Section: Zoology
Topic: Genetics/Genomics, Population biology

Population genetics of Glossina fuscipes fuscipes from southern Chad

Ravel, Sophie1 ; Mahamat, Mahamat Hissène2; Ségard, Adeline1 ; Argilés-Herrero, Rafael3 ; Bouyer, Jérémy3 ; Rayaisse, Jean-Baptiste4 ; Solano, Philippe1 ; Guihini Mollo, Brahim2; Pèka, Mallaye5; Darnas, Justin5; Belem, Adrien Marie Gaston6 ; Yoni, Wilfrid4 ; Noûs, Camille7; De Meeûs, Thierry1  
1 Intertryp, IRD, Cirad, Univ Montpellier, Montpellier, France
2 Institut de Recherche en Elevage pour le Développement (IRED), Ndjaména, Tchad
3 Insect Pest Control Laboratory, Joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency Program of Nuclear Techniques in Food and Agriculture, A-1400, Vienna, Austria
4 Centre International de Recherche Développement sur l’Elevage en zone Subhumide (Cirdes), Bobo-Dioulasso, Burkina Faso
5 Programme National de Lutte contre la THA (PNLTHA), Ndjaména, Tchad
6 Université Nazi Boni, Bobo-Dioulasso, Burkina Faso
7 Cogitamus laboratory, France, https://www.cogitamus.fr/

Corresponding author(s): De Meeûs, Thierry (thierry.demeeus@ird.fr)

10.24072/pcjournal.257 - Peer Community Journal, Volume 3 (2023), article no. e31.

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In Subsaharan Africa, tsetse flies (genus Glossina) are vectors of trypanosomes causing Human African Trypanosomiasis (HAT) and Animal African Trypanosomosis (AAT). Some foci of HAT persist in Southern Chad, where a program of tsetse control was started against the local vector Glossina fuscipes fuscipes in the Mandoul focus in 2014, and in Maro in 2018. Flies were also sampled in 2018 in Timbéri and Dokoutou. We analyzed the population genetics of G. fuscipes fuscipes from the four tsetse-infested zones. The trapping samples were characterized by a strong female biased sex-ratio, except in Timbéri and Dokoutou that had high tsetse densities. Apparent density and effective population density appeared smaller in the main foci of Mandoul and Maro and the average dispersal distance (within the spatial scale of each zone) was as large as or larger than the total length of each respective zone. The genetic signature of a population bottleneck was found in the Mandoul and Timbéri area, suggesting a large ancient interconnected metapopulation that underwent genetic subdivision into small, isolated pockets due to adverse environmental conditions. The long-range dispersal and the existence of genetic outliers suggest a possibility of migration from remote sites such as the Central African Republic in the south (although the fly situation remains unknown there) and/or a genetic signature of recent exchanges. Due to likely isolation, an eradication strategy may be considered for sustainable HAT control in Mandoul focus. Another strategy will probably be required in Maro focus, which probably experiences much more exchanges with its neighbors.

Published online:
DOI: 10.24072/pcjournal.257
Type: Research article
Mots-clés : Tsetse flies, Dispersal, Trypanosomosis, Control, Polulation subdivision, Isolation by distance

Ravel, Sophie 1; Mahamat, Mahamat Hissène 2; Ségard, Adeline 1; Argilés-Herrero, Rafael 3; Bouyer, Jérémy 3; Rayaisse, Jean-Baptiste 4; Solano, Philippe 1; Guihini Mollo, Brahim 2; Pèka, Mallaye 5; Darnas, Justin 5; Belem, Adrien Marie Gaston 6; Yoni, Wilfrid 4; Noûs, Camille 7; De Meeûs, Thierry 1

1 Intertryp, IRD, Cirad, Univ Montpellier, Montpellier, France
2 Institut de Recherche en Elevage pour le Développement (IRED), Ndjaména, Tchad
3 Insect Pest Control Laboratory, Joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency Program of Nuclear Techniques in Food and Agriculture, A-1400, Vienna, Austria
4 Centre International de Recherche Développement sur l’Elevage en zone Subhumide (Cirdes), Bobo-Dioulasso, Burkina Faso
5 Programme National de Lutte contre la THA (PNLTHA), Ndjaména, Tchad
6 Université Nazi Boni, Bobo-Dioulasso, Burkina Faso
7 Cogitamus laboratory, France, https://www.cogitamus.fr/
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_257,
     author = {Ravel, Sophie and Mahamat, Mahamat Hiss\`ene and S\'egard, Adeline and Argil\'es-Herrero, Rafael and Bouyer, J\'er\'emy and Rayaisse, Jean-Baptiste and Solano, Philippe and Guihini Mollo, Brahim and  P\`eka, Mallaye and Darnas, Justin and Belem, Adrien Marie Gaston and Yoni, Wilfrid and No\^us, Camille and De Mee\^us, Thierry},
     title = {Population genetics of {\protect\emph{Glossina} fuscipes fuscipes} from southern {Chad}},
     journal = {Peer Community Journal},
     eid = {e31},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.257},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.257/}
}
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AU  - Mahamat, Mahamat Hissène
AU  - Ségard, Adeline
AU  - Argilés-Herrero, Rafael
AU  - Bouyer, Jérémy
AU  - Rayaisse, Jean-Baptiste
AU  - Solano, Philippe
AU  - Guihini Mollo, Brahim
AU  -  Pèka, Mallaye
AU  - Darnas, Justin
AU  - Belem, Adrien Marie Gaston
AU  - Yoni, Wilfrid
AU  - Noûs, Camille
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%A Ségard, Adeline
%A Argilés-Herrero, Rafael
%A Bouyer, Jérémy
%A Rayaisse, Jean-Baptiste
%A Solano, Philippe
%A Guihini Mollo, Brahim
%A  Pèka, Mallaye
%A Darnas, Justin
%A Belem, Adrien Marie Gaston
%A Yoni, Wilfrid
%A Noûs, Camille
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Ravel, Sophie; Mahamat, Mahamat Hissène; Ségard, Adeline; Argilés-Herrero, Rafael; Bouyer, Jérémy; Rayaisse, Jean-Baptiste; Solano, Philippe; Guihini Mollo, Brahim;  Pèka, Mallaye; Darnas, Justin; Belem, Adrien Marie Gaston; Yoni, Wilfrid; Noûs, Camille; De Meeûs, Thierry. Population genetics of Glossina fuscipes fuscipes from southern Chad. Peer Community Journal, Volume 3 (2023), article  no. e31. doi : 10.24072/pcjournal.257. https://peercommunityjournal.org/articles/10.24072/pcjournal.257/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.zool.100127

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Balloux, F. Heterozygote excess in small populations and the heterozygote-excess effective population size, Evolution, Volume 58, 2004 no. 9, p. 1891-900 | DOI

[2] Belkhir, K.; Borsa, P.; Chikhi, L.; Raufaste, N.; Bonhomme, F. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France), 2004 (https://kimura.univ-montp2.fr/genetix/)

[3] Benjamini, Y.; Yekutieli, D. The control of the false discovery rate in multiple testing under dependency, The Annals of Statistics, Volume 29 (2001) no. 4, pp. 1165-1188 | DOI

[4] Bouyer, J.; Desquesnes, M.; Yoni, W.; Chamisa, A.; Guerrini, L. Attracting and trapping insect vectors, Attracting and trapping insect vectors, 2015 (https://agritrop.cirad.fr/575786/1/document_575786.pdf)

[5] Bouyer, J.; Solano, P.; de la Rocque, S.; Desquesnes, M.; Cuisance, D.; Itard, J.; Frézil, J.-L.; Authié, É. Infectious and Parasitic Diseases of Livestock (2009), pp. 1936-1943

[6] Brookfield, J. F. Y. A simple new method for estimating null allele frequency from heterozygote deficiency, Molecular Ecology, Volume 5 (1996) no. 3, pp. 453-455 | DOI

[7] Büscher, P.; Bart, J. M.; Boelaert, M.; Bucheton, B.; Cecchi, G.; Chitnis, N.; Courtin, D.; Figueiredo, L. M.; Franco, J. R.; Grébaut, P.; Hasker, E.; Ilboudo, H.; Jamonneau, V.; Koffi, M.; Lejon, V.; MacLeod, A.; Masumu, J.; Matovu, E.; Mattioli, R.; Noyes, H.; Picado, A.; Rock, K. S.; Rotureau, B.; Simo, G.; Thévenon, S.; Trindade, S.; Truc, P.; Van Reet, N. Do cryptic reservoirs threaten gambiense-sleeping sickness elimination?, Trends in Parasitology, Volume 34 (2018) no. 3, pp. 197-207 | DOI

[8] Cavalli-Sforza, L.; Edwards, A. Phylogenetic analysis: model and estimation procedures, American Journal of Human Genetics, Volume 19 (1967), pp. 233-257 | DOI

[9] Challier, A.; Laveissière, C. Un nouveau piège pour la capture des glossines (Glossina: Diptera, Muscidae): description et assais sur le terrain, Cahier de l'ORSTOM, Série Entomologie Médicale et Parasitologie, Volume 11 (1973) no. 4, pp. 251-262 (http://www.sleeping-sickness.ird.fr/pdf/19003.pdf)

[10] Chapuis, M. P.; Estoup, A. Microsatellite null alleles and estimation of population differentiation, Molecular Biology and Evolution, Volume 24 (2007) no. 3, pp. 621-631 | DOI

[11] Coombs, J. .. A.; Letcher, B. .. H.; Nislow, K. .. H. CREATE: A software to create input files from diploid genotypic data for 52 genetic software programs, Molecular Ecology Resources, Volume 8 (2008), pp. 578-580 | DOI

[12] Cornuet, J. M.; Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data, Genetics, Volume 144 (1996) no. 4, pp. 2001-2014 | DOI

[13] Cuisance, D. Réactualisation de la situation des tsé-tsés et des trypanosomoses animales au Tchad. Enquète réalisée du 9 février au 18 mars 1995, Maisons-Alfort : CIRAD-EMVT, Maison-Alfort, 1995, p. 161

[14] Cuisance, D.; Février, J.; Déjardin, J.; Filledier, J. Dispersion linéaire de Glossina palpalis gambiensis et G. tachinoides dans une galerie forestière en zone soudano-guinéenne (Burkina Faso), Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux, Volume 38 (1985), pp. 153-172 | DOI

[15] De Meeûs, T. Initiation à la génétique des populations naturelles: Applications aux parasites et à leurs vecteurs, Didactiques, IRD Editions, Marseille, 2012, p. 356

[16] De Meeûs, T. Statistical decision from k test series with particular focus on population genetics tools: a DIY notice, Infection Genetics and Evolution, Volume 22 (2014), pp. 91-93 | DOI

[17] De Meeûs, T. Revisiting FIS, FST, Wahlund effects, and null alleles, Journal of Heredity, Volume 109 (2018) no. 4, pp. 446-456 | DOI

[18] De Meeûs, T.; Chan, C. T.; Ludwig, J. M.; Tsao, J. I.; Patel, J.; Bhagatwala, J.; Beati, L. Deceptive combined effects of short allele dominance and stuttering: an example with Ixodes scapularis, the main vector of Lyme disease in the U.S.A., Peer Community Journal, Volume 1 (2021), p. e40 | DOI

[19] De Meeûs, T.; Goudet, J. A step-by-step tutorial to use HierFstat to analyse populations hierarchically structured at multiple levels, Infection Genetics and Evolution, Volume 7 (2007) no. 6, pp. 731-735 | DOI

[20] De Meeûs, T.; Guégan, J. F.; Teriokhin, A. T. MultiTest V.1.2, a program to binomially combine independent tests and performance comparison with other related methods on proportional data, BMC Bioinformatics, Volume 10 (2009) no. 1, p. 443 | DOI

[21] De Meeûs, T.; Humair, P. F.; Grunau, C.; Delaye, C.; Renaud, F. Non-Mendelian transmission of alleles at microsatellite loci: an example in Ixodes ricinus, the vector of Lyme disease, International Journal for Parasitology, Volume 34 (2004) no. 8, pp. 943-950 | DOI

[22] De Meeûs, T.; Koffi, B. B.; Barré, N.; de Garine-Wichatitsky, M.; Chevillon, C. Swift sympatric adaptation of a species of cattle tick to a new deer host in New-Caledonia, Infection Genetics and Evolution, Volume 10 (2010) no. 7, pp. 976-983 | DOI

[23] De Meeûs, T.; McCoy, K. D.; Prugnolle, F.; Chevillon, C.; Durand, P.; Hurtrez-Boussès, S.; Renaud, F. Population genetics and molecular epidemiology or how to "débusquer la bête", Infection Genetics and Evolution, Volume 7 (2007) no. 2, pp. 308-332 | DOI

[24] De Meeûs, T.; Ravel, S.; Solano, P.; Bouyer, J. Negative density-dependent dispersal in tsetse flies: a risk for control campaigns?, Trends in Parasitology, Volume 35 (2019) no. 8, pp. 615-621 | DOI

[25] Do, C.; Waples, R. S.; Peel, D.; Macbeth, G. M.; Tillett, B. J.; Ovenden, J. R. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data, Molecular Ecology Resources, Volume 14 (2014) no. 1, pp. 209-214 | DOI

[26] Fox, J. The R commander: a basic statistics graphical user interface to R, Journal of Statistical Software, Volume 14 (2005) no. 9, pp. 1-42 | DOI

[27] Fox, J. Extending the R commander by "plugin" packages, R News (R News), Volume 7, 2007 no. 3, pp. 46-52 (https://stat.ethz.ch/pipermail/r-help/attachments/20071101/3603125e/attachment.pdf)

[28] Frontier, S. Etude de la décroissance des valeurs propres dans une analyse en composantes principales: comparaison avec le modèle du bâton brisé, Journal of Experimental Marine Biology and Ecology, Volume 25 (1976), pp. 67-75 (https://horizon.documentation.ird.fr/exl-doc/pleins_textes/pleins_textes_5/b_fdi_06-07/08515.pdf)

[29] Gimonneau, G.; Ouedraogo, R.; Salou, E.; Rayaisse, J.-B.; Buatois, B.; Solano, P.; Dormont, L.; Roux, O.; Bouyer, J. Larviposition site selection mediated by volatile semiochemicals in Glossina palpalis gambiensis, Ecological Entomology, Volume 46 (2021), pp. 301-309 | DOI

[30] Goudet, J. FSTAT (Version 1.2): A computer program to calculate F-statistics, Journal of Heredity, Volume 86 (1995) no. 6, pp. 485-486 | DOI

[31] Goudet, J. Fstat (ver. 2.9.4), a program to estimate and test population genetics parameters. Updated from Goudet (1995) (2003) (http://www.t-de-meeus.fr/Programs/Fstat294.zip)

[32] Goudet, J. HIERFSTAT, a package for R to compute and test hierarchical F-statistics, Molecular Ecology Notes, Volume 5 (2005) no. 1, pp. 184-186 | DOI

[33] Goudet, J.; Perrin, N.; Waser, P. Tests for sex-biased dispersal using bi-parentally inherited genetic markers, Molecular Ecology, Volume 11 (2002), p. 1103 | DOI

[34] Goudet, J.; Raymond, M.; De Meeûs, T.; Rousset, F. Testing differentiation in diploid populations, Genetics, Volume 144 (1996) no. 4, pp. 1933-1940 | DOI

[35] Gruvel, J. Les glossines vectrices des trpanosomiases au Tchad, Revue d’élevage et de médecine vétérinaire des pays tropicaux, Volume 19 (1966) no. 2, pp. 169-212 | DOI

[36] Guinand, B. Use of a multivariate model using allele frequency distributions to analyse patterns of genetic differentiation among populations, Biological Journal of the Linnean Society, Volume 58 (1996) no. 2, pp. 173-195 | DOI

[37] Hargrove, J. W.; Vale, G. A. Aspects of the feasibility of employing odor-baited traps for controlling tsetse flies (Diptera, Glossinidae), Bulletin of Entomological Research, Volume 69 (1979) no. 2, pp. 283-290 | DOI

[38] Hedrick, P. W. Genetics of populations (Third Edition), Jones and Bartlett Publishers, Sudbury, Massachusetts (2005), p. 737

[39] Hedrick, P. W. A standardized genetic differentiation measure, Evolution, Volume 59 (2005) no. 8, pp. 1633-1638 | DOI

[40] Hijmans, R. J.; Williams, E.; Vennes, C. Package 'geosphere': Spherical Trigonometry. CRAN, pp. Spherical trigonometry for geographic applications. That is, compute distances and related measures for angular (longitude/latitude) locations, 2019 (https://cran.r-project.org/web/packages/geosphere/geosphere.pdf)

[41] Ibrahim, M. A. M.; Weber, J. S.; Ngomtcho, S. C. H.; Signaboubo, D.; Berger, P.; Hassane, H. M.; Kelm, S. Diversity of trypanosomes in humans and cattle in the HAT foci Mandoul and Maro, Southern Chad-A matter of concern for zoonotic potential?, Plos Neglected Tropical Diseases, Volume 15 (2021) no. 6, p. e0009323 | DOI

[42] Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers, Bioinformatics, Volume 24 (2008) no. 11, pp. 1403-1405 | DOI

[43] Jombart, T.; Devillard, S.; Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations, BMC Genetics, Volume 11 (2010) no. 1 | DOI

[44] Karney, C. F. F. Algorithms for geodesics, Journal of Geodesy, Volume 87 (2013) no. 1, pp. 43-55 | DOI

[45] Koné, N.; Bouyer, J.; Ravel, S.; Vreysen, M. J. B.; Domagni, K. T.; Causse, S.; Solano, P.; de Meeûs, T. Contrasting population structures of two vectors of african trypanosomoses in Burkina Faso: Consequences for control, PLoS Neglected Tropical Diseases, Volume 5 (2011) no. 6 | DOI

[46] Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets, Molecular Biology and Evolution, Volume 33 (2016) no. 7, pp. 1870-1874 | DOI

[47] Mahamat, M. H.; Peka, M.; Rayaisse, J.-B.; Rock, K. S.; Toko, M. A.; Darnas, J.; Brahim, G. M.; Alkatib, A. B.; Yoni, W.; Tirados, I.; Courtin, F.; Brand, S. P. C.; Nersy, C.; Alfaroukh, I. O.; Torr, S. J.; Lehane, M. J.; Solano, P. Adding tsetse control to medical activities contributes to decreasing transmission of sleeping sickness in the Mandoul focus (Chad), PLOS Neglected Tropical Diseases, Volume 11 (2017) no. 7 | DOI

[48] Manangwa, O.; De Meeûs, T.; Grébaut, P.; Segard, A.; Byamungu, M.; Ravel, S. Detecting Wahlund effects together with amplification problems : cryptic species, null alleles and short allele dominance in Glossina pallidipes populations from Tanzania, Molecular Ecology Resources, Volume 19 (2019) no. 3, pp. 757-772 | DOI

[49] Manly, B. J. F. Randomization and monte carlo methods in biology, Second Edition, Chapman Hall, London, 1997, p. 407

[50] Meirmans, P. Using the amova framework to estimate a standardized genetic differentiation measure, Evolution, Volume 60 (2006) no. 11, pp. 2399-2402 | DOI

[51] Meirmans, P. G.; Hedrick, P. W. Assessing population structure: FST and related measures, Molecular Ecology Resources, Volume 11 (2011) no. 1, pp. 5-18 | DOI

[52] Melachio, T. T. T.; Simo, G.; Ravel, S.; De Meeûs, T.; Causse, S.; Solano, P.; Lutumba, P.; Asonganyi, T.; Njiokou, F. Population genetics of Glossina palpalis palpalis from central African sleeping sickness foci, Parasites And Vectors, Volume 4 (2011) no. 1 | DOI

[53] Ndung’u, J. M.; Boulangé, A.; Picado, A.; Mugenyi, A.; Mortensen, A.; Hope, A.; Mollo, B. G.; Bucheton, B.; Wamboga, C.; Waiswa, C.; Kaba, D.; Matovu, E.; Courtin, F.; Garrod, G.; Gimonneau, G.; Bingham, G. V.; Hassane, H. M.; Tirados, I.; Saldanha, I.; Kabore, J.; Rayaisse, J.-B.; Bart, J.-M.; Lingley, J.; Esterhuizen, J.; Longbottom, J.; Pulford, J.; Kouakou, L.; Sanogo, L.; Cunningham, L.; Camara, M.; Koffi, M.; Stanton, M.; Lehane, M.; Kagbadouno, M. S.; Camara, O.; Bessell, P.; Mallaye, P.; Solano, P.; Selby, R.; Dunkley, S.; Torr, S.; Biéler, S.; Lejon, V.; Jamonneau, V.; Yoni, W.; Katz, Z. Trypa-NO! contributes to the elimination of gambiense human African trypanosomiasis by combining tsetse control with “screen, diagnose and treat” using innovative tools and strategies, PLOS Neglected Tropical Diseases, Volume 14 (2020) no. 11 | DOI

[54] Nomura, T. Estimation of effective number of breeders from molecular coancestry of single cohort sample, Evolutionary Applications, Volume 1 (2008), pp. 462-474 | DOI

[55] Pearson, K. Assortative mating in man: a cooperative study, Biometrika, Volume 2 (1903) no. 4, pp. 481-498 | DOI

[56] Peel, D.; Waples, R. S.; Macbeth, G. M.; Do, C.; Ovenden, J. R. Accounting for missing data in the estimation of contemporary genetic effective population size (Ne), Molecular Ecology Resources, Volume 13 (2012) no. 2, pp. 243-253 | DOI

[57] Piry, S.; Luikart, G.; Cornuet, J.-M. BOTTLENECK: A computer program for detecting recent reductions in the effective size using allele frequency data, Journal of Heredity, Volume 90 (1999) no. 4, pp. 502-503 | DOI

[58] Prugnolle, F.; de Meeus, T. Inferring sex-biased dispersal from population genetic tools: a review, Heredity, Volume 88 (2002) no. 3, pp. 161-165 | DOI

[59] Prugnolle, F.; De Meeus, T. Apparent high recombination rates in clonal parasitic organisms due to inappropriate sampling design, Heredity, Volume 104 (2010) no. 2, pp. 135-140 | DOI

[60] Ravel, S.; Rayaisse, J.-B.; Courtin, F.; Solano, P.; de Meeus, T. Genetic signature of a recent southern range shift in Glossina tachinoides in East Burkina Faso, Infection, Genetics and Evolution, Volume 18 (2013), pp. 309-314 | DOI

[61] Ravel, S.; Sere, M.; Manangwa, O.; Kagbadouno, M.; Mahamat, M. H.; Shereni, W.; Okeyo, W. A.; Argiles-Herrero, R.; De Meeûs, T. Developing and quality testing of microsatellite loci for four species of Glossina, Infection Genetics and Evolution, Volume 85 (2020), p. 104515 | DOI

[62] Ravel, S.; Mahamat, H. M.; Ségard, A.; Argilés-Herrero, R.; Bouyer, J.; Rayaisse, J.-B.; Solano, P.; Brahim, G. M.; Pèka, M.; Darnas, J.; Belem, A. M. F.; Yoni, W.; Noûs, C.; De Meeûs, T. Population genetics of Glossina fuscipes fuscipes from southern Chad [Dataset], Zenodo, 2021 | DOI

[63] R-Core-Team R: A language and environment for statistical computing, Version 3.6.3 (2020-02-29) ed. R foundation for statistical computing, Vienna, Austria, 2020 (http://www.R-project.org)

[64] Rousset, F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance, Genetics, Volume 145 (1997) no. 4, pp. 1219-1228 | DOI

[65] Rousset, F. GENEPOP ' 007: a complete re-implementation of the GENEPOP software for Windows and Linux, Molecular Ecology Resources, Volume 8 (2008) no. 1, pp. 103-106 | DOI

[66] Saitou, N.; Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees, Molecular Biology and Evolution, Volume 4 (1987) no. 4, pp. 406-425 | DOI

[67] Séré, M.; Thévenon, S.; Belem, A. M. G.; De Meeûs, T. Comparison of different genetic distances to test isolation by distance between populations, Heredity, Volume 119 (2017) no. 2, pp. 55-63 | DOI

[68] She, J. X.; Autem, M.; Kotulas, G.; Pasteur, N.; Bonhomme, F. Multivariate analysis of genetic exchanges between Solea aegyptiaca and Solea senegalensis (Teleosts, Soleidae), Biological Journal of the Linnean Society, Volume 32 (1987) no. 4, pp. 357-371 | DOI

[69] Signaboubo, D.; Payne, V. K.; Moussa, I. M. A.; Hassane, H. M.; Berger, P.; Kelm, S.; Simo, G. Diversity of tsetse flies and trypanosome species circulating in the area of Lake Iro in southeastern Chad, Parasites Vectors, Volume 14 (2021) no. 1, p. 293 | DOI

[70] Solano, P.; Ravel, S.; De Meeûs, T. How can tsetse population genetics contribute to african trypanosomiasis control?, Trends in Parasitology, Volume 26 (2010) no. 5, pp. 255-263 | DOI

[71] Takezaki, N.; Nei, M. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA, Genetics, Volume 144 (1996) no. 1, pp. 389-399 | DOI

[72] Teriokhin, A. T.; De Meeûs, T.; Guegan, J. F. On the power of some binomial modifications of the Bonferroni multiple test, Zhurnal Obshchei Biologii, Volume 68 (2007), pp. 332-340

[73] Thomas, F.; Renaud, F.; Derothe, J. M.; Lambert, A.; De Meeüs, T.; Cézilly, F. Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite, Oecologia, Volume 104 (1995) no. 2, pp. 259-264 | DOI

[74] Traynor, K. S.; Mondet, F.; de Miranda, J. R.; Techer, M.; Kowallik, V.; Oddie, M. A. Y.; Chantawannakul, P.; McAfee, A. Varroa destructor: a complex parasite, crippling honey bees worldwide, Trends in Parasitology, Volume 36 (2020) no. 7, pp. 592-606 | DOI

[75] Vale, G. A.; Hursey, B. S.; Hargrove, J. W.; Torr, S. J.; Allsopp, R. The use of small plots to study populations of tsetse (Diptera, Glossinidae): difficulties associated with population dispersal, Insect Science and Its Application, Volume 5 (1984) no. 5, pp. 403-410 | DOI

[76] Van Oosterhout, C.; Hutchinson, W. F.; Wills, D. P. M.; Shipley, P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data, Molecular Ecology Notes, Volume 4 (2004) no. 3, pp. 535-538 | DOI

[77] Vitalis, R. Estim 1.2-2: a computer program to infer population parameters from one- and two-locus gene identity probabilities, updated from Vitalis and Couvet (2001), Molecular Ecology Notes, Volume 1, 2002, pp. 354-356 (Available At: http://www.t-de-meeus.fr/ProgMeeusGB.html) | DOI

[78] Vitalis, R.; Couvet, D. ESTIM 1.0: a computer program to infer population parameters from one- and two-locus gene identity probabilities, Molecular Ecology Notes, Volume 1 (2001a) no. 4, pp. 354-356 | DOI

[79] Vitalis, R.; Couvet, D. Estimation of effective population size and migration rate from one- and two-locus identity measures, Genetics, Volume 157 (2001b) no. 2, pp. 911-925 | DOI

[80] Vreysen, M. J. B.; Balenghien, T.; Saleh, K. M.; Maiga, S.; Koudougou, Z.; Cecchi, G.; Bouyer, J. Release-Recapture Studies Confirm Dispersal of Glossina palpalis gambiensis between River Basins in Mali, Plos Neglected Tropical Diseases, Volume 7 (2013) no. 4, p. e2022 | DOI

[81] Wahlund, S. Zusammensetzung von populationen und korrelationsers-chinungen von standpunkt der vererbungslehre aus betrachtet, Hereditas, Volume 11 (1928), pp. 65-106 | DOI

[82] Wang, J. Does GST underestimate genetic differentiation from marker data?, Molecular Ecology, Volume 24 (2015) no. 14, pp. 3546-3558 | DOI

[83] Waples, R. S. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci, Conservation Genetics, Volume 7 (2006) no. 2, pp. 167-184 | DOI

[84] Waples, R. S.; Do, C. Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution, Evolutionary Applications, Volume 3 (2010), pp. 244-262 | DOI

[85] Watts, P. C.; Rousset, F.; Saccheri, I. J.; Leblois, R.; Kemp, S. J.; Thompson, D. J. Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata: Zygoptera) populations: analysis of 'neighbourhood size' using a more precise estimator, Molecular Ecology, Volume 16 (2007) no. 4, p. 737-51 | DOI

[86] Weir, B.; Cockerham, C. Estimating F-statistics for the analysis of population structure, Evolution, Volume 38 (1984), pp. 1358-1370 | DOI

[87] Werren, J. H. Sex ratio adaptations to local mate competition in a parasitic wasp, Science, Volume 208 (1980) no. 4448, pp. 1157-1159 | DOI

[88] Wright, S. The interpretation of population structure by F-statistics with special regard to system of mating, Evolution, Volume 19 (1965), pp. 395-420 | DOI

[89] Yang, R. C. Estimating hierarchical F-statistics, Evolution, Volume 52 (1998) no. 4, pp. 950-956 | DOI

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