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Patterns of genetic diversity and differentiation in the tsetse fly Glossina morsitans morsitans Westwood populations in East and southern Africa

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Abstract

Genetic diversity and differentiation within and among nine G. morsitans morsitans populations from East and southern Africa was assessed by examining variation at seven microsatellite loci and a mitochondrial locus, cytochrome oxidase (COI). Mean COI diversity within populations was 0.63 ± 0.33 and 0.81 taken over all populations. Diversities averaged over microsatellite loci were high (mean number of alleles/locus ≥7.4; mean H E ≥ 65%) in all populations. Diversities averaged across populations were greater in East Africa (mean number of alleles = 22 ± 2.6; mean h e = 0.773 ± 0.033) than in southern Africa (mean number of alleles = 18.7 ± 4.0; mean h e = 0.713 ± 0.072). Differentiation among all populations was highly significant (R ST = 0.25, F ST = 0.132). Nei’s G ij statistics were 0.09 and 0.19 within regions for microsatellites and mitochondria, respectively; between regions, G ij was 0.14 for microsatellites and 0.23 for mitochondria. G ST among populations was 0.23 for microsatellite loci and 0.40 for mitochondria. The F, G and R statistics indicate highly restricted gene flow among G. m. morsitans populations separated over geographic scales of 12–917 km.

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References

  • Baker MD, Krafsur ES (2001) Identification and properties of microsatellite markers in tsetse flies Glossina morsitans sensu lato (Diptera: Glossinidae). Mol Ecol Notes 1:234–236

    Article  PubMed  CAS  Google Scholar 

  • Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol Ecol 11:771–783

    Article  PubMed  CAS  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165

    Article  PubMed  Google Scholar 

  • Barton NH, Slatkin M (1986) A quasi-equilibrium theory of distribution of rare alleles in a subdivided population. Heredity 56:409–415

    PubMed  Google Scholar 

  • Buxton PA (1955) The natural history of tsetse flies: memoir of the London School of Hygiene and Tropical Medicine no. 10. H.K. Lewis, London

    Google Scholar 

  • Challier A, Laveissière C (1973) Un nouveau piège pour la capture des glossines (Glossina; Diptera, Muscidae): description et essays sur le terrain. Cah. O.R.S.T.O.M. Sér Ent Méd Parasit 11:251–262

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Estoup A, Garnery L, Solignac M, Cornuet JM (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679– 695

    PubMed  CAS  Google Scholar 

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Ford J (1971) The role of trypanosomiases in African ecology. Clarendon Press, Oxford

    Google Scholar 

  • Ford J, Katondo KM (1977) The distribution of tsetse flies (Glossina) in Africa (1973) organization of African unity—scientific and technical research commission. Cook, Hammond & Kell, London

    Google Scholar 

  • Gaggioti OE, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8:1513–1520

    Article  Google Scholar 

  • Gooding RH, Krafsur ES (2005) Tsetse genetics: contributions to biology, systematics, and control of tsetse flies. Annu Rev Entomol 50:101–123

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2) available from http://www.unil.ch/izea/softwares/fstat.html

  • Greenacre MJ (1993) Correspondence analysis in practice. Academic Press, London

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hargrove JW (2000) A theoretical study of the invasion of cleared areas by tsetse flies (Diptera: Glossinidae). Bull Entomol Res 90:201–209

    PubMed  CAS  Google Scholar 

  • Hedrick PW (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  • Jordan AM (1993) Tsetse flies (Glossinidae). In: Lane RP, Crosskey RW (eds) Medical insects and arachnids. Chapman & Hall, London, pp 333–388

    Google Scholar 

  • Jordan AM, Trewern MA, Southern DI, Pell PE, Davies EDG (1977) Differences in laboratory performance between strains of Glossina morsitans morsitans Westwood from Rhodesia and Tanzania and associated chromosome diversity. Bull Entomol Res 67:35–48

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Krafsur ES (2003) Tsetse fly population genetics: an indirect approach to dispersal. Trends Parasitol 19:162–166

    Article  PubMed  Google Scholar 

  • Krafsur ES, Endsley MA (2002) Microsatellite diversities and gene flow in the tsetse fly, Glossina morsitans s.l. Med Vet Entomol 16:292–300

    Article  PubMed  CAS  Google Scholar 

  • Krafsur ES, Griffiths N (1997) Genetic variation at structural loci in the Glossina morsitans species group. Biochem Genet 35:1–11

    Article  PubMed  CAS  Google Scholar 

  • Krafsur ES, Wohlford DL (1999) Breeding structure of Glossina pallidipes populations evaluated by mitochondrial variation. J Hered 90:635–642

    Article  PubMed  CAS  Google Scholar 

  • Krafsur ES, Endsley MA, Wohlford DL, Griffiths NT, Allsopp R (2001) Genetic differentiation of Glossina morsitans centralis populations. Insect Mol Biol 10:387–395

    Article  PubMed  CAS  Google Scholar 

  • Krafsur ES, Griffiths N, Brockhouse CL, Brady J (1997) Breeding structure of G. pallidipes in East and southern Africa. Bull Entomol Res 87:67–73

    Article  Google Scholar 

  • Kreitman M, Akashi H (1995) Molecular evidence for natural selection. Annu Rev Ecol Syst 26:403–422

    Article  Google Scholar 

  • Leak SGA (1999) Tsetse biology and ecology: their role in the epidemiology and control of trypanosomosis. CABI Publishing, Wallingford, 568 pp

  • Li CC, Horvitz DG (1953) Some methods of estimating the inbreeding coefficient. Am J Hum Genet 5:107–117

    PubMed  CAS  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • 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

    Google Scholar 

  • Ouma JO, Cummings MA, Jones KC, Krafsur ES (2003) Characterization of microsatellite markers in the tsetse fly, Glossina pallidipes (Diptera: Glossinidae). Mol Ecol Notes 3:450–453

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249. Software available at http://wbiomed.curtin.edu.au/genepop/

    Google Scholar 

  • Robinson TP, Rogers DJ, Williams B (1997a) Mapping tsetse habitat suitability in the common fly belt of Southern Africa using multivariate analysis of climate and remotely sensed vegetation data. Med Vet Entomol 11:235–245

    CAS  Google Scholar 

  • Robinson TP, Rogers DJ, Williams B (1997b) Univariate analysis of tsetse habitat in the common fly belt of Southern Africa using climate and remotely sensed vegetation data. Med Vet Entomol 11:223–234

    CAS  Google Scholar 

  • Rogers DJ (1977) Study of a natural population of tsetse flies and a model for fly movements. J Anim Ecol 46:309–330

    Article  Google Scholar 

  • Rogers DJ (1998) Satellite imagery and the prediction of tsetse distribution in East Africa. Proceedings of the symposium on the diagnosis and control of livestock disease using nuclear and related techniques: towards disease control in the 21st century, IAEA, Vienna, 1997, pp 397–420

  • Rogers DJ, Robinson TP (2004) Tsetse distribution. In: Maudlin I, Holmes P, Miles M (eds) The trypanosomiases. CAB International, Oxford, pp 139–179

    Google Scholar 

  • Rozas J, Sanches-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • SAS (2001) SAS language reference, version 8.2. SAS Institute Inc., Cary, North Carolina

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva

  • Shahjahan RM, Hughes KJ, Leopold RA, DeVault JD (1995) Lower incubation temperature increases yield of insect genomic DNA isolated by the CTAB method. BioTechniques 19:333–334

    Google Scholar 

  • Simon C, Fratti F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel tests of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Terblanche JS, Klok CJ, Krafsur ES, Chown SL (2005) Phenotypic plasticity and geographic variation in thermal tolerance and water loss in the tsetse Glossina pallidipes (Diptera: Glossinidae): implications for distributional modelling. Am J Trop Med Hyg 74:786–794

    Google Scholar 

  • Vale GA, Harshey BS, Hargrove JW (1984) The use of small plots to study populations of tsetse (Diptera: Glossinidae). Insect Sci Appl 5:403–410

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Williams B, Dransfield R, Brightwell R (1992) The control of tsetse flies in relation to fly movement and trapping efficiency. J Appl Ecol 29:163–179

    Article  Google Scholar 

  • Wohlford DL, Krafsur ES, Griffiths NT, Marquez JG, Baker MD (1999) Genetic differentiation of some Glossina morsitans morsitans populations. Med Vet Entomol 13:377–385

    Article  PubMed  CAS  Google Scholar 

  • Workman PL, Niswander JD (1970) Population studies on south-western Indian tribes. II. Local differentiation in the Papago. Am J Hum Genet 22:24–49

    PubMed  CAS  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, vol. 2. The theory of gene frequencies. University of Chicago Press, Chicago

    Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations, vol. 4. Variability within and among natural populations. University of Chicago Press, Chicago

    Google Scholar 

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Acknowledgements

We thank Dra Imna Malele, Dr. John Terblanche, Messrs Godfrey Mashenge, Cassim Omari and Juma Mwita of TTRI for assistance with sampling G. m. morsitans in Tanzania. Dr. Nigel Griffiths did the southern African samplings. Thanks to Prof. David Rogers, TALA Research Group, Zoology department, Oxford, for the distribution map of G. m. morsitans. This research was supported by NIH USPHS Grants AI-40048 and AI-52456 to ESK.

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Ouma, J.O., Marquez, J.G. & Krafsur, E.S. Patterns of genetic diversity and differentiation in the tsetse fly Glossina morsitans morsitans Westwood populations in East and southern Africa. Genetica 130, 139–151 (2007). https://doi.org/10.1007/s10709-006-9001-0

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