Spatial distribution and male mating success of Anopheles gambiae swarms

BMC Evolutionary Biology

Tovi Lehmann²  Diana L Huestis²  Moussa Diallo¹  Adama Dao¹  Alpha S Yaro¹  Abdoulaye Diabaté³ 

[1] Malaria Research and Training Center, University of Bamako, Bamako, Mali;Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland 20852, USA;Institut de Recherche en Sciences de la Santé/Centre Muraz, Bobo-Dioulasso, Burkina Faso

关键词: scramble competition;    lek;    mating success;    Anopheles gambiae;   

Others  :  1143671
DOI  :  10.1186/1471-2148-11-184

 received in 2011-03-11, accepted in 2011-06-28,  发布年份 2011

【 摘 要 】

Background

Anopheles gambiae mates in flight at particular mating sites over specific landmarks known as swarm markers. The swarms are composed of males; females typically approach a swarm, and leave in copula. This mating aggregation looks like a lek, but appears to lack the component of female choice. To investigate the possible mechanisms promoting the evolution of swarming in this mosquito species, we looked at the variation in mating success between swarms and discussed the factors that structure it in light of the three major lekking models, known as the female preference model, the hotspot model, and the hotshot model.

Results

We found substantial variation in swarm size and in mating success between swarms. A strong correlation between swarm size and mating success was observed, and consistent with the hotspot model of lek formation, the per capita mating success of individual males did not increase with swarm size. For the spatial distribution of swarms, our results revealed that some display sites were more attractive to both males and females and that females were more attracted to large swarms. While the swarm markers we recognize help us in localizing swarms, they did not account for the variation in swarm size or in the swarm mating success, suggesting that mosquitoes probably are attracted to these markers, but also perceive and respond to other aspects of the swarming site.

Conclusions

Characterizing the mating system of a species helps understand how this species has evolved and how selective pressures operate on male and female traits. The current study looked at male mating success of An. gambiae and discussed possible factors that account for its variation. We found that swarms of An. gambiae conform to the hotspot model of lek formation. But because swarms may lack the female choice component, we propose that the An. gambiae mating system is a lek-like system that incorporates characteristics pertaining to other mating systems such as scramble mating competition.

【 授权许可】

   
2011 Diabaté et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Beehler BM, Foster MS: Hotshots, hotspots, and female preference in the organization of lek mating systems. American Naturalist 1988, 131:203-219.
• [2]Bradbury JW: The evolution of leks. In Natural selection and social behavior: research and new theory. Edited by Alexander RD, Tinkle DW. New York Chiron Press; 1981:138-169.
• [3]Jiguet F, Bretagnolle V: Manipulating lek size and composition using decoys: an experimental investigation of lek evolution models. American Naturalist 2006, 168:758-768.
• [4]Mackenzie A, Reynolds JD, Brown VJ, and Sutherland WJ: Variation in male mating success at leks. American Naturalist 1995, 145:633-652.
• [5]McGhee KE, Fuller RC, and Travis J: Male competition and female choice interact to determine mating success in the bluefin killifish. Behavioral Ecology 2007, 18:822-830.
• [6]Bradbury JW, Gibson RM: Leks and mate choice. In Bateson P (ed) Mate choice. Cambridge University Press; 1983:109-138.
• [7]Wiley RH: Lekking in birds and mammals: Behavioural and evolutionary issues. Adv Study Behav 1991, 20:201-291.
• [8]Alexander RD: Natural selection and specialized chorusing behavior in acoustical insects. In Insects, Science and Society. Edited by Pimentel D. New York: Academic Press; 1975:35-77.
• [9]Parker GA: Evolution of competitive mate searching. Annual Review of Entomol 1978, 23:173-196.
• [10]Bradbury JW, Gibson R, Tsai IM: Hotspots and the dispersion of leks. Anim Behav 1986, 34:1694-1709.
• [11]Hoglund J, Atalato R: Leks. Princeton: Princeton University Press; 1995.
• [12]Sutherland W J: From individual behavior to population ecology. In Oxford series in ecology and evolution. Oxford, UK: Oxford University Press; 1996.
• [13]Arak A: Male-male competition and mate choice in anuran amphibians. In Mate Choice. Edited by Bateson P. Cambridge: Cambridge University Press; 1983:181-210.
• [14]Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C, do Rosario VE: The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol 2002, 27:178-183.
• [15]Downes JA: The swarming and mating flight of Diptera. Annu Rev Entomol 1969, 14:271-298.
• [16]Yuval B: Mating systems of blood-feeding flies. Annu Rev Entomol 2006, 51:413-440.
• [17]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. Transactions of Royal Society of Tropical Medicine and Hygiene 2003, 97:1-4.
• [18]Diabaté A, Dao A, Yaro AS, Adamaou A, Gonzalez R, Manoukis N, Traoré SF, Gwadz RW, Lehmann T: Reproductive isolation through swarm segregation in the molecular forms of Anopheles gambiae. Proceedings of the Royal Society of London Series B - Biological Sciences 2009, 276:4215-4222.
• [19]Charlwood JD, Jones DR: Mating behaviour in the mosquito, Anopheles gambiae s.l. I. Close range and contact behaviour. Physiological Entomology 1979, 4:111-120.
• [20]Thornhill R, Alcock J: The Evolution of Insect Mating Systems. Cambridge, MA: Harvard University Press; 1983.
• [21]Queller DG: The evolution of leks through female choice. Anim Behav 1987, 35:1424-1432.
• [22]Emlen ST, Oring LW: Ecology, sexual selection, and the evolution of mating systems. Science 1977, 197:215-223.
• [23]Höglund J, Montgomerie R, Widemo F: Costs and consequences of variation in the size of ruff leks. Behavioral Ecology and Sociobiology 1993, 32:31-39.
• [24]Kokko H: The lekking game: can female choice explain aggregated male displays? Journal of Theoretical Biology 1997, 187:57-64.
• [25]Niyazi N, Shuker DM, Wood RJ: Male position and calling effort together influence male attractiveness in leks of the medfly, Ceratitis capitata (Diptera: Tephritidae). Biol J Linn Soc 2008, 95:479-487.
• [26]Jones TM, Quinnell RJ: Testing predictions for the evolution of lekking in the sandfly, Lutzomyia longipalpis. Anim Behav 2002, 63:605-612.
• [27]Droney DC: Tests of hypotheses for lek formation in a Hawaiian Drosophila. Anim Behav 1994, 47:351-361.
• [28]Charlwood JD, Thompson R, Madsen H: Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malaria J 2003, 2:2. BioMed Central Full Text
• [29]Duraes R, Loiselle BA, Parker PG, Blake JG: Female mate choice across spatial scales: influence of lek and males attributes on mating success of blue-crowned manikins. Proceedings of the Royal Society of London Series B - Biological Sciences 2009, 276:1875-1881.
• [30]McLachlan A, Cant M: Small males are more symmetrical: mating success in the midge Chironomus plumosus (Diptera Chironomidae). Anim Behav 1995, 50:841-846.
• [31]Charlwood JD, Pinto J, Sousa CA, Ferreira C, Do Rosario VE: Male size does not affect mating success (of Anopheles gambiae in Sao Tome). Med Vet Entomol 2002, 16:109-111.
• [32]Yuval B, Wekesa JW, Washino RK: Effects of body size on swarming behaviour and mating success of male Anopheles freeborni (Diptera: Culicidae). J Insect Behav 1993, 6:333-342.
• [33]Ng'habi K, Huho BJ, Nkwengulila G, Killeen GF, Knols BGJ, Ferguson HM: Sexual selection in mosquito swarms: may the best man lose? Anim Behav 2008, 76:105-112.
• [34]Ng'habi KR, John B, Nkwengulila G, Knols BGJ, Killeen GF, Ferguson HM: Effect of larval crowding on mating competitiveness of Anopheles gambiae mosquitoes. Malaria Journal 2005, 4:1-9. BioMed Central Full Text
• [35]Verhoek BA, Takken W: Age effects on the Insemination rate of Anopheles gambiae sl in the laboratory. Entomol Exp Appl 1994, 72:167-172.
• [36]Chambers GM, Klowden MJ: Age of Anopheles gambiae Giles male mosquitoes at time of mating influences female oviposition. J Vector Ecol 2001, 26:196-201.
• [37]Voordouw MJ, Koella JC: Genetic variation of male reproductive success in a laboratory population of Anopheles gambiae. Malaria Journal 2007, 6:99. BioMed Central Full Text
• [38]Voordouw MJ, Koella JC, Hurd H: Intra-specific variation of sperm length in the malaria vector Anopheles gambiae: males with shorter sperm have higher reproductive success. Malaria Journal 2008, 7:214. BioMed Central Full Text
• [39]Cabrera M, Jaffe K: An aggregation pheromone modulates lekking behavior in the vector mosquito Aedes aegypti (Diptera: Culicidae). Journal of the American Mosquito Control Association 2007, 23:1-10.
• [40]Gibson G, Russell I: Flying in tune: sexual recognition in mosquitoes. Curr Biol 2006, 16:1311-1316.
• [41]Cator LJ, Arthur BJ, Harrington LC, Hoy RR: Harmonic convergence in the love songs of the dengue vector mosquito. Science 2009, 323:1077-1079.
• [42]Pennetier C, Warren B, Roch RK, Russell IJ, Gibson G: "Singing on the wing" as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Current Biology 2010, 26:131-136.
• [43]Yuval B, Bouskila A: Temporal dynamics of mating and predation in mosquito swarms. Oecologia 1993, 95:65-69.
• [44]Beani L, Turillazzi S: Male swarms at landmarks and scramble competition polygyny in Polistes gallicus (Hymenoptera, Vespidae). Journal of Insect Behavior 1990, 3:545-556.
• [45]Wiley RH, Poston J: Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 1996, 50:1371-1381.
• [46]Dao A: Etude du comportement pour l'accouplement chez Anopheles gambiae s.l. à l'intérieur des habitations rurales au Mali. PhD thesis. University of Bamako, Faculty of Medicine, Pharmacy & Odonto-Stomology; 2010.
• [47]Lehmann T, Dao A, Yaro AS, Adamou A, Kassogue Y, Diallo M, Sékou T, Coscaron-Arias C: Aestivation of the African malaria mosquito, Anopheles gambiae, in the Sahel. American Journal of Tropical Medicine and Hygiene 2010, 83:601-606.
• [48]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.
• [49]Huestis DL, Yaro AS, Traoré AI, Adamou A, Kassogué Y, Diallo M, Timbiné S, Dao A, Lehmann T: Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. Journal of Experimental Biology 2011, 214:2345-2353.