Differences in timing of mating swarms in sympatric populations of Anopheles coluzzii and Anopheles gambiae s.s. (formerly An. gambiae M and S molecular forms) in Burkina Faso, West Africa

Particle and Fibre Toxicology

Roch K Dabiré³  Gabriella Gibson⁴  Abdoulaye Diabaté³  Cédric Pennetier¹  Carlo Costantini²  Simon P Sawadogo³ 

[1] IRD/CREC, MIGEVEC (UM1, UM2, CNRS5290, IRD 224), Cotonou 08 BP 841, Bénin;IRD/UMR, MIGEVEC (UM1, UM2, CNRS5290, IRD 224), Centre IRD de Montpellier, Montpellier Cedex 5 BP 64501, 34394, France;Institut de Recherche en Sciences de la Santé (IRSS)/Centre Muraz, Bobo-Dioulasso 01 BP 545, Burkina Faso;Department of Agriculture, Health and Environment, Natural Resources Institute (NRI), University of Greenwich at Medway, Chatham ME4 4TB, Kent, UK

关键词: Anopheles gambiae s.s;    Anopheles coluzzii;    Reproductive isolation;    Mating swarms;    Environmental factors;    Circadian rhythms;    Behaviour;    Allochronic speciation;    Actographs;    Activity rhythms;   

Others  :  824536
DOI  :  10.1186/1756-3305-6-275

 received in 2012-10-20, accepted in 2013-09-13,  发布年份 2013

【 摘 要 】

Background

The M and S molecular forms of Anopheles gambiae s.s. Giles appear to have speciated in West Africa and the M form is now formally named An. coluzzii Coetzee & Wilkerson sp.n. and the S form retains the nominotypical name (abbreviated here to An. gambiae). Reproductive isolation is thought to be the main barrier to hybridisation; even though both species are found in the same mating swarms, hybrid fertilisations in copulae have not been found in the study area. The aim of the study, therefore, was to determine whether differences in circadian and/or environmental control over the timing of swarming in the two species contribute to reproductive isolation.

Methods

The timing of male swarming in these species was recorded four nights per month over four years at five swarming sites in each of two villages. The timing of the start and end of swarming, and the concurrent environmental parameters, temperature, humidity and light intensity, were recorded for n = 20 swarms/month/species. The timing of 'spontaneous’ activity at dusk of individual An. coluzzii and An. gambiae males was video-recorded in an actograph outdoors for 21 nights.

Results

Of the environmental parameters considered, swarming was most strongly correlated with sunset (r² > 0.946). Anopheles gambiae started and stopped swarming earlier than An. coluzzii (3:35 ± 0:68 min:sec and 4:51 ± 1:21, respectively), and the mean duration of swarming was 23:37 ± 0:33 for An. gambiae and 21:39 ± 0:33 for An. coluzzii. Accordingly, in principle, whenever both species swarm over the same marker, a mean of 15.3 ± 3.1% of An. gambiae swarming would occur before An. coluzzii males arrived, and 19.5 ± 4.55% of An. coluzzii swarming would occurred after An. gambiae males had stopped swarming. These results are consistent with the finding that An. gambiae males became active in the actograph 09:35 ± 00:22 min:sec earlier than An. coluzzii males.

Conclusions

The timing of swarming and spontaneous activity at dusk are primarily under circadian control, with the phase linked closely to sunset throughout the year. The mating activity of these two species is temporally segregated for 15-20% of the swarming period, which may contribute to the observed reproductive isolation of these species in local sympatric populations.

【 授权许可】

   
2013 Sawadogo et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]WHO 2013. http://www.who.int/features/factfiles/malaria/en/index.html webcite
• [2]WHO: Global malaria programme; indoor residual spraying; use of indoor residual spraying for scaling up global malaria control and elimination. Geneva: World Health Organization; 2006.
• [3]Diabaté A, Baldet T, Chandre F, Akogbeto M, Guiguemdé TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM: The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 2002, 67(6):617-622.
• [4]Dabiré KR, Diabaté A, Namountougou M, Toé KH, Ouari A, Kengne P, Bass C, Baldet T: Distribution of pyrethroid and DDT resistance and the L1014F kdr mutation in Anopheles gambiae s.l. from Burkina Faso (West Africa). Trans R Soc Trop Med Hyg 2009, 103:1113-1120.
• [5]Dabiré KR, Diabaté A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T: Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health 2009, 14:396-403.
• [6]N’Guessan R, Corbel V, Akogbéto M, Rowland M: Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis 2007, 13:199-206.
• [7]Czeher C, Labbo R, Arzika I, Duchemin JB: Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar J 2008, 7:189. BioMed Central Full Text
• [8]Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M: Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 2002, 417:452-455.
• [9]Moreira AL, Ito J, Ghosh A, Devenport M, Zieler H, Abraham EG, Crisanti A, Nolan T, Catteruccia F, Jacobs-Lorena M: Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 2002, 277:40839-40843.
• [10]James AA: Blocking malaria parasite invasion of mosquito salivary glands. J Exp Biol 2003, 206:3817-3821.
• [11]Benedict MQ, Robinson AS: The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol 2003, 19:349-355.
• [12]Dame DA, Curtis CF, Benedict MQ, Robinson AS, Knols BGJ: Historical applications of induced sterilization in field populations of mosquitoes. Malar J 2009, 8:S2.
• [13]Coetzee M, Hunt RH, Wilkerson R, dellaTorre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 2013, 3619:246-274.
• [14]Reidenbach KR, Neafsey DE, Costantini C, Sagnon NF, Simard F, Ragland GJ, Egan SP, Feder JL, Muskavitch MAT, Besansky NJ: Patterns of genomic differentiation between ecologically differentiated M and S forms of Anopheles gambiae in West and Central Africa. Genome, Biol and Evol 2012, 4:1202-1212.
• [15]Della Torre A, Tu Z, Petrarca V: On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem Mol Biol 2005, 35:755-769.
• [16]Caputo B, Santolamazza F, Vicente JL, Nwakanma DC, Jawara M, Palsson K, Jaenson T, White BJ, Mancini E, Petrarca V, Conway DJ, Besansky NJ, Pinto J, della Torre A: The “far-west” of Anopheles gambiae molecular forms. PLoS One 2011, 6:e16415.
• [17]Oliveira E, Salgueiro P, Palsson K, Vicente JL, Arez AP, Jaenson TG, Caccone A, Pinto J: High levels of hybridization between molecular forms of Anopheles gambiae from Guinea Bissau. J Med Entomol 2008, 45:1057-1063.
• [18]Marsden CD, Lee Y, Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, Lanzaro GC: Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol 2011, 20:4983-4994.
• [19]Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ: Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol 2012, 29:279-291.
• [20]Tripet F, Touré YT, Taylor CE, Norris DE, Dolo G, Lanzaro GC: DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol Ecol 2001, 10:1725-1732.
• [21]Dabiré KR, Sawadodgo SP, Diabaté A, Toe KH, Kengne P, Ouari A, Costantini C, Gouagna C, Simard F, Baldet T, Lehmann T, Gibson G: Assortative mating in mixed swarms of the mosquito Anopheles gambiae s.s. M and S molecular forms, in Burkina Faso, West Africa. Med Vet Entomol 2013, 27:298-312.
• [22]Downes JA: The swarming and mating flight of Diptera. Ann Rev Entomol 1969, 14:271-298.
• [23]Reisen WK, Aslamkhan M: Observations on the swarming and mating behavior of Anopheles culicifacies Giles in nature. Bull World Health Org 1976, 54:155-158.
• [24]Baker RH, Reisen WK, Sakai RK, Rathor HR, Raana K, Azra A, Niaz S: Anopheles culicifacies: mating behavior and competitiveness in nature of males carrying a complex chromosomal aberration. Ann Entomol Soc Am 1980, 73:581-588.
• [25]Sullivan RT: Insect swarming and mating. Fl Entomol 1981, 64:44-65.
• [26]Yuval B, Wekesa JW, Washino RK: Effect of body size on swarming behaviour and mating success of male Anopheles freeborni (Diptera: Culicidae). J Insect Behav 1993, 6:333-342.
• [27]Clements AN: The Biology of mosquitoes. Sensory Reception and Behavior Volume 2. London: CABI; 1999.
• [28]Downes JA: Assembly and mating in the biting Nematocera. In Proceedings of the Tenth International Congress on Entomology 1958, 2:425-434.
• [29]Yuval B: Mating systems of blood-feeding flies. Ann Rev Entomol 2006, 51:413-440.
• [30]Gibson G: The swarming behaviour of the mosquito Culex pipiens quinqufasciatus: a quantitative analysis. Physiol Entomol 1985, 10:283-296.
• [31]Charlwood JD, Jones MDR: Mating behaviour in the mosquito Anopheles gambiae s.l. I. Close range and contact behaviour. Physiol Entomol 1979, 4:111-120.
• [32]Marchand RP: Field observations on swarming and mating in Anopheles gambiae mosquitoes in Tanzania. Neth J Zool 1984, 34:367-387.
• [33]Charlwood JD, Thomson R, Madsen H: The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol 2002, 27:178-183.
• [34]Manoukis NC, Diabaté A, Abdola A, Diallo M, Dao A, Yaro AS, Ribeiro JMC, Lehman T: Structure and dynamics of male swarms of Anopheles gambiae. J Med Entomol 2009, 46:227-235.
• [35]Butail S, Manoukis N, Diallo M, Ribeiro J, Lehmann T, Paley DA: Reconstructing the flight kinematics of swarming and mating in wild mosquitoes. J R Soc Interface 2012, 9:2624-38.
• [36]Diabaté A, Baldet T, Brengues C, Kengne P, Dabiré KR, Simard F, Chandre F, Hougard JM, Hemingway J, Ouédraogo JB, Fontenille D: Natural swarming behaviour in the molecular M form of Anopheles gambiae. Trans R Soc Trop Med Hyg 2003, 97:713-716.
• [37]Diabaté A, Dabiré KR, Kengne P, Baldet T, Ouari A, Costantini C, Simard F, Fontenille D: Mixed-swarms of the molecular M and S forms of Anopheles gambiae in a sympatric area from Burkina Faso. J Med Entomol 2006, 43:480-483.
• [38]Diabaté A, Dao A, Yaro AS, Adamou A, Gonzalez R, Manoukis NC, Traoré SF, Gwadz WR, Lehmann T: Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc R Soc B 2009, 276:4215-4222.
• [39]Diabaté A, Yaro AS, Dao A, Diallo M, Huestis DL, Lehmann T: Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evolutionary Biol 2011, 11:184. BioMed Central Full Text
• [40]Choi C, Nitbach MN: Circadian Biology: Environmental Regulation of a Multi-Oscillator Network. Curr Biol 2012, 29:R322-324.
• [41]Jones MDR, Gubbins SJ: Changes in the circadian flight activity of the mosquito Anopheles gambiae in relation to insemination, feeding and oviposition. Physiol Entomol 1978, 3:213-220.
• [42]Baldet T, Diabaté A, Guiguemdé TR: Etude de la transmission du paludisme en 1999 dans la zone rizicole de la Vallée du Kou (Bama), Burkina Faso. Cahier Santé 2003, 13:55-60.
• [43]Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C: Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae ss. Insect Mol Biol 2001, 10:19-23.
• [44]Scott JA, Brogdon WG, Collins FH: Identification of a single specimen of An. gambiae complex by polymerase chain reaction. Am J Trop Med Hyg 1993, 49:520-529.
• [45]Fanello C, Santolamazza F, della Torre A: Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol 2002, 16:461-464.
• [46]Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, della Torre A: Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J 2008, 7:163. BioMed Central Full Text
• [47]Santolamazza F, Caputo B, Calzetta M, Vicente JL, Mancini E, Petrarca V, Pinto , della Torre A: Comparative analyses reveal discrepancies among results of commonly used methods for Anopheles gambiae molecular form identification. Malar J 2011, 10:215. BioMed Central Full Text
• [48]Hawkes F, Young S, Gibson G: Modification of spontaneous activity patterns in the malaria vector Anopheles gambiae s.s. when presented with host-associated stimuli. Physiol Entomol 2012, 37:233-240.
• [49]Gibson G: A behavioural test of the sensitivity of a nocturnal mosquito, An. gambiae, to dim white, red and infra-red light. Physiol Entomol 1995, 20:224-228.
• [50]R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2009. ISBN 3-900051-07-0, URL http://www.R-project.org webcite
• [51]Charlwood JD, Jones MDR: Mating in the mosquito Anopheles gambiae s.l. II. Swarming behaviour. Physiol Entomol 1980, 5:315-320.
• [52]Rund SSC, Lee SJ, Bush BR, Duffield GE: Strain- and sex-specific differences in daily flight activity and the circadian clock of Anopheles gambiae mosquitoes. J Insect Physiol 2012, 58:1609-1619.
• [53]Sakai T, Ishida N: Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci U S A 2001, 98:9221-9225.
• [54]Miyatake T, Matsumoto A, Matsuyama T, Ueda HR, Toyosato T, Tanimura T: The period gene and allochronic reproductive isolation in Batrocera cucurbitae. Proc Roy Soc Lond. B 2002, 269:2467-2472.
• [55]Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP: Temporal mating isolation driven by a behavioural gene in Drosophila. Curr Biol 2003, 13:140-145.
• [56]Kiszewski AE, Spielman A: Spatially explicit model of transposon-based genetic drive mechanisms for displacing fluctuating populations of anopheline vector mosquitoes. J Med Entomol 1998, 35:584-590.
• [57]Knols BGJ, Njiru BN, Mathenge EM, Mukabana WR, Beier JC, Killeen GF: Malaria sphere: A greenhouse-enclosed simulation of a natural Anopheles gambiae (Diptera: Culicidae) ecosystem in Western Kenya. Malar J 2002, 1:19. BioMed Central Full Text
• [58]Scott TW, Takken W, Knols BGJ, Boete C: The ecology of genetically modified mosquitoes. Science 2002, 298:117-119.
• [59]Knols BGJ, Njiru BN, Mukabana RW, Mathenge EM, Killeen GF: Contained semi-field environments for ecological studies on transgenic African malaria vectors. In Ecology of transgenic mosquitoes. Edited by Scott TW, Takken W. Wageningen: Wageningen University and Research Centre; 2003:99-106.
• [60]Ferguson FM, John B, Ng’habi K, Knols BGJ: Addressing the sex imbalance in knowledge of vector biology. Trends Evol Ecol 2005, 20:202-209.