Buguet A, Mpanzou G, Bentivoglio M, 2014. Human african trypanosomiasis: a highly neglected neurological disease. Bentivoglio M, Cavalheiro E, Kristensson K, Patel N, eds. Neglected Tropical Diseases and Conditions of the Nervous System. New York, NY: Springer, 165–181.
Courtin F et al. 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.
Alsan M, 2015. The effect of the tsetse fly on African development. Am Econ Rev 105: 382–410.
Fèvre EM, Wissmann BV, Welburn SC, Lutumba P, 2008. The burden of human African trypanosomiasis. PLoS Negl Trop Dis 2: e333.
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.
La Greca F, Magez S, 2011. Vaccination against trypanosomiasis. Hum Vaccin 7: 1225–1233.
Aksoy S, 2003. Control of tsetse flies and trypanosomes using molecular genetics. Vet Parasitol 115: 125–145.
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.
Anene BM, Onah DN, Nawa Y, 2001. Drug resistance in pathogenic African trypanosomes: what hopes for the future? Vet Parasitol 96: 83–100.
Wilkinson SR, Kelly JM, 2009. Trypanocidal drugs: mechanisms, resistance and new targets. Expert Rev Mol Med 11: e31.
Barrett MP, Vincent IM, Burchmore RJ, Kazibwe AJ, Matovu E, 2011. Drug resistance in human African trypanosomiasis. Future Microbiol 6: 1037–1047.
Welburn SC, Molyneux DH, Maudlin I, 2016. Beyond tsetse—implications for research and control of human African trypanosomiasis epidemics. Trends Parasitol 32: 230–241.
Aksoy S, Caccone A, Galvani AP, Okedi LM, 2013. Glossina fuscipes populations provide insights for human African trypanosomiasis transmission in Uganda. Trends Parasitol 29: 394–406.
Brightwell R, Dransfield R, 1997. Odour attractants for tsetse: Glossina austeni, G. brevipalpis and G. swynnertoni. Med Vet Entomol 11: 297–299.
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 265–276.
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: 239–253.
Maudlin I, 2006. African trypanosomiasis. Ann Trop Med Parasitol 100: 679–701.
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: 99–107.
Schofield CJ, Kabayo JP, 2008. Trypanosomiasis vector control in Africa and Latin America. Parasit Vectors 1: 24.
Torr SJ, Hargrove JW, Vale GA, 2005. Towards a rational policy for dealing with tsetse. Trends Parasitol 21: 537–541.
Vreysen MJ, 2001. Principles of area-wide integrated tsetse fly control using the sterile insect technique. Med Trop (Mars) 61: 397–411.
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): 119–125.
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.
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.
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.
Arora AK, Douglas AE, 2017. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J Insect Physiol 103: 10–17.
WHO, 2017. Human African trypanosomiasis. WHO Factsheets. Available at: http://www.who.int/mediacentre/factsheets/fs259/en/. Accessed May 2, 2017.
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: 1038–1048.
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.
Ouma JO, Marquez JG, Krafsur ES, 2005. Macrogeographic population structure of the tsetse fly, Glossina pallidipes (Diptera: Glossinidae). Bull Entomol Res 95: 437–447.
FAO, 2006. Tsetse Fly Habitat and Land Cover: An Analysis at Continental Level. Rome, Italy: GLCN, FAO, 1–16.
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: 59–68.
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: 167–179.
Ouma JO, Marquez JG, Krafsur ES, 2006. Microgeographical breeding structure of the tsetse fly, Glossina pallidipes in south-western Kenya. Med Vet Entomol 20: 138–149.
Swai ES, Kaaya JE, 2012. A parasitological survey for bovine trypanosomosis in the livestock/wildlife ecozone of northern Tanzania. Vet World 5: 459–464.
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.
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.
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.
Krafsur ES, 2002. Population structure of the tsetse fly Glossina pallidipes estimated by allozyme, microsatellite and mitochondrial gene diversities. Insect Mol Biol 11: 37–45.
Solano P, Ravel S, de Meeus T, 2010. How can tsetse population genetics contribute to African trypanosomiasis control? Trends Parasitol 26: 255–263.
Solano P et al. 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.
Okeyo WA et al. 2017. Temporal genetic differentiation in Glossina pallidipes tsetse fly populations in Kenya. Parasit Vectors 10: 471.
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: 83–95.
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: 535–538.
Brookfield JF, 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5: 453–455.
Rousset F, 2008. genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103–106.
Benjamini Y, Hochberg Y, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289–300.
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.
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: 564–567.
Kalinowski ST, Wagner AP, Taper ML, 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6: 576–579.
Evanno G, Regnaut S, Goudet J, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620.
Earl DA, vonHoldt BM, 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359–361.
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: 1179–1191.
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.
Jombart T, 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.
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.
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, 1–43.
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The tsetse fly Glossina pallidipes, 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 G. pallidipes 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 G. pallidipes 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 FST = 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 FST; 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 G. pallidipes in Kenya, and that vector control efforts should include some region-specific strategies to effectively control this disease vector.
Financial support: NIH Grant no. U01 AI115648; NIH-Fogarty Global Infectious Diseases Training Grant (D43TW007391).
Authors’ addresses: Winnie A. Okeyo, Department of Biomedical Sciences and Technology, School of Public Health and Community Development, Maseno University, Kisumu, Kenya, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, Nairobi, Kenya, and Yale School of Public Health, Yale University, New Haven, CT, E-mail: okeyo.winnie@gmail.com. Norah P. Saarman, Kirstin Dion, Michael Mengual, and Adalgisa Caccone, Department of Ecology & Evolutionary Biology, Yale University, New Haven, CT, E-mails: norah.saarman@yale.edu, kirstin.dion@yale.edu, michael.mengual@yale.edu, and adalgisa.caccone@yale.edu. Rosemary Bateta, Sylvance Okoth, and Grace Murilla, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, Nairobi, Kenya, E-mails: batetarw@yahoo.com, sokotho@gmail.com, and gmurilla@yahoo.co.uk. Paul O. Mireji, Biotechnology Research Institute, Kenya Agricultural and Livestock Research Organization, Nairobi, Kenya, and Yale School of Public Health, Yale University, New Haven, CT, E-mail: mireji.paul@gmail.com. Collins Ouma, School of Public Health and Community Development, Maseno University, Kisumu, Kenya, E-mail: profcollinsouma@gmail.com. Serap Aksoy, Yale School of Public Health, Yale University, New Haven, CT, E-mail: serap.aksoy@yale.edu.
These authors contributed equally to this work.
Buguet A, Mpanzou G, Bentivoglio M, 2014. Human african trypanosomiasis: a highly neglected neurological disease. Bentivoglio M, Cavalheiro E, Kristensson K, Patel N, eds. Neglected Tropical Diseases and Conditions of the Nervous System. New York, NY: Springer, 165–181.
Courtin F et al. 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.
Alsan M, 2015. The effect of the tsetse fly on African development. Am Econ Rev 105: 382–410.
Fèvre EM, Wissmann BV, Welburn SC, Lutumba P, 2008. The burden of human African trypanosomiasis. PLoS Negl Trop Dis 2: e333.
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.
La Greca F, Magez S, 2011. Vaccination against trypanosomiasis. Hum Vaccin 7: 1225–1233.
Aksoy S, 2003. Control of tsetse flies and trypanosomes using molecular genetics. Vet Parasitol 115: 125–145.
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.
Anene BM, Onah DN, Nawa Y, 2001. Drug resistance in pathogenic African trypanosomes: what hopes for the future? Vet Parasitol 96: 83–100.
Wilkinson SR, Kelly JM, 2009. Trypanocidal drugs: mechanisms, resistance and new targets. Expert Rev Mol Med 11: e31.
Barrett MP, Vincent IM, Burchmore RJ, Kazibwe AJ, Matovu E, 2011. Drug resistance in human African trypanosomiasis. Future Microbiol 6: 1037–1047.
Welburn SC, Molyneux DH, Maudlin I, 2016. Beyond tsetse—implications for research and control of human African trypanosomiasis epidemics. Trends Parasitol 32: 230–241.
Aksoy S, Caccone A, Galvani AP, Okedi LM, 2013. Glossina fuscipes populations provide insights for human African trypanosomiasis transmission in Uganda. Trends Parasitol 29: 394–406.
Brightwell R, Dransfield R, 1997. Odour attractants for tsetse: Glossina austeni, G. brevipalpis and G. swynnertoni. Med Vet Entomol 11: 297–299.
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 265–276.
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: 239–253.
Maudlin I, 2006. African trypanosomiasis. Ann Trop Med Parasitol 100: 679–701.
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: 99–107.
Schofield CJ, Kabayo JP, 2008. Trypanosomiasis vector control in Africa and Latin America. Parasit Vectors 1: 24.
Torr SJ, Hargrove JW, Vale GA, 2005. Towards a rational policy for dealing with tsetse. Trends Parasitol 21: 537–541.
Vreysen MJ, 2001. Principles of area-wide integrated tsetse fly control using the sterile insect technique. Med Trop (Mars) 61: 397–411.
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): 119–125.
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.
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.
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.
Arora AK, Douglas AE, 2017. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J Insect Physiol 103: 10–17.
WHO, 2017. Human African trypanosomiasis. WHO Factsheets. Available at: http://www.who.int/mediacentre/factsheets/fs259/en/. Accessed May 2, 2017.
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: 1038–1048.
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.
Ouma JO, Marquez JG, Krafsur ES, 2005. Macrogeographic population structure of the tsetse fly, Glossina pallidipes (Diptera: Glossinidae). Bull Entomol Res 95: 437–447.
FAO, 2006. Tsetse Fly Habitat and Land Cover: An Analysis at Continental Level. Rome, Italy: GLCN, FAO, 1–16.
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: 59–68.
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: 167–179.
Ouma JO, Marquez JG, Krafsur ES, 2006. Microgeographical breeding structure of the tsetse fly, Glossina pallidipes in south-western Kenya. Med Vet Entomol 20: 138–149.
Swai ES, Kaaya JE, 2012. A parasitological survey for bovine trypanosomosis in the livestock/wildlife ecozone of northern Tanzania. Vet World 5: 459–464.
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.
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.
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.
Krafsur ES, 2002. Population structure of the tsetse fly Glossina pallidipes estimated by allozyme, microsatellite and mitochondrial gene diversities. Insect Mol Biol 11: 37–45.
Solano P, Ravel S, de Meeus T, 2010. How can tsetse population genetics contribute to African trypanosomiasis control? Trends Parasitol 26: 255–263.
Solano P et al. 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.
Okeyo WA et al. 2017. Temporal genetic differentiation in Glossina pallidipes tsetse fly populations in Kenya. Parasit Vectors 10: 471.
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: 83–95.
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: 535–538.
Brookfield JF, 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5: 453–455.
Rousset F, 2008. genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103–106.
Benjamini Y, Hochberg Y, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289–300.
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.
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: 564–567.
Kalinowski ST, Wagner AP, Taper ML, 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6: 576–579.
Evanno G, Regnaut S, Goudet J, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620.
Earl DA, vonHoldt BM, 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359–361.
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: 1179–1191.
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.
Jombart T, 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.
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.
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