Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-23T21:44:06.878Z Has data issue: false hasContentIssue false
  • English
  • Français

The fine-scale genetic structure of the malaria vectors Anopheles funestus and Anopheles gambiae (Diptera: Culicidae) in the north-eastern part of Tanzania

Published online by Cambridge University Press:  17 August 2016

P. Gélin ,
H. Magalon ,
C. Drakeley ,
C. Maxwell ,
S. Magesa ,
W. Takken  and
C. Boëte
P. Gélin
Affiliation:
UMR ENTROPIE Université de La Réunion/IRD/CNRS, Faculté des Sciences et Technologies, Université de La Réunion, 15 Bd René Cassin, CS 92003, 97744 St Denis Cedex 09, La Réunion, France
H. Magalon
Affiliation:
UMR ENTROPIE Université de La Réunion/IRD/CNRS, Faculté des Sciences et Technologies, Université de La Réunion, 15 Bd René Cassin, CS 92003, 97744 St Denis Cedex 09, La Réunion, France
C. Drakeley
Affiliation:
Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, WC1E 7HT, London, UK Joint Malaria Programme, PO Box 2228 Moshi, Tanzania
C. Maxwell
Affiliation:
Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, WC1E 7HT, London, UK Amani Medical Research Centre, National Institute for Medical Research, PO Box 81, Muheza, Tanzania
S. Magesa
Affiliation:
Amani Medical Research Centre, National Institute for Medical Research, PO Box 81, Muheza, Tanzania
W. Takken
Affiliation:
Laboratory of Entomology, Wageningen University and Research Centre, PO Box 16, 6700, AA Wageningen, the Netherlands
C. Boëte*
Affiliation:
Joint Malaria Programme, PO Box 2228 Moshi, Tanzania Laboratory of Entomology, Wageningen University and Research Centre, PO Box 16, 6700, AA Wageningen, the Netherlands UMR “Emergence des Pathologies Virales”, EPV Aix-Marseille Université, IRD 190 - Inserm 1207 - EHESP, 27 Bd Jean Moulin, 13005, Marseille, France
*
*E-mail: cboete@gmail.com
Get access

Abstract

Understanding the impact of altitude and ecological heterogeneity at a fine scale on the populations of malaria vectors is essential to better understand and anticipate eventual epidemiological changes. It could help to evaluate the spread of alleles conferring resistance to insecticides and also determine any increased entomological risk of transmission in highlands due to global warming. We used microsatellite markers to measure the effect of altitude and distance on the population genetic structure of Anopheles funestus and Anopheles gambiae s.s. in the Muheza area in the north-eastern part of Tanzania (seven loci for each species). Our analysis reveals strong gene flow between the different populations of An. funestus from lowland and highland areas, as well as between populations of An. gambiae sampled in the lowland area. These results highlight for An. funestus the absence of a significant spatial subpopulation structuring at small-scale, despite a steep ecological and altitudinal cline. Our findings are important in the understanding of the possible spread of alleles conferring insecticide resistance through mosquito populations. Such information is essential for vector control programmes to avoid the rapid spread and fixation of resistance in mosquito populations.

Keywords

Anopheles funestusAnopheles gambiaealtitudemalariamicrosatellitepopulation geneticsTanzania
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 36 , Issue 4 , December 2016 , pp. 161 - 170
Copyright
Copyright © icipe 2016 

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

Alilio, M. S., Kitua, A., Njunwa, K., Medina, M., Rønn, A.M., Mhina, J., Msuya, F., Mahundi, J., Depinay, J. M., Whyte, S., Krasnik, A. and Bygbjerg, I. C. (2004) Malaria control at the district level in Africa: The case of the Muheza District in Northeastern Tanzania. American Journal of Tropical Medicine and Hygiene 71 (2 Suppl), 205–213.Google Scholar
Boëte, C. and Joint Malaria Programme, KCMC, Tanzania (2006) Genetically Modified Mosquitoes for Malaria Control, http://www.landesbioscience.com. ISBN: 1-58706-096-5.Google Scholar
Chaves, L. F., Imanishi, N. and Hoshi, T. (2015) Population dynamics of Armigeres subalbatus (Diptera: Culicidae) across a temperate altitudinal gradient. Bulletin of Entomological Research 105, 589–597. doi: 10.1017/S0007485315000474.Google Scholar
Cohuet, A., Simard, F., Berthomieu, A., Raymond, M., Fontenille, D. and Weill, M. (2002) Isolation and characterization of microsatellite DNA markers in the malaria vector Anopheles funestus . Molecular Ecology Notes 2, 498–500. doi: 10.1046/j.1471-8286.2002.00290.x.Google Scholar
Donnelly, M. J., Pinto, J., Girod, R., Besansky, N. J. and Lehmann, T. (2004) Revisiting the role of introgression vs shared ancestral polymorphisms as key processes shaping genetic diversity in the recently separated sibling species of the Anopheles gambiae complex. Heredity 92, 61–68. doi:10.1038/sj.hdy.6800377.Google Scholar
Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: A simulation study. Molecular Ecology 14, 2611–2620.Google Scholar
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin (Version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47–50.Google Scholar
Falush, D., Stephens, M. and Pritchard, J. K. (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587.Google Scholar
Gillies, M. T. and Coetzee, M. (1987) A Supplement to the Anophelinae of Africa South of Sahara (Afrotropical Region). South African Institute for Medical Research, Johannesburg, South Africa. 143 pp.Google Scholar
Gillies, M. T. and De Meillon, B. (1968) The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). South African Institute for Medical Research, Johannesburg, South Africa. 343 pp.Google Scholar
Gorospe, K. D. and Karl, S. A. (2013) Genetic relatedness does not retain spatial pattern across multiple spatial scales: Dispersal and colonization in the coral, Pocillopora damicornis . Molecular Ecology 22, 3721–3736. doi:10.1111/mec.12335.Google Scholar
Gorospe, K. D. and Karl, S. A. (2015) Depth as an organizing force in Pocillopora damicornis: Intra-reef genetic architecture. PLoS ONE 10, e0122127. doi:10.1371/journal.pone.0122127.Google Scholar
Goudet, J. (1995) FSTAT (Version 1.2): A computer program to calculate F-Statistics. Journal of Heredity 86, 485–486.Google Scholar
Hodkinson, I. D. (2005) Terrestrial insects along elevation gradients: Species and community responses to altitude. Biological Reviews 80, 489–513. doi:10.1017/S1464793105006767.Google Scholar
Kamau, L., Lehmann, T., Hawley, W. A., Orago, A. S. and Collins, F. H. (1998) Microgeographic genetic differentiation of Anopheles gambiae mosquitoes from Asembo bay, western Kenya: A comparison with Kilifi in coastal Kenya. The American Journal of Tropical Medicine and Hygiene 58, 64–69.Google Scholar
Kamugisha, M. L., Maxwell, C. and Curtis, C. F. (2005) Characteristics of malaria among children living in lowlands and highlands of Muheza District, north-east Tanzania. Tanzania Health Research Bulletin 7, 67–72.Google Scholar
Koekemoer, L. L., Kamau, L., Hunt, R. H. and Coetzee, M. (2002) A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. The American Journal of Tropical Medicine and Hygiene 66, 804–811.Google Scholar
Lehmann, T., Hawley, W. A., Kamau, L., Fontenille, D., Simard, F. and Collins, F. H. (1996) Genetic differentiation of Anopheles gambiae populations from East and West Africa: Comparison of microsatellite and allozyme loci. Heredity 77, 192–208.Google Scholar
Levy, S. (2007) Mosquito modifications: New approaches to controlling malaria. BioScience 57, 816–821. doi:10.1641/B571003.Google Scholar
Luckhart, S., Li, K., Dunton, R., Lewis, E. E., Crampton, A. L., Ryan, J. R. and Rosenberg, R. (2003) Anopheles gambiae immune gene variants associated with natural Plasmodium infection. Molecular and Biochemical Parasitology 128, 83–86. doi: 10.1016/S0166-6851(03)00016-1.Google Scholar
Magesa, S. M., Wilkes, T. J., Mnzava, A. E., Njunwa, K. J., Myamba, J., Kivuyo, M. D., Hill, N., Lines, J. D. and Curtis, C. F. (1991) Trial of pyrethroid impregnated bednets in an area of Tanzania holoendemic for malaria. Part 2. Effects on the malaria vector population. Acta Tropica 49, 97–108.CrossRefGoogle Scholar
Maliti, D., Ranson, H., Magesa, S., Kisinza, W., Mcha, J., Haji, K., Killeen, G. and Weetman, D. (2014) Islands and stepping-stones: Comparative population structure of Anopheles gambiae sensu stricto and Anopheles arabiensis in Tanzania and implications for the spread of insecticide resistance. PLoS ONE 9 (10), e110910. doi:10.1371/journal.pone.0110910.Google Scholar
Mboera, L. and Magesa, S. (2001) The rise and fall of malarial sporozoite rates in Anopheles gambiae s.l. and An. funestus in north-eastern Tanzania, between 1934 and 1999. Annals of Tropical Medicine & Parasitology 95, 325–330.Google Scholar
Michel, A. P., Guelbeogo, W. M., Grushko, O., Schemerhorn, B. J., Kern, M., Willard, M. B., Sagnon, N'F., Costantini, C. and Besansky, N. J. (2005) Molecular differentiation between chromosomally defined incipient species of Anopheles funestus . Insect Molecular Biology 14, 375–387. doi: 10.1111/j.1365-2583.2005.00568.x.Google Scholar
Midega, J. T., Muturi, E. J., Baliraine, F. N., Mbogo, C. M., Githure, J., Beier, J. C. and Yan, G. (2010) Population structure of Anopheles gambiae along the Kenyan coast. Acta Tropica 114, 103–108. doi:10.1016/j.actatropica.2010.01.011.Google Scholar
Perrier, X. and Jacquemoud-Collet, J. P. (2006) DARwin Software v 5.0. http://darwin.cirad.fr/.Google Scholar
Pritchard, J. K., Stephens, M. and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle ScholarPubMed
Ranson, H., N'guessan, R., Lines, J., Moiroux, N., Nkuni, Z. and Corbel, V. (2011) Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends in Parasitology 27, 91–98.Google Scholar
Sinkins, S. P., Hackett, B. J., Costantini, C., Vulule, J., Ling, Y.-Y., Collins, F. H. and Besansky, N. J. (2000) Isolation of polymorphic microsatellite loci from the malaria vector Anopheles funestus . Molecular Ecology 9, 490–492. doi:10.1046/j.1365-294x.2000.00871-2.Google Scholar
Stein, A., Gerstner, K. and Kreft, H. (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters 17, 866–880.Google Scholar
Temu, E. A., Minjas, J. N., Coetzee, M., Hunt, R. H. and Shiff, C. J. (1998) The role of four anopheline species (Diptera: Culicidae) in malaria transmission in coastal Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 152–158.Google Scholar
Temunović, M., Franjić, J., Satovic, Z., Grgurev, M., Frascaria-Lacoste, N. and Fernández-Manjarrés, J. F. (2012) Environmental heterogeneity explains the genetic structure of continental and Mediterranean populations of Fraxinus angustifolia Vahl. PLoS ONE 7 (8), e42764. doi:10.1371/journal.pone.0042764.Google Scholar
Torda, G., Lundgren, P., Willis, B. L. and van Oppen, M. J. H. (2013) Revisiting the connectivity puzzle of the common coral Pocillopora damicornis . Molecular Ecology 22, 5805–5820. doi:10.1111/mec.12540.Google Scholar
Touré, Y. T., Petrarca, V., Traoré, S. F., Coulibaly, A., Maïga, H. M., Sankaré, O., Sow, M., Di Deco, M. A. and Coluzzi, M. (1994) Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Genetica 94, 213–223.Google Scholar
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M. and Shipley, P. (2004) Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.CrossRefGoogle Scholar
van Rooyen, J., Lalubin, F., Glaizot, O. and Christe, P. (2013) Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites & Vectors 6, 139. doi: 10.1186/1756-3305-6-13.Google Scholar
Wang, S. and Jacobs-Lorena, M. (2013) Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends in Biotechnology 31, 185–193. doi: 10.1016/j.tibtech.2013.01.001.Google Scholar
Weir, B. S. and Cockerham, C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
WHO [World Health Organization] (2014) World Malaria Report 2014. World Health Organization, Geneva, Switzerland. 242 pp. ISBN: 978 92 4 156483 0.Google Scholar
Wilkins, E. E., Howell, P. I. and Benedict, M. Q. (2006) IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis . Malaria Journal 5, 125. doi: 10.1186/1475-2875-5-125.Google Scholar
Zheng, L., Benedict, M. Q., Cornel, A. J., Collins, F. H. and Kafatos, F. C. (1996) An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae . Genetics 143, 941–952.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gélin supplementary material

Gélin supplementary material 1

Download Gélin supplementary material(File)
File 54.3 KB
Supplementary material: File

Gélin supplementary material

Gélin supplementary material 2

Download Gélin supplementary material(File)
File 36.9 KB
Supplementary material: File

Gélin supplementary material

Gélin supplementary material 3

Download Gélin supplementary material(File)
File 28.7 KB