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“Singing on the Wing” as a Mechanism for Species Recognition in the Malarial Mosquito Anopheles gambiae

2010; Elsevier BV; Volume: 20; Issue: 2 Linguagem: Inglês

10.1016/j.cub.2009.11.040

1879-0445

Cédric Pennetier, Ben Warren, Roch K. Dabiré, Ian J. Russell, Gabriella Gibson,

Viral Infections and Vectors

Anopheles gambiae, responsible for the majority of malaria deaths annually, is a complex of seven species and several chromosomal/molecular forms. The complexity of malaria epidemiology and control is due in part to An. gambiae's remarkable genetic plasticity, enabling its adaptation to a range of human-influenced habitats. This leads to rapid ecological speciation when reproductive isolation mechanisms develop [1Powell J.R. Petrarca V. della Torre A. Caccone A. Coluzzi M. Population structure, speciation, and introgression in the Anopheles gambiae complex.Parassitologia. 1999; 41: 101-113PubMed Google Scholar, 2Costantini C. Ayala D. Guelbeogo W.M. Pombi M. Some C.Y. Bassole I.H. Ose K. Fotsing J.M. Sagnon N. Fontenille D. et al.Living at the edge: Biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae.BMC Ecol. 2009; 9: 16Crossref PubMed Scopus (154) Google Scholar, 3della Torre A. Costantini C. Besansky N.J. Caccone A. Petrarca V. Powell J.R. Coluzzi M. Speciation within Anopheles gambiae—the glass is half full.Science. 2002; 298: 115-117Crossref PubMed Scopus (179) Google Scholar, 4Ayala F.J. Coluzzi M. Chromosome speciation: Humans, Drosophila, and mosquitoes.Proc. Natl. Acad. Sci. USA. 2005; 102: 6535-6542Crossref PubMed Scopus (237) Google Scholar, 5Besansky N.J. Krzywinski J. Lehmann T. Simard F. Kern M. Mukabayire O. Fontenille D. Touré Y. Sagnon N. Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: Evidence from multilocus DNA sequence variation.Proc. Natl. Acad. Sci. USA. 2003; 100: 10818-10823Crossref PubMed Scopus (167) Google Scholar, 6della Torre A. Fanello C. Akogbeto M. Dossou-yovo J. Favia G. Petrarca V. Coluzzi M. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa.Insect Mol. Biol. 2001; 10: 9-18Crossref PubMed Scopus (259) Google Scholar]. Although reproductive isolation is essential for speciation, little is known about how it occurs in sympatric populations of incipient species [2Costantini C. Ayala D. Guelbeogo W.M. Pombi M. Some C.Y. Bassole I.H. Ose K. Fotsing J.M. Sagnon N. Fontenille D. et al.Living at the edge: Biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae.BMC Ecol. 2009; 9: 16Crossref PubMed Scopus (154) Google Scholar]. We show that in such a population of “M” and “S” molecular forms, a novel mechanism of sexual recognition (male-female flight-tone matching [7Gibson G. Russell I. Flying in tune: Sexual recognition in mosquitoes.Curr. Biol. 2006; 16: 1311-1316Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar, 8Warren B. Gibson G. Russell I.J. Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion.Curr. Biol. 2009; 19: 485-491Abstract Full Text Full Text PDF PubMed Scopus (90) Google Scholar, 9Cator L.J. Arthur B.J. Harrington L.C. Hoy R.R. Harmonic convergence in the love songs of the dengue vector mosquito.Science. 2009; 323: 1077-1079Crossref PubMed Scopus (201) Google Scholar]) also confers the capability of mate recognition, an essential precursor to assortative mating; frequency matching occurs more consistently in same-form pairs than in mixed-form pairs (p = 0.001). Furthermore, the key to frequency matching is “difference tones” produced in the nonlinear vibrations of the antenna by the combined flight tones of a pair of mosquitoes and detected by the Johnston's organ. By altering their wing-beat frequencies to minimize these difference tones, mosquitoes can match flight-tone harmonic frequencies above their auditory range. This is the first description of close-range mating interactions in incipient An. gambiae species.