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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Molecular and physiological analysis of Anopheles funestus swarms in Nchelenge, Zambia

Authors: Jacek W. Zawada, Yael L. Dahan-Moss, Mbanga Muleba, Roch K. Dabire, Hamid Maïga, Nelius Venter, Craig Davies, Richard H. Hunt, Maureen Coetzee, Lizette L. Koekemoer

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Anopheles funestus has been recognized as a major malaria vector in Africa for over 100 years, but knowledge on many aspects of the biology of this species is still lacking. Anopheles funestus, as with most other anophelines, mate through swarming. A key event that is crucial for the An. funestus male to mate is genitalia rotation. This involves the 135° to 180° rotation of claspers, which are tipped with claws. This physical change then enables the male to grasp the female during copulation. The aim of this investigation was to molecularly characterize wild An. funestus swarms from Zambia and examine the degree of genitalia rotation within the swarm.

Methods

Anopheles funestus swarms were collected from Nchelenge, northern Zambia, during dusk periods in May 2016. All the adults from the swarm were analysed morphologically and identified to species level using a multiplex PCR assay. Anopheles funestus s.s. specimens were molecularly characterized by restriction fragment length polymorphism type and Clade type assays. The different stages of genitalia rotation were examined in the adult males.

Results

A total of six swarms were observed during the study period and between 6 and 26 mosquitoes were caught from each swarm. Species analysis revealed that 90% of the males from the swarms were An. funestus s.s. MW-type, with 84% belonging to clade I compared to 14% clade II and 2% failed to amplify. Very few specimens (3.4%) were identified as Anopheles gambiae s.s. Eighty percent of the males from the swarm had complete genitalia rotation.

Conclusions

This is the first time that An. funestus swarms have been molecularly identified to species level. Anopheles funestus swarms appear to be species-specific with no evidence of clade-type differentiation within these swarms. The An. funestus swarms consist mainly of males with fully rotated genitalia, which strongly suggests that swarming behaviour is triggered primarily when males have matured.
Literature
2.
go back to reference Gillies MT, De Meillon B. The anophelinae of Africa South of the Sahara. S Afr Inst Med Res Annu Rep. 1968;54:1–343. Gillies MT, De Meillon B. The anophelinae of Africa South of the Sahara. S Afr Inst Med Res Annu Rep. 1968;54:1–343.
3.
go back to reference Gillies MT, Coetzee M. A supplement to the anophelinae of Africa South of the Sahara. S Afr Inst Med Res Annu Rep. 1987;55:1–141. Gillies MT, Coetzee M. A supplement to the anophelinae of Africa South of the Sahara. S Afr Inst Med Res Annu Rep. 1987;55:1–141.
4.
go back to reference Harbach RE. The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res. 2004;94:537–53.CrossRefPubMed Harbach RE. The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res. 2004;94:537–53.CrossRefPubMed
5.
go back to reference Spillings BL, Brooke BD, Koekemoer LL, Chiphwanya J, Coetzee M, Hunt RH. A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg. 2009;81:510–5.PubMed Spillings BL, Brooke BD, Koekemoer LL, Chiphwanya J, Coetzee M, Hunt RH. A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg. 2009;81:510–5.PubMed
6.
go back to reference Cohuet A, Simard F, Toto J-C, Kengne P, Coetzee M, Fontenille D. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg. 2003;69:200–5.PubMed Cohuet A, Simard F, Toto J-C, Kengne P, Coetzee M, Fontenille D. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg. 2003;69:200–5.PubMed
7.
go back to reference Garros C, Koekemoer LL, Kamau L, Awolola TS, Van Bortel W, Coetzee M, et al. Restriction fragment length polymorphism method for the identification of major African and Asian malaria vectors within the Anopheles funestus and An. minimus groups. Am J Trop Med Hyg. 2004;70:260–5.PubMed Garros C, Koekemoer LL, Kamau L, Awolola TS, Van Bortel W, Coetzee M, et al. Restriction fragment length polymorphism method for the identification of major African and Asian malaria vectors within the Anopheles funestus and An. minimus groups. Am J Trop Med Hyg. 2004;70:260–5.PubMed
8.
go back to reference Koekemoer LL, Kamau L, Garros C, Manguin S, Hunt RH, Coetzee M. Impact of the Rift Valley on restriction fragment length polymorphism typing of the major African malaria vector Anopheles funestus (Diptera: Culicidae). J Med Entomol. 2006;43:1178–84.CrossRefPubMed Koekemoer LL, Kamau L, Garros C, Manguin S, Hunt RH, Coetzee M. Impact of the Rift Valley on restriction fragment length polymorphism typing of the major African malaria vector Anopheles funestus (Diptera: Culicidae). J Med Entomol. 2006;43:1178–84.CrossRefPubMed
9.
go back to reference Michel AP, Ingrasci MJ, Schemerhorn BJ, Kern M, Le Goff G, Coetzee M, Elissa N, et al. Rangewide population genetic structure of the African malaria vector Anopheles funestus. Mol Ecol. 2005;14:4235–48.CrossRefPubMed Michel AP, Ingrasci MJ, Schemerhorn BJ, Kern M, Le Goff G, Coetzee M, Elissa N, et al. Rangewide population genetic structure of the African malaria vector Anopheles funestus. Mol Ecol. 2005;14:4235–48.CrossRefPubMed
10.
go back to reference Choi KS, Coetzee M, Koekemoer LL. Detection of clade types (clades I and II) within Anopheles funestus sensu stricto by the hydrolysis probe analysis (Taqman assay). Parasit Vectors. 2013;6:173.CrossRefPubMedPubMedCentral Choi KS, Coetzee M, Koekemoer LL. Detection of clade types (clades I and II) within Anopheles funestus sensu stricto by the hydrolysis probe analysis (Taqman assay). Parasit Vectors. 2013;6:173.CrossRefPubMedPubMedCentral
11.
go back to reference Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, et al. Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 2014;8(7):464.CrossRef Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, et al. Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 2014;8(7):464.CrossRef
12.
go back to reference Charlwood JD, Thompson R, Madsen H. Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malar J. 2003;2:2.CrossRefPubMedPubMedCentral Charlwood JD, Thompson R, Madsen H. Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malar J. 2003;2:2.CrossRefPubMedPubMedCentral
13.
go back to reference Harper JO. Note on the swarming of males of Anopheles funestus Giles in East Africa. E Afr Med J. 1944;21:150–1. Harper JO. Note on the swarming of males of Anopheles funestus Giles in East Africa. E Afr Med J. 1944;21:150–1.
14.
go back to reference Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction (PCR) assay to identify the Anopheles funestus (Diptera: Culucidae) group. Am J Trop Med Hyg. 2002;36:125–36. Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction (PCR) assay to identify the Anopheles funestus (Diptera: Culucidae) group. Am J Trop Med Hyg. 2002;36:125–36.
15.
go back to reference Ng’habi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BG, Ferguson HM. Sexual selection in mosquito swarms: may the best man lose? Anim Behav. 2008;31(76):105–12.CrossRef Ng’habi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BG, Ferguson HM. Sexual selection in mosquito swarms: may the best man lose? Anim Behav. 2008;31(76):105–12.CrossRef
16.
17.
go back to reference Pennetier C, Warren B, Dabiré 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.CrossRefPubMed Pennetier C, Warren B, Dabiré 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.CrossRefPubMed
18.
go back to reference Rees DM, Onishi K. Morphology of the terminalia and internal reproductive organs, and copulation in the mosquito, Culiseta inornata (Williston) (Diptera, Culicidae). Proc Entomol Soc Wash. 1951;53:233–46. Rees DM, Onishi K. Morphology of the terminalia and internal reproductive organs, and copulation in the mosquito, Culiseta inornata (Williston) (Diptera, Culicidae). Proc Entomol Soc Wash. 1951;53:233–46.
19.
go back to reference Dahan YL, Koekemoer LL. Analysis of the genitalia rotation in the male Anopheles funestus (Diptera: Culicidae). Acta Trop. 2014;132:S20–5.CrossRefPubMed Dahan YL, Koekemoer LL. Analysis of the genitalia rotation in the male Anopheles funestus (Diptera: Culicidae). Acta Trop. 2014;132:S20–5.CrossRefPubMed
20.
go back to reference Clements AN. The biology of mosquitoes, vol. 2. CABI, Wallinford: Sensory reception and behaviour; 1999. Clements AN. The biology of mosquitoes, vol. 2. CABI, Wallinford: Sensory reception and behaviour; 1999.
21.
go back to reference Yuval B, Holliday-Hanson ML, Washing RK. Energy budget of swarming male mosquitoes. Ecol Entomol. 1994;19:74–8.CrossRef Yuval B, Holliday-Hanson ML, Washing RK. Energy budget of swarming male mosquitoes. Ecol Entomol. 1994;19:74–8.CrossRef
22.
go back to reference Warburg MS, Yuval B. Effects of energetic reserves on behavioral patterns of Mediterranean fruit flies (Diptera: Tephritidae). Oecologia. 1997;112:314–9.CrossRefPubMed Warburg MS, Yuval B. Effects of energetic reserves on behavioral patterns of Mediterranean fruit flies (Diptera: Tephritidae). Oecologia. 1997;112:314–9.CrossRefPubMed
23.
go back to reference Maïga H, Dabiré RK, Lehmann T, Tripet F, Diabaté A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J Vector Ecol. 2012;37:289–97.CrossRefPubMed Maïga H, Dabiré RK, Lehmann T, Tripet F, Diabaté A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J Vector Ecol. 2012;37:289–97.CrossRefPubMed
24.
go back to reference Yuval B, Bouskila A. Temporal dynamics of mating and predation in mosquito swarms. Oecologia. 1993;95:65–9.CrossRefPubMed Yuval B, Bouskila A. Temporal dynamics of mating and predation in mosquito swarms. Oecologia. 1993;95:65–9.CrossRefPubMed
25.
go back to reference Dahan-Moss YL, Koekemoer LL. Analysis of esterase enzyme activity in adults of the major malaria vector Anopheles funestus. Parasit Vectors. 2016;9:110.CrossRefPubMedPubMedCentral Dahan-Moss YL, Koekemoer LL. Analysis of esterase enzyme activity in adults of the major malaria vector Anopheles funestus. Parasit Vectors. 2016;9:110.CrossRefPubMedPubMedCentral
26.
go back to reference Dabiré KR, Sawadogo PS, Hien DF, Bimbilé-Somda NS, Soma DD, Millogo A, et al. Occurrence of natural Anopheles arabiensis swarms in an urban area of Bobo-Dioulasso city, Burkina Faso. West Africa. Acta Trop. 2014;132:S35–41.CrossRefPubMed Dabiré KR, Sawadogo PS, Hien DF, Bimbilé-Somda NS, Soma DD, Millogo A, et al. Occurrence of natural Anopheles arabiensis swarms in an urban area of Bobo-Dioulasso city, Burkina Faso. West Africa. Acta Trop. 2014;132:S35–41.CrossRefPubMed
27.
go back to reference Scott JA, Brogdon W, Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRefPubMed Scott JA, Brogdon W, Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRefPubMed
28.
go back to reference Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibally MB, Besansky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013;3619:246–74.CrossRefPubMed Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibally MB, Besansky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013;3619:246–74.CrossRefPubMed
29.
go back to reference Sawadogo PS, Namountougou M, Toé KH, Rouamba J, Maïga H, Ouédraogo KR, et al. Swarming behaviour in natural populations of Anopheles gambiae and An. coluzzii: review of 4 years survey in rural areas of sympatry, Burkina Faso (West Africa). Acta Trop. 2014;132:S42–52.CrossRefPubMed Sawadogo PS, Namountougou M, Toé KH, Rouamba J, Maïga H, Ouédraogo KR, et al. Swarming behaviour in natural populations of Anopheles gambiae and An. coluzzii: review of 4 years survey in rural areas of sympatry, Burkina Faso (West Africa). Acta Trop. 2014;132:S42–52.CrossRefPubMed
30.
go back to reference Koekemoer LL, Coetzee M, Hunt RH. Hpall endonuclease distinguishes between two species in the Anopheles funestus group. Insect Mol Biol. 1998;7:273–7.CrossRefPubMed Koekemoer LL, Coetzee M, Hunt RH. Hpall endonuclease distinguishes between two species in the Anopheles funestus group. Insect Mol Biol. 1998;7:273–7.CrossRefPubMed
32.
go back to reference Diabaté A, Dabire RK, Kengne P, Brengues C, Baldet T, Ouari A, et al. 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.CrossRefPubMed Diabaté A, Dabire RK, Kengne P, Brengues C, Baldet T, Ouari A, et al. 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.CrossRefPubMed
Metadata
Title
Molecular and physiological analysis of Anopheles funestus swarms in Nchelenge, Zambia
Authors
Jacek W. Zawada
Yael L. Dahan-Moss
Mbanga Muleba
Roch K. Dabire
Hamid Maïga
Nelius Venter
Craig Davies
Richard H. Hunt
Maureen Coetzee
Lizette L. Koekemoer
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2196-6

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