Volume 99, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



The tsetse fly , the major vector of the parasite that causes animal African trypanosomiasis in Kenya, has been subject to intense control measures with only limited success. The population dynamics and dispersal patterns that underlie limited success in vector control campaigns remain unresolved, and knowledge on genetic connectivity can provide insights, and thereby improve control and monitoring efforts. We therefore investigated the population structure and estimated migration and demographic parameters in using genotypic data from 11 microsatellite loci scored in 250 tsetse flies collected from eight localities in Kenya. Clustering analysis identified two genetically distinct eastern and western clusters (mean between-cluster = 0.202) separated by the Great Rift Valley. We also found evidence of admixture and migration between the eastern and western clusters, isolation by distance, and a widespread signal of inbreeding. We detected differences in population dynamics and dispersal patterns between the western and eastern clusters. These included lower genetic diversity (allelic richness; 7.48 versus 10.99), higher relatedness (percent related individuals; 21.4% versus 9.1%), and greater genetic differentiation (mean within-cluster ; 0.183 versus 0.018) in the western than the eastern cluster. Findings are consistent with the presence of smaller, less well-connected populations in Western relative to eastern Kenya. These data suggest that recent anthropogenic influences such as land use changes and vector control programs have influenced population dynamics in in Kenya, and that vector control efforts should include some region-specific strategies to effectively control this disease vector.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Buguet A, Mpanzou G, Bentivoglio M, Bentivoglio M, Cavalheiro E, Kristensson K, Patel N, , 2014. Human african trypanosomiasis: a highly neglected neurological disease. , eds. Neglected Tropical Diseases and Conditions of the Nervous System. New York, NY: Springer, 165181. [Google Scholar]
  2. Courtin F, 2015. Reducing human-tsetse contact significantly enhances the efficacy of sleeping sickness active screening campaigns: a promising result in the context of elimination. PLoS Negl Trop Dis 9: e0003727. [Google Scholar]
  3. Alsan M, , 2015. The effect of the tsetse fly on African development. Am Econ Rev 105: 382410. [Google Scholar]
  4. Fèvre EM, Wissmann BV, Welburn SC, Lutumba P, , 2008. The burden of human African trypanosomiasis. PLoS Negl Trop Dis 2: e333. [Google Scholar]
  5. Muhanguzi D, Picozzi K, Hattendorf J, Thrusfield M, Kabasa JD, Waiswa C, Welburn SC, , 2014. The burden and spatial distribution of bovine African trypanosomes in small holder crop-livestock production systems in Tororo District, south-eastern Uganda. Parasit Vectors 7: 603. [Google Scholar]
  6. La Greca F, Magez S, , 2011. Vaccination against trypanosomiasis. Hum Vaccin 7: 12251233. [Google Scholar]
  7. Aksoy S, , 2003. Control of tsetse flies and trypanosomes using molecular genetics. Vet Parasitol 115: 125145. [Google Scholar]
  8. CDC, 2015. Parasites—Africa trypanosomiasis (Also Known as Sleeping Sickness). Centres for Disease Control and Prevention. Available at: https://www.cdc.gov/parasites/sleepingsickness/treatment.html. Accessed July 13, 2017.
  9. Anene BM, Onah DN, Nawa Y, , 2001. Drug resistance in pathogenic African trypanosomes: what hopes for the future? Vet Parasitol 96: 83100. [Google Scholar]
  10. Wilkinson SR, Kelly JM, , 2009. Trypanocidal drugs: mechanisms, resistance and new targets. Expert Rev Mol Med 11: e31. [Google Scholar]
  11. Barrett MP, Vincent IM, Burchmore RJ, Kazibwe AJ, Matovu E, , 2011. Drug resistance in human African trypanosomiasis. Future Microbiol 6: 10371047. [Google Scholar]
  12. Welburn SC, Molyneux DH, Maudlin I, , 2016. Beyond tsetse—implications for research and control of human African trypanosomiasis epidemics. Trends Parasitol 32: 230241. [Google Scholar]
  13. Aksoy S, Caccone A, Galvani AP, Okedi LM, , 2013. Glossina fuscipes populations provide insights for human African trypanosomiasis transmission in Uganda. Trends Parasitol 29: 394406. [Google Scholar]
  14. Brightwell R, Dransfield R, , 1997. Odour attractants for tsetse: Glossina austeni, G. brevipalpis and G. swynnertoni. Med Vet Entomol 11: 297299. [Google Scholar]
  15. Dransfield RD, Brightwell R, Kyorku C, Williams B, , 1990. Control of tsetsefly (Diptera: Glossinidae) populations using traps at Nguruman, south-west Kenya. Bull Entomol Res 265276. [Google Scholar]
  16. Echessah PN, Swallow BM, Kamara DW, Curry JJ, , 1997. Willingness to contribute labor and money to tsetse control: application of contingent valuation in Busia District, Kenya. World Dev 25: 239253. [Google Scholar]
  17. Maudlin I, , 2006. African trypanosomiasis. Ann Trop Med Parasitol 100: 679701. [Google Scholar]
  18. Muriuki GW, Njoka TJ, Reid RS, Nyariki DM, , 2005. Tsetse control and land-use change in Lambwe valley, south-western Kenya. Agric Ecosyst Environ 106: 99107. [Google Scholar]
  19. Schofield CJ, Kabayo JP, , 2008. Trypanosomiasis vector control in Africa and Latin America. Parasit Vectors 1: 24. [Google Scholar]
  20. Torr SJ, Hargrove JW, Vale GA, , 2005. Towards a rational policy for dealing with tsetse. Trends Parasitol 21: 537541. [Google Scholar]
  21. Vreysen MJ, , 2001. Principles of area-wide integrated tsetse fly control using the sterile insect technique. Med Trop (Mars) 61: 397411. [Google Scholar]
  22. Wellde BT, Waema D, Chumo DA, Reardon MJ, Oloo F, Njogu AR, Opiyo EA, Mugutu S, , 1989. Review of tsetse control measures taken in the Lambwe Valley in 1980–1984. Ann Trop Med Parasitol 83 (Suppl 1): 119125. [Google Scholar]
  23. Mbewe NJ, Saini RK, Torto B, Irungu J, Yusuf AA, Pirk CWW, , 2018. Sticky small target: an effective sampling tool for tsetse fly Glossina fuscipes fuscipes Newstead, 1910. Parasit Vectors 11: 268. [Google Scholar]
  24. Shaw AP, Tirados I, Mangwiro CT, Esterhuizen J, Lehane MJ, Torr SJ, Kovacic V, , 2015. Costs of using “tiny targets” to control Glossina fuscipes fuscipes, a vector of gambiense sleeping sickness in Arua District of Uganda. PLoS Negl Trop Dis 9: e0003624. [Google Scholar]
  25. Lindh JM, Torr SJ, Vale GA, Lehane MJ, , 2009. Improving the cost-effectiveness of artificial visual baits for controlling the tsetse fly Glossina fuscipes fuscipes. PLoS Negl Trop Dis 3: e474. [Google Scholar]
  26. Arora AK, Douglas AE, , 2017. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J Insect Physiol 103: 1017. [Google Scholar]
  27. WHO, 2017. Human African trypanosomiasis. WHO Factsheets. Available at: http://www.who.int/mediacentre/factsheets/fs259/en/. Accessed May 2, 2017.
  28. Messina JP, Moore NJ, DeVisser MH, McCord PF, Walker ED, , 2012. Climate change and risk projection: dynamic spatial models of tsetse and African trypanosomiasis in Kenya. Ann Assoc Am Geogr 102: 10381048. [Google Scholar]
  29. Wolf T, Wichelhaus T, Göttig S, Kleine C, Brodt HR, Just-Nuebling G, , 2012. Trypanosoma brucei rhodesiense infection in a German traveller returning from the Masai Mara area, Kenya, January 2012. Euro Surveill 17: pii:20114. [Google Scholar]
  30. Ouma JO, Marquez JG, Krafsur ES, , 2005. Macrogeographic population structure of the tsetse fly, Glossina pallidipes (Diptera: Glossinidae). Bull Entomol Res 95: 437447. [Google Scholar]
  31. FAO, 2006. Tsetse Fly Habitat and Land Cover: An Analysis at Continental Level. Rome, Italy: GLCN, FAO, 116.
  32. Ouma JO, Krafsur ES, , 2010. The influence of temporal and seasonal changes on genetic diversity and population structure of the tsetse fly, Glossina pallidipes in Kenya. East African Agric Forum J 77: 5968. [Google Scholar]
  33. Williams B, Dransfield R, Brightwell R, , 1990. Monitoring tsetse fly populations. I. The intrinsic variability of trap catches of Glossina pallidipes at Nguruman, Kenya. Med Vet Entomol 4: 167179. [Google Scholar]
  34. Ouma JO, Marquez JG, Krafsur ES, , 2006. Microgeographical breeding structure of the tsetse fly, Glossina pallidipes in south-western Kenya. Med Vet Entomol 20: 138149. [Google Scholar]
  35. Swai ES, Kaaya JE, , 2012. A parasitological survey for bovine trypanosomosis in the livestock/wildlife ecozone of northern Tanzania. Vet World 5: 459464. [Google Scholar]
  36. Hyseni C, Kato AB, Okedi LM, Masembe C, Ouma JO, Aksoy S, Caccone A, , 2012. The population structure of Glossina fuscipes fuscipes in the Lake Victoria basin in Uganda: implications for vector control. Parasit Vectors 5: 222. [Google Scholar]
  37. Echodu R, Sistrom M, Hyseni C, Enyaru J, Okedi L, Aksoy S, Caccone A, , 2013. Genetically distinct Glossina fuscipes fuscipes populations in the Lake Kyoga region of Uganda and its relevance for human African trypanosomiasis. BioMed Res Int 2013: 614721. [Google Scholar]
  38. Ouma JO, Beadell JS, Hyseni C, Okedi LM, Krafsur ES, Aksoy S, Caccone A, , 2011. Genetic diversity and population structure of Glossina pallidipes in Uganda and western Kenya. Parasit Vectors 4: 122. [Google Scholar]
  39. Krafsur ES, , 2002. Population structure of the tsetse fly Glossina pallidipes estimated by allozyme, microsatellite and mitochondrial gene diversities. Insect Mol Biol 11: 3745. [Google Scholar]
  40. Solano P, Ravel S, de Meeus T, , 2010. How can tsetse population genetics contribute to African trypanosomiasis control? Trends Parasitol 26: 255263. [Google Scholar]
  41. Solano P, 2010. Population genetics as a tool to select tsetse control strategies: suppression or eradication of Glossina palpalis gambiensis in the Niayes of Senegal. PLoS Negl Trop Dis 4: e692. [Google Scholar]
  42. Okeyo WA, 2017. Temporal genetic differentiation in Glossina pallidipes tsetse fly populations in Kenya. Parasit Vectors 10: 471. [Google Scholar]
  43. Dransfield RD, Brightwell R, Kiilu J, Chaudhury MF, Abie DAAD, , 1989. Size and mortality rates of Glossina pallidipes in the semi‐arid zone of southwestern Kenya. Med Vet Entomol 3: 8395. [Google Scholar]
  44. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, , 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535538. [Google Scholar]
  45. Brookfield JF, , 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5: 453455. [Google Scholar]
  46. Rousset F, , 2008. genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103106. [Google Scholar]
  47. Benjamini Y, Hochberg Y, , 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289300. [Google Scholar]
  48. Goudet J, , 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at: https://www2.unil.ch/popgen/softwares/fstat.htm. Accessed February 22, 2017.
  49. Excoffier L, Lischer HE, , 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564567. [Google Scholar]
  50. Kalinowski ST, Wagner AP, Taper ML, , 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6: 576579. [Google Scholar]
  51. Evanno G, Regnaut S, Goudet J, , 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 26112620. [Google Scholar]
  52. Earl DA, vonHoldt BM, , 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359361. [Google Scholar]
  53. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I, , 2015. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15: 11791191. [Google Scholar]
  54. Jombart T, Devillard S, Balloux F, , 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11: 94. [Google Scholar]
  55. Jombart T, , 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 14031405. [Google Scholar]
  56. R Core Team, 2011. R: A Language And Environment For Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/. Accessed February 14, 2017. [Google Scholar]
  57. Jombart T, Collins C, , 2015. A Tutorial for Discriminant Analysis of Principal Components (DAPC) Using Adegenet 2.0.0. London, United Kingdom: Imperial College London, MRC Centre for Outbreak Analysis and Modelling, 143. [Google Scholar]
  58. Wright S, , 1951. The genetical structure of populations. Ann Eugen 15: 323354. [Google Scholar]
  59. Weir BS, Cockerham CC, , 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 13581370. [Google Scholar]
  60. Jensen JL, Bohonak AJ, Kelley ST, , 2005. Isolation by distance, web service. BMC Genet 6: 13. [Google Scholar]
  61. Smouse PE, Long JC, Sokal RR, , 1986. Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35: 627632. [Google Scholar]
  62. Ersts PJ, , 2011. Geographic Distance Matrix Generator (Version 1.2. 3). New York City, NY: American Museum of Natural History. [Google Scholar]
  63. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A, , 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95: 536539. [Google Scholar]
  64. Duchesne P, Turgeon J, , 2009. FLOCK: a method for quick mapping of admixture without source samples. Mol Ecol Resour 9: 13331344. [Google Scholar]
  65. Paetkau D, Slade R, Burden M, Estoup A, , 2004. Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13: 5565. [Google Scholar]
  66. Rannala B, Mountain JL, , 1997. Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94: 91979201. [Google Scholar]
  67. DeVisser MH, Messina JP, , 2009. Optimum land cover products for use in a Glossina-morsitans habitat model of Kenya. Int J Health Geogr 8: 39. [Google Scholar]
  68. Osano PM, Said MY, deLeeuw J, Moiko SS, OleKaelo D, Schomers S, Birner R, Ogutu JO, , 2013. Pastoralism and ecosystem-based adaptation in Kenyan Masailand. Int J Clim Chang Strateg Manag 5: 198214. [Google Scholar]
  69. Wamwiri FN, Changasi RE, , 2016. Tsetse flies (Glossina) as vectors of human African trypanosomiasis: a review. Biomed Res Int 2016: 8. [Google Scholar]
  70. Zhivotovsky LA, , 2015. Relationships between Wright’s FST and FIS statistics in a context of Wahlund effect. J Hered 106: 306309. [Google Scholar]
  71. Alam U, 2012. Implications of microfauna-host interactions for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda. Appl Environ Microbiol 78: 46274637. [Google Scholar]
  72. Krafsur ES, Wohlford DL, , 1999. Breeding structure of Glossina pallidipes populations evaluated by mitochondrial variation. J Hered 90: 635642. [Google Scholar]
  73. Ruiz Guajardo JC, Schnabel A, Ennos R, Preuss S, Otero-Arnaiz A, Stone G, , 2010. Landscape genetics of the key African acacia species Senegalia mellifera (Vahl)—the importance of the Kenyan Rift Valley. Mol Ecol 19: 51265139. [Google Scholar]
  74. Bertola LD, 2011. Genetic diversity, evolutionary history and implications for conservation of the lion (Panthera leo) in west and central Africa. J Biogeography 38: 13561367. [Google Scholar]
  75. Brown DM, Brenneman RA, Koepfli KP, Pollinger JP, Milá B, Georgiadis NJ, Louis EE, Jr. Grether GF, Jacobs DK, Wayne RK, , 2007. Extensive population genetic structure in the giraffe. BMC Biol 5: 57. [Google Scholar]
  76. Dubach J, Patterson BD, Briggs MB, Venzke K, Flamand J, Stander P, Scheepers L, Kays RW, , 2005. Molecular genetic variation across the southern and eastern geographic ranges of the African lion, Panthera leo. Conserv Genet Resour 6: 1524. [Google Scholar]
  77. Evans BJ, Bliss SM, Mendel SA, Tinsley RC, , 2011. The Rift Valley is a major barrier to dispersal of African clawed frogs (Xenopus) in Ethiopia. Mol Ecol 20: 42164230. [Google Scholar]
  78. Franco JR, Simarro PP, Diarra A, Jannin JG, , 2005. Epidemiology of human African trypanosomiasis. Clin Epidemiol 6: 257275. [Google Scholar]
  79. Lehmann T, Hawley WA, Grebert H, Danga M, Atieli F, Collins FH, , 1999. The Rift Valley complex as a barrier to gene flow for Anopheles gambiae in Kenya. J Hered 90: 613621. [Google Scholar]
  80. Lehmann T, Licht M, Elissa N, Maega BTA, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA, , 2003. Population structure of Anopheles gambiae in Africa. J Hered 94: 133147. [Google Scholar]
  81. Cano J, Descalzo MÁ, Ndong-mabale N, Ndong-asumu P, Bobuakasi L, Nzambo-ondo S, Benito A, Roche J, , 2007. Predicted distribution and movement of Glossina palpalis palpalis (Diptera: Glossinidae) in the wet and dry seasons in the Kogo trypanosomiasis focus (Equatorial Guinea). J Vector Ecol 32: 218225. [Google Scholar]
  82. Wint W, Rogers D, , 2000. Predicted Distributions of Tsetse in Africa. Oxford, United Kingdom: FAO Consultants’ Report, ERGO Ltd and the TALA Research Group. [Google Scholar]

Data & Media loading...

Supplemental appendices

  • Received : 20 Feb 2018
  • Accepted : 15 Jun 2018
  • Published online : 13 Aug 2018

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error