results demonstrate the occurrence of both genetic connectivity as well as independent evolutionary origin, depending on the trypanosome species between the two ecologies.

Keywords

Genetic diversitymicrosatellitestrypanosomestsetse belttsetse-free ecologies
Type
Research Article
Information
Parasitology , Volume 149 , Issue 3 , March 2022 , pp. 285 - 297
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Adamack, G (2014) Introduction to PopGenReport using PopGenReport Ver. 2.0.Google Scholar
Adams, ER, Hamilton, PB, Rodrigues, AC, Malele, II, Delespaux, V, Teixeira, MM and Gibson, W (2010) New Trypanosoma (Duttonella) vivax genotypes from tsetse flies in East Africa. Parasitology 137, 641–650.CrossRefGoogle ScholarPubMed
Balmer, O, Palma, C, Macleod, A and Caccone, A (2006) Characterization of di-, tri- and tetranucleotide microsatellite markers with perfect repeats for Trypanosoma brucei and related species. Molecular Ecology Notes 6, 508–510.CrossRefGoogle ScholarPubMed
Borst, P, Fase-Fowler, F and Gibson, WC (1987) Kinetoplast DNA of Trypanosoma evansi. Molecular Biochemical Parasitology 23, 31–38.CrossRefGoogle ScholarPubMed
Büscher, P, Gonzatti, MI, Hebert, L, Inoue, N, Pascucci, I, Schnaufer, A, Suganuma, K, Touratier, L and Reet, NV (2019) Equine trypanosomosis: enigmas and diagnostic challenges. Parasites and Vectors 12, 1–8.CrossRefGoogle ScholarPubMed
Caljon, G, Vooght, L and Van Den Abbele, J (2014) The biology of tsetse-trypanosome interactions. Trypanosomes and Trypanosomiasis 53, 1–83.Google Scholar
Carnes, J, Anupama, A, Balmer, O, Jackson, A, Lewis, M, Brown, R, Cestari, I, Desquesnes, M, Gendrin, C, Hertz-Fowler, C, Imamura, H, Ivens, A, Kořený, L, Lai, DH, MacLeod, A, McDermott, SM, Merritt, C, Monnerat, S, Moon, W, Myler, P, Phan, I, Ramasamy, G, Sivam, D, Lun, ZR, Lukeš, J, Stuart, K and Schnaufer, A (2015) Genome and phylogenetic analyses of Trypanosoma evansi reveal extensive similarity to T. brucei and multiple independent origins for dyskinetoplasty. PLoS Neglected Tropical Diseases 9, 1.CrossRefGoogle Scholar
Claes, F, Büscher, P, Touratier, L and Goddeeris, BM (2005) Trypanosoma equiperdum: master of disguise or historical mistake? Trends in Parasitology 21, 316–321.CrossRefGoogle ScholarPubMed
Desquesnes, M and Dia, ML (2003) Mechanical transmission of Trypanosoma congolense in cattle by the African tabanid Atylotus agrestis. Experimental Parasitology 105, 226–231.CrossRefGoogle ScholarPubMed
Desquesnes, M and Dia, ML (2004) Mechanical transmission of Trypanosoma vivax in cattle by the African tabanid Atylotus fuscipes. Veterinary Parasitology 119, 9–19.CrossRefGoogle ScholarPubMed
Duffy, CW, Morrison, LJ, Black, A, Pinchbeck, GL, Christley, RM, Schoenefeld, A, Tait, A, Turner, CM and MacLeod, A (2009) Trypanosoma vivax displays a clonal population structure. International Journal for Parasitology 39, 1475–1483.CrossRefGoogle ScholarPubMed
Earl, DA and von Holdt, BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.CrossRefGoogle Scholar
Echodu, R, Sistrom, M, Bateta, R, Murilla, G, Okedi, L, Aksoy, S, Enyioha, C, Enyaru, J, Opiyo, E, Gibson, W and Caccone, A (2015) Genetic diversity and population structure of Trypanosoma brucei in Uganda: implications for the epidemiology of sleeping sickness and Nagana. PLOS Neglected Tropical Diseases, 1–19. doi: 10.5061/dryad.m7q4cGoogle ScholarPubMed
El-Sayed, NM, Myler, PJ, Blandin, G, Berriman, M, Crabtree, J, Aggarwal, G, Caler, E, Renauld, H, Worthey, EA, Hertz-Fowler, C, Ghedin, E, Peacock, C, Bartholomeu, DC, Haas, BJ, Tran, AN, Wortman, JR, Alsmark, UC, Angiuoli, S, Anupama, A, Badger, J, Bringaud, F, Cadag, E, Carlton, JM, Cerqueira, GC, Creasy, T, Delcher, AL, Djikeng, A, Embley, TM, Hauser, C, Ivens, AC, Kummerfeld, SK, Pereira-Leal, JB, Nilsson, D, Peterson, J, Salzberg, SL, Shallom, J, Silva, JC, Sundaram, J, Westenberger, S, White, O, Melville, SE, Donelson, JE, Andersson, B, Stuart, KD and Hall, N (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science (New York, N.Y.) 309, 404–409.CrossRefGoogle ScholarPubMed
Evanno, G, Regnaut, S and Goudet, J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.CrossRefGoogle ScholarPubMed
Fasogbon, AI, Knowles, G and Gardiner, PR (1990) A comparison of the isoenzymes of Trypanosoma (Duttonella) vivax isolates from East and West Africa. International Journal for Parasitology 20, 389–394.CrossRefGoogle ScholarPubMed
Fikru, R, Hagos, A, Rogé, S, Reyna-Bello, A, Gonzatti, MI, Merga, B, Goddeeris, BM and Büscher, P (2014) A proline racemase based PCR for identification of Trypanosoma vivax in cattle blood. PLoS ONE 9, 1–7.CrossRefGoogle ScholarPubMed
Fikru, R, Matetovici, I, Rogé, S, Merga, B, Goddeeris, BM, Büscher, P and Van Reet, N (2016) Ribosomal DNA analysis of tsetse and non-tsetse transmitted Ethiopian Trypanosoma vivax strains in view of improved molecular diagnosis. Veterinary Parasitology 220, 15–22.CrossRefGoogle ScholarPubMed
Garcia, HA, Rodrigues, AC, Rodrigues, CMF, Bengaly, Z, Minervino, AHH, Riet-Correa, F, Machado, RZ, Paiva, F, Batista, JS, Neves, L, Hamilton, PB and Teixeira, MMG (2014) Microsatellite analysis supports clonal propagation and reduced divergence of Trypanosoma vivax from asymptomatic to fatally infected livestock in South America compared to West Africa. Parasites and Vectors 7, 1–13.CrossRefGoogle ScholarPubMed
Getahun, M, Villinger J, Bargul JL, Orone A, Ngiela J, Ahuya PO, Muema JM, Saini RK, Torto B and Masiga DK (2020) Molecular characterization of pathogenic African trypanosomes in biting flies and camels in surra-endemic areas outside the tsetse fly belt in Kenya, pp. 1–37. doi: 10.1101/2020.06.18.156869CrossRefGoogle Scholar
Gibson, WC, Wilson, AJ and Moloo, SK (1983) Characterisation of Trypanosoma evansi (T. (Trypanozoon)) from camels in Kenya using isoenzyme electrophoresis. Research in Veterinary Science 34, 114–118.CrossRefGoogle Scholar
Goudet, J (2003) FSTAT (version 2.9.4), a program (for Windows 95 and above) to estimate and test population genetics parameters, pp. 1–54.Google Scholar
Jombart, T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford, England) 24, 1403–1405.CrossRefGoogle Scholar
Jombart, T, Devillard, S and Balloux, F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. doi: 10.1186/1471-2156-11-94CrossRefGoogle Scholar
Kalinowski, ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5, 539–543.CrossRefGoogle Scholar
Kalinowski, ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5, 187–189.CrossRefGoogle Scholar
Kamidi, CM, Saarman NP, Dion K, Mireji PO, Ouma C, Murilla G, Aksoy S, Schnaufer A and Caccone A (2017) Multiple evolutionary origins of Trypanosoma evansi in Kenya. PLOS Neglected Tropical Diseases, 1–21. doi: 10.5061/dryad.8g678.FundingGoogle ScholarPubMed
Lai, DH, Hashimi H, Lun ZR, Ayala FJ and Lukes J (2008) Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proceedings of the National Academy of Sciences 105, 1999–2004.CrossRefGoogle ScholarPubMed
Li, MM, Li BL, Jiang SX, Zhao YW, Xu XL and Wu JX (2019) Microsatellite-based analysis of genetic structure and gene flow of Mythimna separata (Walker) (Lepidoptera: Noctuidae) in China. Ecology and Evolution 9, 13426–13437.CrossRefGoogle ScholarPubMed
Mantel, N (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.Google Scholar
Moreno, SA and Nava, M (2015) Trypanosoma evansi is alike to Trypanosoma brucei brucei in the subcellular localisation of glycolytic enzymes. Memorias do Instituto Oswaldo Cruz 110, 468–475.CrossRefGoogle ScholarPubMed
Njiru, ZK, Constantine CC, Ndung'u JM, Robertson I, Okaye S, Thompson RC and Reid SA (2004) Detection of Trypanosoma evansi in camels using PCR and CATT/T. evansi tests in Kenya. Veterinary Parasitology 124, 187–199.CrossRefGoogle ScholarPubMed
Njiru, ZK, Constantine CC, Guya S, Crowther J, Kiragu JM, Thompson RC and Dávila AM (2005) The use of ITS1 rDNA PCR in detecting pathogenic African trypanosomes. Parasitology Research 95, 186–192.CrossRefGoogle ScholarPubMed
Njiru, ZK, Constantine CC, Masiga DK, Reid SA, Thompson RC and Gibson WC (2006) Characterization of Trypanosoma evansi type B. Infection Genetics and Evolution 6, 292–300.CrossRefGoogle ScholarPubMed
Oksanen, AJ, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E and Wagner H (2020) Package ‘vegan’.Google Scholar
Ooi, CP, Schuster S, Travaille CC, Bertiaux E, Cosson A, Goyard S, Perrot S and Rotureau B (2016) The cyclical development of Trypanosoma vivax in the tsetse fly involves an asymmetric division. Frontiers in Cellular and Infection Microbiology 6, 1–16.CrossRefGoogle ScholarPubMed
Oyieke, FA and Reid, G (2003) The mechanical transmission of Trypanosoma evansi by Haematobia minuta (Diptera: Muscidae) and Hippobosca camelina (Diptera: Hippoboscidae) from an infected camel to a mouse and the survival of trypanosomes in fly mouthparts and gut. Folia Veterinaria 47, 38–41.Google Scholar
Peakall, R and Smouse, PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.CrossRefGoogle Scholar
Porras-Hurtado, L, Ruiz Y, Santos C, Phillips C, Carracedo A and Lareu MV (2013) An overview of STRUCTURE: applications, parameter settings, and supporting software. Frontiers in Genetics 4, 1–13.CrossRefGoogle ScholarPubMed
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle ScholarPubMed
Prugnolle, F and De Meeûs, T (2008) The impact of clonality on parasite population genetic structure. Parasite 15, 455–457.CrossRefGoogle Scholar
Roditi, I and Lehane, MJ (2008) Interactions between trypanosomes and tsetse flies. Current Opinion in Microbiology 11, 345–351.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Neves L, Garcia HA, Viola LB, Marcili A, Da Silva FM, Sigauque I, Batista JS, Paiva F and Teixeira MM (2008) Phylogenetic analysis of Trypanosoma vivax supports the separation of South American/West African from East African isolates and a new T. vivax-like genotype infecting a nyala antelope from Mozambique. Parasitology 135, 1317–1328.CrossRefGoogle Scholar
Rodrigues, CM, Garcia HA, Rodrigues AC, Costa-Martins AG, Pereira CL, Pereira DL, Bengaly Z, Neves L, Camargo EP, Hamilton PB and Teixeira MM (2017) New insights from Gorongosa National Park and Niassa National Reserve of Mozambique increasing the genetic diversity of Trypanosoma vivax and Trypanosoma vivax-like in tsetse flies, wild ungulates and livestock from East Africa. Parasites and Vectors 10, 1–16.CrossRefGoogle ScholarPubMed
Rotureau, B and Van Den Abbeele, J (2013) Through the dark continent: African trypanosome development in the tsetse fly. Frontiers in Cellular and Infection Microbiology 4, 1–7.Google Scholar
Rousset, F, Lopez, L and Belkhir, K (2020) R package: genepop, p. 16.Google Scholar
Salim, B, de Meeûs T, Bakheit MA, Kamau J, Nakamura I and Sugimoto C (2011) Population genetics of Trypanosoma evansi from camel in the Sudan. PLoS Neglected Tropical Diseases 5, e1196.CrossRefGoogle ScholarPubMed
Schnaufer, A (2010) Evolution of dyskinetoplastic trypanosomes: how, and how often? Trends Parasitology 26, 557–558.CrossRefGoogle Scholar
Senan, S, Kizhakayil D, Sasikumar B and Sheeja TE (2014) Methods for development of microsatellite markers: an overview. Notulae Scientia Biologicae 6, 1–13.CrossRefGoogle Scholar
Sistrom, M, Echodu R, Hyseni C, Enyaru J, Aksoy S and Caccone A (2013) Taking advantage of genomic data to develop reliable microsatellite loci in Trypanosoma brucei. Molecular Ecology Resources e33, 1–9.Google Scholar
Solymos, P, Cori, A and Calboli, F (2020) Package ‘adegenet’ R topics documented.Google Scholar
Szöőr, B, Silvester, E and Matthews, KR (2020) A leap into the unknown – early events in African Trypanosome transmission. Trends in Parasitology 36, 266–278.CrossRefGoogle ScholarPubMed
Wells, EA (1972) The importance of mechanical transmission in the epidemiology of nagana: a review. Tropical Animal Health and Production 4, 74–89.CrossRefGoogle ScholarPubMed
Wen, YZ, Lun, ZR, Zhu, XQ, Hide, G and Lai, DH (2016) Further evidence from SSCP and ITS DNA sequencing support Trypanosoma evansi and Trypanosoma equiperdum as subspecies or even strains of Trypanosoma brucei. Infection, Genetics and Evolution 41, 56–62.CrossRefGoogle ScholarPubMed
Whitlock, MC and McCauley, DE (1999) Indirect measures of gene flow and migration: F ST≠1/(4N m+1). Journal of Revenue and Pricing Management 82, 117–125.Google Scholar
Wilson, GA and Rannala, B (2003) Bayesian Inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–1191.CrossRefGoogle ScholarPubMed
Wright, S (1990) Evolution in Mendelian populations. Bulletin of Mathematical Biology 52, 241–295.CrossRefGoogle ScholarPubMed
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