Targeting male mosquito mating behaviour for malaria control

Particle and Fibre Toxicology

Frédéric Tripet¹  Abdoulaye Diabate² 

[1] Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Newcastle-under-Lyme, UK;Institut de Recherche en Sciences de la Santé/Centre Muraz, Bobo-Dioulasso, Burkina Faso

关键词: Lure-and-kill;    Swarm killing;    Transgenic mosquito releases;    Sterile male release;    Vector control;    Mating behaviour;    Swarm ecology;    Anopheles gambiae;   

Others  :  1224139
DOI  :  10.1186/s13071-015-0961-8

 received in 2014-12-01, accepted in 2015-06-17,  发布年份 2015

【 摘 要 】

Malaria vector control relies heavily on the use of Long-Lasting Insecticidal Nets (LLINs) and Indoor Residual Spraying (IRS). These, together with the combined drug administration efforts to control malaria, have reduced the death toll to less than 700,000 deaths/year. This progress has engendered real excitement but the emergence and spread of insecticide resistance is challenging our ability to sustain and consolidate the substantial gains that have been made. Research is required to discover novel vector control tools that can supplement and improve the effectiveness of those currently available. Here, we argue that recent and continuing progress in our understanding of male mating biology is instrumental in the implementation of new approaches based on the release of either conventional sterile or genetically engineered males. Importantly, further knowledge of male biology could also lead to the development of new interventions, such as sound traps and male mass killing in swarms, and contribute to new population sampling tools. We review and discuss recent advances in the behavioural ecology of male mating with an emphasis on the potential applications that can be derived from such knowledge. We also highlight those aspects of male mating ecology that urgently require additional study in the future.

【 授权许可】

   
2015 Diabate and Tripet.

【 图 表 】

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【 参考文献 】

• [1]Campbell CC. Halting the toll of malaria in Africa. Am J Trop Med Hyg. 2008; 78:851-3.
• [2]World malaria report. 2008.
• [3]Ulrich JN, Naranjo DP, Alimi TO, Muller GC, Beier JC. How much vector control is needed to achieve malaria elimination? Trends Parasitol. 2013; 29:104-9.
• [4]Ferguson HM, John B, Nghabi K, Knols BGJ. Redressing the sex imbalance in knowledge of vector biology. Trends Ecol Evol. 2005; 20:202-9.
• [5]Benedict MQ, Robinson AS. The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol. 2003; 19:349-55.
• [6]Diabate A, Yaro AS, Dao A, Diallo M, Huestis DL, Lehmann T. Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evol Biol. 2011; 11:184. BioMed Central Full Text
• [7]Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013; 3619:246-74.
• [8]Diabate A, Dao A, Yaro AS, Adamou A, Gonzalez R, Manoukis NC, Traore SF, Gwadz RW, Lehmann T. Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc R Soc Lond B Biol Sci. 2009; 276:4215-22.
• [9]Dabire KR, Sawadogo PS, Hien DF, Bimbile-Somda NS, Soma DD, Millogo A, Baldet T, Gouagna LC, Simard F, Lefevre T et al.. Occurrence of natural Anopheles arabiensis swarms in an urban area of Bobo-Dioulasso city, Burkina Faso, West Africa. Acta Trop. 2014; 132 Suppl:35-41.
• [10]Assogba BS, Djogbenou L, Saizonou J, Diabate A, Dabire RK, Moiroux N, Gilles JRL, Makoutode M, Baldet T. Characterization of swarming and mating behaviour between Anopheles coluzzii and Anopheles melas in a sympatry area of Benin. Acta Trop. 2014; 132 Suppl:53-63.
• [11]Downes JA. The swarming and mating flight of Diptera. Ann Rev Entomol. 1969; 14:271-98.
• [12]Charlwood JD, Pinto J, Sousa CA, Ferreira C, Do Rosario VE. Male size does not affect mating success of Anopheles gambiae in São Tomé. Med Vet Entomol. 2002; 16:109-11.
• [13]Butail S, Manoukis N, Diallo M, Ribeiro JM, Lehmann T, Paley DA. Reconstructing the flight kinematics of swarming and mating in wild mosquitoes. J R Soc Interface. 2012; 9:2624-38.
• [14]Beehler BM, Foster MS. Hotshots, hotspots, and female preference in the organization of lek mating systems. Am Nat. 1988; 131:203-19.
• [15]Diabate A, Dabire RK, Kengne P, Brengues C, Baldet T, Ouari A, Simard F, Lehmann T. Mixed swarms of the molecular M and S forms of Anopheles gambiae (Diptera : Culicidae) in sympatric area from Burkina Faso. J Med Entomol. 2006; 43:480-3.
• [16]Maiga H, Niang A, Sawadogo SP, Dabire RK, Lees RS, Gilles JRL, Tripet F, Diabate A. Role of nutritional reserves and body size in Anopheles gambiae males mating success. Acta Trop. 2014; 132 Suppl:102-7.
• [17]Caputo B, Nwakanma D, Jawara M, Adiamoh M, Dia I, Konate L, Petrarca V, Conway DJ, Della Torre A. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s. Malar J. 2008; 7:182. BioMed Central Full Text
• [18]Dao A, Adamou A, Yaro AS, Maiga HM, Kassogue Y, Traore SF, Lehmann T. Assessment of alternative mating strategies in Anopheles gambiae: does mating occur indoor ? J Med Entomol. 2008; 45:643-52.
• [19]Pitts RJ, Mozuaraitis R, Gauvin-Bialecki A, Lemperiere G. The roles of kairomones, synomones and pheromones in the chemically-mediated behaviour of male mosquitoes. Acta Trop. 2014; 132 Suppl:26-34.
• [20]Lanzaro GC, Tripet F. Gene flow among populations of Anopheles gambiae: A critical review. In: Ecological aspects for application of genetically modified mosquitoes. Takken W, Scott TW, editors. Kluwer Academic Press, Dordrecht; 2003: p.109-32.
• [21]Lang TL, Foster WA. Is there a female pheromone in the mosquito Culiseta inornata? Environ Entomol. 1976; 5:1109-15.
• [22]Lang JT. Contact sex-pheromone in mosquito Culiseta inornata (Diptera Culicidae). J Med Entomol. 1978; 14:448-54.
• [23]Nijhout HF, Craig GB. Reproductive isolation in Stegomyia mosquitoes. III. Evidence for a sexual pheromone. Entomol Exp Appl. 1971; 14:399-412.
• [24]Caputo B, Dani FR, Horne GL, N’Fale S, Diabate A, Turillazzi S, Coluzzi M, Costantini C, Priestman AA, Petrarca V et al.. Comparative analysis of epicuticular lipid profiles of sympatric and allopatric field populations of Anopheles gambiae s.s. molecular forms and An. arabiensis from Burkina Faso (West Africa). Insect Biochem Mol Biol. 2007; 37:389-98.
• [25]Brogdon WG. Measurement of flight tone differentiates among members of the Anopheles gambiae species complex (Diptera: Culicidae). J Med Entomol. 1998; 35:681-4.
• [26]Wekesa JW, Brogdon WG, Hawley WA, Besansky NJ. Flight tone of field-collected populations of Anopheles gambiae and An. arabiensis (Diptera: Culicidae). Physiol Entomol. 1998; 23:289-94.
• [27]Tripet F, Dolo G, Traore S, Lanzaro GC. The “wingbeat hypothesis” of reproductive isolation between members of the Anopheles gambiae complex (Diptera : Culicidae) does not fly. J Med Entomol. 2004; 41:375-84.
• [28]Gibson G, Russell I. Flying in tune: sexual recognition in mosquitoes. Curr Biol. 2006; 16:1311-6.
• [29]Pennetier C, Warren B, Dabire KR, Russell IJ, Gibson G. “Singing on the Wing” as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr Biol. 2010; 20:131-6.
• [30]Cator LJ, Arthur BJ, Harrington LC, Hoy RR. Harmonic convergence in the love songs of the dengue vector mosquito. Science. 2009; 323:1077-9.
• [31]Warren B, Gibson G, Russell IJ. Sex recognition through midflight mating duets in culex mosquitoes is mediated by acoustic distortion. Curr Biol. 2009; 19:485-91.
• [32]Gibson G, Warren B, Russell IJ. Humming in tune: sex and species recognition by mosquitoes on the wing. J Assoc Res Otolaryngol. 2010; 11:527-40.
• [33]Cator LJ, Ng’Habi KR, Hoy RR, Harrington LC. Sizing up a mate: variation in production and response to acoustic signals in Anopheles gambiae. Behav Ecol. 2010; 21:1033-9.
• [34]Cator LJ, Harrington LC. The harmonic convergence of fathers predicts the mating success of sons in Aedes aegypti. Anim Behav. 2011; 82:627-33.
• [35]Kahn MC, Offenhauser W. The first field tests of recorded mosquito sounds used for mosquito destruction. Am J Trop Med Hyg. 1949; 29:811-25.
• [36]Clements AN. The biology of mosquitoes: sensory reception and behaviour. Cambridge University Press, Cambridge, UK; 1999.
• [37]Ikeshoji T. Acoustic attraction of male mosquitoes in a cage. Med Entomol Zool. 1981; 32:7-15.
• [38]Kanda T, Loong KP, Chiang GL, Cheong WH, Lim TW. Field study on sound trapping and the development of trapping method for both sexes of Mansonia in Malaysia. Trop Biomed. 1988; 5:37-42.
• [39]Cade W. The evolution of alternative male reproductive strategies in field crickets. Academic, New York; 1979.
• [40]Ulagaraj SM, Walker TJ. Response of flying mole crickets to 3 parameters of synthetic songs broadcast outdoors. Nature. 1975; 253:530-2.
• [41]Forrest TG. Phonotaxis in mole crickets: its reproductive significance. Fla Entomol. 1980; 63:45-53.
• [42]Njiru BN, Mukabana WR, Takken W, Knols BGJ. Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malaria J. 2006; 5:39. BioMed Central Full Text
• [43]Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W et al.. Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS One. 2010; 5:e8951.
• [44]Mweresa CK, Omusula P, Otieno B, van Loon JJA, Takken W, Mukabana WR. Molasses as a source of carbon dioxide for attracting the malaria mosquitoes Anopheles gambiae and Anopheles funestus. Malaria J. 2014; 13:160. BioMed Central Full Text
• [45]Sinkins SP, Gould F. Gene drive systems for insect disease vectors. Nat Rev Genet. 2006; 7:427-35.
• [46]Alphey L. Genetic control of mosquitoes. Annu Rev Entomol. 2014; 59:205-24.
• [47]Burt A. Heritable strategies for controlling insect vectors of disease. Philos Trans R Soc B Biol Sci. 2014; 369:20130432.
• [48]Davidson G, Odetoyinbo JA, Colussa B, Coz J. A field attempt to assess the mating competitiveness of sterile males produced by crossing 2 members species of the Anopheles gambiae complex. Bull World Health Organ. 1970; 42:55-67.
• [49]Seawright JA, Kaiser PE, Willis NL, Dame DA. Field competitiveness of double translocation heterozygote males of Aedes aegypti (L). J Med Entomol. 1976; 13:208-11.
• [50]Reisen WK, Knop NF, Peloquin JJ. Swarming and mating-behavior of laboratory and field strains of Culex tarsalis (Diptera, Culicidae). Ann Entomol Soc Am. 1985; 78:667-73.
• [51]Dame DA, Woodard DB, Ford HR, Weidhaas DE. Field behavior of sexually sterile Anopheles quadrimaculatus males. Mosq News. 1964; 24:6-14.
• [52]Milby MM, Nelson RL, McDonald PT. Release of heterozygous translocated adult males for genetic control of Culex tarsalis at an isolated site. Mosq News. 1980; 40:83-90.
• [53]Reisen WK, Milby MM, Asman SM, Bock ME, Meyer RP, McDonald PT, Reeves WC. Attempted suppression of a semi-isolated Culex tarsalis population by the release of irradiated males: a 2nd experiment using males from a recently colonized strain. Mosq News. 1982; 42:565-75.
• [54]Baeshen R, Ekechukwu NE, Toure M, Paton D, Coulibaly M, Traore SF, Tripet F. Differential effects of inbreeding and selection on male reproductive phenotype associated with the colonization and laboratory maintenance of Anopheles gambiae. Malaria J. 2014; 13:19. BioMed Central Full Text
• [55]Tripet F, Toure 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; 10:1725-32.
• [56]Takken W, Costantini C, Dolo G, Hassanali A, Sagnon N, Osir E. Mosquito mating behaviour. In: Bridging Laboratory and Field Research for Genetic Control of Disease Vectors. Kitsos L, Knols B, editors. Kluwer Academic Press, Dordrecht; 2006: p.157-64.
• [57]Lees RS, Knols B, Bellini R, Benedict MQ, Bheecarry A, Bossin HC, Chadee DD, Charlwood J, Dabire RK, Djogbenou L et al.. Review: Improving our knowledge of male mosquito biology in relation to genetic control programmes. Acta Trop. 2014; 132 Suppl:2-11.
• [58]Benedict MQ, Knols BGJ, Bossin HC, Howell PI, Mialhe E, Caceres C, Robinson AS. Colonisation and mass rearing: learning from others. Malaria J. 2009; 8 Suppl 2:S4. BioMed Central Full Text
• [59]Sawadogo SP, Diabate A, Toe HK, Sanon A, Lefevre T, Baldet T, Gilles J, Simard F, Gibson G, Sinkins S et al.. Effects of age and size on Anopheles gambiae s.s. male mosquito mating success. J Med Entomol. 2013; 50:285-93.
• [60]Marrelli MT, Moreira CK, Kelly D, Alphey L, Jacobs-Lorena M. Mosquito transgenesis: what is the fitness cost? Trends Parasitol. 2006; 22:197-202.
• [61]Paton D, Underhill A, Meredith J, Eggleston P, Tripet F. Contrasted fitness costs of docking and antibacterial constructs in the EE and EVida3 strains validates two-phase Anopheles gambiae genetic transformation system. PLoS One. 2013; 8:e0067364.
• [62]Paton D, Toure M, Sacko A, Coulibaly MB, Traore SF, Tripet F. Genetic and environmental factors associated with laboratory rearing affect survival and assortative mating but not overall mating success in Anopheles gambiae sensu stricto. PLoS One. 2013; 8:e82631.
• [63]Nghabi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BGJ, Ferguson HM. Sexual selection in mosquito swarms: may the best man lose? Anim Behav. 2008; 76:105-12.
• [64]Aboagye-Antwi F, Guindo A, Traore AS, Hurd H, Coulibaly M, Traore S, Tripet F. Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malaria J. 2010; 9:243. BioMed Central Full Text
• [65]Maiga H, Dabire RK, Lehmann T, Tripet F, Diabate A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J Vector Ecol. 2012; 37:289-97.
• [66]Crompton B, Thomason JC, McLachlan A. Mating in a viscous universe: the race is to the agile, not to the swift. Proc R Soc Lond B Biol Sci. 2003; 270:1991-5.
• [67]Mahmood F, Reisen WK. Anopheles Culicifacies: effects of age on the male reproductive system and mating ability of virgin adult mosquitoes. Med Vet Entomol. 1994; 8:31-7.
• [68]Bonduriansky R. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev. 2001; 76:305-39.
• [69]Lyimo EO, Takken W. Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol. 1993; 7:328-32.
• [70]Okanda F, Dao A, Njiru B, Arija J, Akelo H, Toure Y, Odulaja A, Beier J, Githure J, Yan G et al.. Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malar J. 2002; 1:10. BioMed Central Full Text
• [71]Baker RH, Reisen WK, Sakai RK, Rathor HR, Raana K, Azra K, Niaz S. Anopheles culicifacies Diptera, Culicidae - mating-behavior and competitiveness in nature of males carrying a complex chromosomal aberration. Ann Entomol Soc Am. 1980; 73:581-8.
• [72]Asman SM, McDonald PT, Prout T. Field studies of genetic-control systems for mosquitoes. Ann Rev Entomol. 1981; 26:289-318.
• [73]Huettel MD. Introduction: Measuring overall performance. In: Quality control - an idea book for fruitfly workers. IOBC/WPRS Bull. Vol. 5. Boller EF, Chambers DL, editors. IOBC/WPRS, Gent; 1977: p.14-6.
• [74]Singh KRP, Brooks GD, Ansari MA. Mass rearing of mosquitoes. J Commun Dis. 1974; 6:121-6.
• [75]Dame DA, Lofgren CS, Ford HR, Boston MD, Baldwin KF, Jeffery GM. Release of chemosterilized males for the control of Anopheles albimanus in El Salvador. II. Methods of rearing, sterilization, and distribution. Am J Trop Med Hyg. 1974; 23:282-7.
• [76]Dame DA, Haile DG, Lofgren CS, Bailey DL, Munroe WL. Improved rearing techniques for larval Anopheles albimanus - use of dried mosquito eggs and electric-heating tapes. Mosq News. 1978; 38:68-74.
• [77]Bailey DL, Lowe RE, Dame DA, Seawright JA. Mass rearing the genetically altered Macho strain of Anopheles albimanus Wiedemann. Am J Trop Med Hyg. 1980; 29:141-9.
• [78]Boller EF. Behavioral aspects of quality in insectary production. In: Genetics in relation to insect management. Hoy MA, McKelvey JJ, editors. Rockefeller Foundation, New York; 1979: p.153-60.
• [79]Bushland RC. Screwworm eradication program. Science. 1974; 184:1010-1.
• [80]Hibino Y, Iwahashi O. Appearance of wild females unreceptive to sterilized males on okinawa island in the eradication program of the melon fly, Dacus cucurbitae coquillett (Diptera, Tephritidae). Appl Entomol Zool. 1991; 26:265-70.
• [81]McInnis DO, Lance DR, Jackson CG. Behavioral resistance to the sterile insect technique by Mediterranean fruit fly (Diptera: Tephritidae) in Hawaii. Ann Entomol Soc Am. 1996; 89:739-44.