Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T10:55:09.215Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic structure and range expansion of Zeugodacus Cucurbitae (Diptera: Tephritidae) in Africa

Published online by Cambridge University Press:  07 February 2019

H. Delatte ,
M. De Meyer  and
M. Virgilio
H. Delatte*
Affiliation:
CIRAD, UMR PVBMT, F-97410 Saint-Pierre, Réunion, France
M. De Meyer
Affiliation:
Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
M. Virgilio
Affiliation:
Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
*
*Author for correspondence Phone: 00262262492735 Fax: 00262262492793 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Hypotheses about the worldwide colonization routes of the melon fly, Zeugodacus cucurbitae (Diptera: Tephritidae), are mainly based on sparse historical records. Here we aim at reconstructing the colonization history of the African continent based on an improved description of the population structure of Z. cucurbitae and approximate Bayesian analyses. Individuals of Z. cucurbitae were sampled in 17 localities from East, West and Central Africa and genotyped at 19 microsatellite markers. Bayesian analyses showed intracontinental population structuring with populations from Uganda diverging from those of Tanzania and populations from Burundi and Kenya showing traces of admixture with West African samples. Approximate Bayesian Computation provided support to the hypothesis of a single introduction Z. cucurbitae into East Africa and subsequent expansion to West Africa, each colonization event was followed by a bottleneck that promoted population divergence within Africa. Parameter estimates suggested that these events are roughly compatible with the historical records of Z. cucurbitae presence in sub-Saharan Africa (viz. 1936 in East Africa and 1999 in West Africa) and allow excluding alternative hypotheses on older or multiple introductions of Z. cucurbitae.

Keywords

agricultural pestsTephritidaeZeugodacuspopulation structurecolonization historyABC
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 6 , December 2019 , pp. 713 - 722
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N. & Bonhomme, F. (1996) GENETIX 4.05, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, Université de Montpellier II, Montpellier (France).Google Scholar
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 57, 289–300.Google Scholar
Boontop, Y., Schutze, M.K., Clarke, A.R., Cameron, S.L. & Krosch, M.N. (2017 a) Signatures of invasion: using an integrative approach to infer the spread of melon fly, Zeugodacus cucurbitae (Diptera: Tephritidae), across Southeast Asia and the West Pacific. Biological Invasions 19, 1597–1619.Google Scholar
Boontop, Y., Kumaran, N., Schutze, M.K., Clarke, A.R., Cameron, S.L. & Krosch, M.N. (2017 b) Population structure in Zeugodacus cucurbitae (Diptera: Tephritidae) across Thailand and the Thai–Malay peninsula: natural barriers to a great disperser. Biological Journal of the Linnean Society 121, 540–555.Google Scholar
Chapuis, M-P. & Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.Google Scholar
Cornuet, J.M., Santos, F., Beaumont, M.A., Robert, C.P., Marin, J.M., Balding, D.J., Guillemaud, T. & Estoup, A. (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics (Oxford, England) 24, 2713–2719.Google Scholar
Cornuet, J-M., Ravigné, V. & Estoup, A. (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1. 0). Bmc Bioinformatics 11, 401.Google Scholar
Cornuet, J-M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M., Leblois, R., Marin, J.-M. & Estoup, A. (2014) DIYABC v2. 0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189. https://doi.org/10.1093/bioinformatics/btt763Google Scholar
De Meyer, M., Delatte, H., Mwatawala, M., Quilici, S., Vayssières, J.-F. & Virgilio, M. (2015) A review of the current knowledge on Zeugodacus cucurbitae (Diptera: Tephritidae) in Africa. ZooKeys 540, 539–557.Google Scholar
Delatte, H., Virgilio, M., Simiand, C., Risterucci, A.M., DeMeyer, M. & Quilici, S. (2010) Isolation and characterization of microsatellite markers from Bactrocera cucurbitae (Coquillett). Molecular Ecology Ressources 10, 576–579.Google Scholar
Dempster, A., Laird, N. & DB, R. (1977) Maximum likelihood from incomplete data via the EM algorithm. Journal of the Royal Statistical Society: Series B 39, 1–38.Google Scholar
Dhillon, M.K., Singh, R., Naresh, J.S. & Sharma, H.C. (2005) The melon fruit fly, Bactrocera cucurbitae: a review of its biology and management. Journal of Insect Science 5, 1–16. https://doi.org/10.1093/jis/5.1.40.Google Scholar
Drew, R. & Hancock, D. (2000) Phylogeny of the tribe Dacini (Dacinae) based on morphological, distributional, and biological data. pp. 491–504 in Aluja, M. (Ed.) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. New York, CRC Press.Google Scholar
Dupuis, J.R., Sim, S.B., San Jose, M., Leblanc, L., Hoassain, M.A., Rubinoff, D. & Geib, S.M. (2017) Population genomics and comparisons of selective signatures in two invasions of melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Biological Invasions 20, 1211–1228.Google Scholar
Estoup, A. & Guillemaud, T. (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Molecular Ecology 19, 4113–4130.Google Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14, 2611–2620.Google Scholar
Gao, H., Williamson, S. & Bustamante, C.D. (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176, 1635–1651.Google Scholar
Goudet, J. (2001) Fstat, a Program to Estimate and Test Gene Diversities and Fixation Indices Version 2.9.3. Available online at http://www.unil.ch/izea/softwares/fstat.html.Google Scholar
Gilbert, E. (2004) Dhows and the Colonial Economy of Zanzibar 1860–1970, p. 167. Athens, Ohio, Ohio University Press.Google Scholar
Jacquard, C., Virgilio, M., David, P., Quilici, S., De Meyer, M. & Delatte, H. (2013) Population structure of the melon fly, Bactrocera cucurbitae, in Reunion Island. Biological Invasions 15, 759–773.Google Scholar
Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics (Oxford, England) 23, 1801–1806.Google Scholar
Khamis, F.M., Karam, N., Ekesi, S., de Meyer, M., Bonomi, A., Gomulski, L.M., Scolari, F., Gabrieli, P., Siciliano, P., Masiga, D., Kenya, E.U., Gasperi, G., Malacrida, A.R. & Guglielmino, C.R. (2009) Uncovering the tracks of a recent and rapid invasion: the case of the fruit fly pest Bactrocera invadens (Diptera: Tephritidae) in Africa. Molecular Ecology 18, 4798–4810.Google Scholar
Lombaert, E., Guillemaud, T., Cornuet, J.M., Malausa, T., Facon, B. & Estoup, A. (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5, e9743.Google Scholar
Mwatawala, M.W., De Meyer, M., Makundi, R.H. & Maerere, A.P. (2009) Host range and distribution of fruit-infesting pestiferous fruit flies (Diptera, Tephritidae) in selected areas of Central Tanzania. Bulletin of Entomological Research 99, 629–641.Google Scholar
Mwatawala, M., Maerere, A.P., Makundi, R. & De Meyer, M. (2010) Incidence and host range of the melon fruit fly Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) in Central Tanzania. International Journal of Pest Management 56, 265–273.Google Scholar
Nei, M. (1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences 70, 3321–3323.Google Scholar
Nei, M. (1987) Molecular Evolutionary Genetics. New York, Columbia University Press.Google Scholar
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. Molecular Ecology 13, 55–65.Google Scholar
Piry, S., Alapetite, A., Cornuet, J-M., Paetkau, D., Baudouin, L. & Estoup, A. (2004) Geneclass2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95, 536–539.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Rannala, B. & Mountain, J.L. (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences 94, 9197–9221.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP: a population genetics software for exact tests and ecumenicisms. Journal of Heredity 86, 248–249.Google Scholar
Rosenberg, N.A. (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.Google Scholar
San Jose, M., Doorenweerd, C., Leblanc, L., Barr, N., Geib, S. & Rubinoff, D. (2017) Incongruence between molecules and morphology: a seven-gene phylogeny of Dacini fruit flies paves the way for reclassification (Diptera: Tephritidae). Molecular Phylogenetics and Evolution 121, 139–149.Google Scholar
Selkoe, K.A. & Toonen, R.J. (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9, 615–629.Google Scholar
Sood, P., Prabhakar, C.S., Yadav, D.S. & Thakur, S.K. (2016) Popularizing IPM of fruit flies in cucurbits and subtropical fruits through an area wide aproach in north western Himalaya. Proceedings of the 9th ISFFEI, 78–86.Google Scholar
Vargas, R.I., Walsh, W.A., Kanehisa, D., Stark, J.D. & Nishida, T. (2000) Comparative demography of three Hawaiian fruit flies (Diptera: Tephritidae) at alternating temperatures. Annals of the Entomological Society of America 93, 75–81.Google Scholar
Vayssières, J.F., Rey, J.Y. & Traoré, L. (2007) Distribution and host plants of Bactrocera cucurbitae in West and Central Africa. Fruits 62, 391–396.Google Scholar
Vayssières, J.F., Carel, Y., Coubes, M. & Duyck, P.F. (2008) Development of immature stages and comparative demography of two cucurbit-attacking fruit flies in Réunion Island: Bactrocera cucurbitae and Dacus ciliatus. Environmental Entomology 37, 307–314.Google Scholar
Virgilio, M., Delatte, H., Backeljau, T. & De Meyer, M. (2010) Macrogeographic population structuring in the cosmopolitan agricultural pest Bactrocera cucurbitae (Diptera: Tephritidae). Molecular Ecology 19, 2713–2724.Google Scholar
Virgilio, M., Jordaens, K., Verwimp, C., White, I.M. & De Meyer, M. (2015) Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): localised partition conflicts and a novel generic classification. Molecular Phylogenetics and Evolution 85, 171–179.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar
White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, CAB International.Google Scholar
Wu, Y., Li, Z. & Wu, J. (2009) Polymorphic microsatellite markers in the melon fruit fly, Bactrocera cucurbitae (Coquillett)(Diptera: Tephritidae). Molecular Ecology Resources 9, 1404–1406.Google Scholar
Supplementary material: File

Delatte et al. supplementary material

Delatte et al. supplementary material 1

Download Delatte et al. supplementary material(File)
File 1.3 MB