CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES >
Olfactory perception and sex determination of vector mosquitoes
Received date: 2020-12-07
Revised date: 2021-01-08
Online published: 2021-03-10
Supported by
National Key R&D Program of China(2020YFC1200100);National Natural Science Foundation of China(31830087);National Natural Science Foundation of China(81829004);National Institutes of Health, USA(AI136850);Guangzhou Synergy Innovation Key Program for Health(201807010005);Guangzhou Synergy Innovation Key Program for Health(201803040006)
Mosquitoe is a type of important vector organism. Female mosquitoes can transmit various infectious diseases such as malaria, dengue fever, and epidemic encephalitis B, through sucking blood. Mosquito olfactory perception and sex determination are essential for reproducing and transmitting pathogens and often critical for control of mosquito population density and mosquito-borne diseases. Herein, we review the basic functions, mechanisms, and research advances on olfactory perception and sex determination of vector mosquitoes, in order to provide reference for controlling mosquito population density and mosquito-borne diseases.
Key words： Mosquito; Olfactory perception; Sex determination; Vector control
Tong LIU , Yang WU , Pei-wen LIU , Wen-qiang YANG , Bin-bin JIN , Jin-bao GU , Xiao-guang CHEN . Olfactory perception and sex determination of vector mosquitoes[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021 , 39(1) : 1 -7 . DOI: 10.12140/j.issn.1000-7423.2021.01.001
| [1] | Liu C, Pitts RJ, Bohbot JD, et al. Distinct olfactory signaling mechanisms in the malaria vector mosquito Anopheles gambiae[J]. PLoS Biol, 2010,8(8):e1000467. |
| [2] | Lutz EK, Lahondère C, Vinauger C, et al. Olfactory learning and chemical ecology of olfaction in disease vector mosquitoes: a life history perspective[J]. Curr Opin Insect Sci, 2017,20:75-83. |
| [3] | Chadee DD, Sutherland JM, Gilles JRL. Diel sugar feeding and reproductive behaviours of Aedes aegypti mosquitoes in Trinidad: with implications for mass release of sterile mosquitoes[J]. Acta Trop, 2014,132:S86-S90. |
| [4] | Barredo E, DeGennaro M. Not just from blood: mosquito nutrient acquisition from nectar sources[J]. Trends Parasitol, 2020,36(5):473-484. |
| [5] | Vargo AM, Foster WA. Responsiveness of female Aedes aegypti (Diptera : Culicidae) to flower extracts[J]. J Med Entomol, 1982,19(6):710-718. |
| [6] | Mauer DJ, Rowley WA. Attraction of Culex pipiens pipiens (Diptera : Culicidae) to flower volatiles[J]. J Med Entomol, 1999,36(4):503-507. |
| [7] | Otienoburu PE, Ebrahimi B, Phelan PL, et al. Analysis and optimization of a synthetic milkweed floral attractant for mosquitoes[J]. J Chem Ecol, 2012,38(7):873-881. |
| [8] | Nyasembe VO, Torto B. Volatile phytochemicals as mosquito semiochemicals[J]. Phytochem Lett, 2014,8:196-201. |
| [9] | Yu BT, Hu Y, Ding YM, et al. Feeding on different attractive flowering plants affects the energy reserves of Culex pipiens pallens adults[J]. Parasitol Res, 2018,117(1):67-73. |
| [10] | Gouagna LC, Kerampran R, Lebon C, et al. Sugar-source preference, sugar intake and relative nutritional benefits in Anopheles arabiensis males[J]. Acta Trop, 2014,132:S70-S79. |
| [11] | Hapairai LK, Joseph H, Sang MA, et al. Field evaluation of selected traps and lures for monitoring the filarial and arbovirus vector, Aedes polynesiensis (Diptera : Culicidae), in French Polynesia[J]. J Med Entomol, 2013,50(4):731-739. |
| [12] | Li Y, Su X, Zhou G, et al. Comparative evaluation of the efficiency of the BG-Sentinel trap, CDC light trap and Mosquito-oviposition trap for the surveillance of vector mosquitoes[J]. Parasit Vectors, 2016,9(1):446. |
| [13] | Takken W, Costantini C, Dolo G, et al. Mosquito mating behaviour[M] //Bridging laboratory and field research for genetic control of disease vectors. Dordrecht: Springer Netherlands, 2006: 183-188. |
| [14] | Pitts RJ, Mozūraitis R, Gauvin-Bialecki A, et al. The roles of kairomones, synomones and pheromones in the chemically-mediated behaviour of male mosquitoes[J]. Acta Trop, 2014,132:S26-S34. |
| [15] | Cabrera M, Jaffe K. An aggregation pheromone modulates lekking behavior in the vector mosquito Aedes aegypti (Diptera : Culicidae)[J]. J Am Mosq Control Assoc, 2007,23(1):1-10. |
| [16] | Fawaz EY, Allan SA, Bernier UR, et al. Swarming mechanisms in the yellow fever mosquito: aggregation pheromones are involved in the mating behavior of Aedes aegypti[J]. J Vector Ecol, 2014,39(2):347-354. |
| [17] | Anton S, van Loon JJ, Meijerink J, et al. Central projections of olfactory receptor neurons from single antennal and palpal sensilla in mosquitoes[J]. Arthropod Struct Dev, 2003,32(4):319-327. |
| [18] | Seenivasagan T, Sharma KR, Shrivastava A, et al. Surface morphology and morphometric analysis of sensilla of Asian tiger mosquito, Aedes albopictus (Skuse): an SEM investigation[J]. J Vector Borne Dis, 2009,46(2):125-135. |
| [19] | Matthews BJ, McBride CS, DeGennaro M, et al. The neurotranscriptome of the Aedes aegypti mosquito[J]. BMC Genom, 2016,17:32. |
| [20] | Yan H, Jafari S, Pask G, et al. Evolution, developmental expression and function of odorant receptors in insects[J]. J Exp Biol, 2020, 223(pt suppl 1): jeb208215. |
| [21] | Gomez-Diaz C, Martin F, Garcia-Fernandez JM, et al. The two main olfactory receptor families in drosophila, ORs and IRs: a comparative approach[J]. Front Cell Neurosci, 2018,12:253. |
| [22] | Leal WS. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes[J]. Annu Rev Entomol, 2013,58:373-391. |
| [23] | Carey AF, Wang GR, Su CY, et al. Odorant reception in the malaria mosquito Anopheles gambiae[J]. Nature, 2010,464(7285):66-71. |
| [24] | Carraher C, Dalziel J, Jordan MD, et al. Towards an understanding of the structural basis for insect olfaction by odorant receptors[J]. Insect Biochem Mol Biol, 2015,66:31-41. |
| [25] | Wang GR, Carey AF, Carlson JR, et al. Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae[J]. Proc Natl Acad Sci USA, 2010,107(9):4418-4423. |
| [26] | Chen XG, Jiang X, Gu J, et al. Genome sequence of the Asian tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution[J]. Proc Natl Acad Sci USA, 2016,113(4):E489. |
| [27] | Matthews BJ, Dudchenko O, Kingan SB, et al. Improved reference genome of Aedes aegypti informs arbovirus vector control[J]. Nature, 2018,563(7732):501-507. |
| [28] | Liu H, Liu T, Xie L, et al. Functional analysis of Orco and odorant receptors in odor recognition in Aedes albopictus[J]. Parasit Vectors, 2016,9(1):363. |
| [29] | Xu PX, Choo YM, de la Rosa A, et al. Mosquito odorant receptor for DEET and methyl jasmonate[J]. Proc Natl Acad Sci USA, 2014,111(46):16592-16597. |
| [30] | Jones PL, Pask GM, Rinker DC, et al. Functional agonism of insect odorant receptor ion channels[J]. Proc Natl Acad Sci USA, 2011,108(21):8821-8825. |
| [31] | DeGennaro M, McBride CS, Seeholzer L, et al. Orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET[J]. Nature, 2013,498(7455):487-491. |
| [32] | Raji JI, Melo N, Castillo JS, et al. Aedes aegypti mosquitoes detect acidic volatiles found in human odor using the IR8a pathway[J]. Curr Biol, 2019, 29(8): 1253-1262.e7. |
| [33] | Hallem EA, Nicole Fox A, Zwiebel LJ, et al. Olfaction: mosquito receptor for human-sweat odorant[J]. Nature, 2004,427(6971):212-213. |
| [34] | Pitts RJ, Derryberry SL, Zhang Z, et al. Variant ionotropic receptors in the malaria vector mosquito Anopheles gambiae tuned to amines and carboxylic acids[J]. Sci Rep, 2017,7:40297. |
| [35] | Thireou T, Kythreoti G, Tsitsanou KE, et al. Identification of novel bioinspired synthetic mosquito repellents by combined ligand-based screening and OBP-structure-based molecular docking[J]. Insect Biochem Mol Biol, 2018,98:48-61. |
| [36] | Kr?ber T, Koussis K, Bourquin M, et al. Odorant-binding protein-based identification of natural spatial repellents for the African malaria mosquito Anopheles gambiae[J]. Insect Biochem Mol Biol, 2018,96:36-50. |
| [37] | Deng Y, Yan H, Gu J, et al. Molecular and functional characterization of odorant-binding protein genes in an invasive vector mosquito, Aedes albopictus[J]. PLoS One, 2013,8(7):e68836. |
| [38] | McBride CS, Baier F, Omondi AB, et al. Evolution of mosquito preference for humans linked to an odorant receptor[J]. Nature, 2014,515(7526):222-227. |
| [39] | Wu Q, Li CX, Liu QM, et al. RNA interference of odorant receptor CquiOR114/117 affects blood-feeding behavior in Culex quinquefasciatus[J]. Acta Trop, 2020,204:105343. |
| [40] | Pelletier J, Guidolin A, Syed Z, et al. Knockdown of a mosquito odorant-binding protein involved in the sensitive detection of oviposition attractants[J]. J Chem Ecol, 2010,36(3):245-248. |
| [41] | Yin J, Choo YM, Duan H, et al. Selectivity of odorant-binding proteins from the southern house mosquito tested against physiologically relevant ligands[J]. Front Physiol, 2015,6:56. |
| [42] | Wang Y, Li TT, Gong MQ. Advances in research on olfactory receptors of mosquitoes[J]. Chin J Parasitol Parasit Dis, 2020,38(5):647-652. (in Chinese) |
| [42] | ( 王洋, 李婷婷, 公茂庆. 蚊虫嗅觉受体研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020,38(5):647-652.) |
| [43] | Schorkopf DL, Spanoudis CG, Mboera LE, et al. Combining attractants and larvicides in biodegradable matrices for sustainable mosquito vector control[J]. PLoS Negl Trop Dis, 2016,10(10):e0005043. |
| [44] | Wondwosen B, Birgersson G, Tekie H, et al. Sweet attraction: sugarcane pollen-associated volatiles attract gravid Anopheles arabiensis[J]. Malar J, 2018,17(1):90. |
| [45] | Xie L, Yang W, Liu H, et al. Enhancing attraction of the vector mosquito Aedes albopictus by using a novel synthetic odorant blend[J]. Parasit Vectors, 2019,12(1):382. |
| [46] | Batista EPA, Ngowo H, Opiyo M, et al. Field evaluation of the BG-Malaria trap for monitoring malaria vectors in rural Tanzanian villages[J]. PLoS One, 2018,13(10):e0205358. |
| [47] | MacKay AJ, Amador M, Barrera R. An improved autocidal gravid ovitrap for the control and surveillance of Aedes aegypti[J]. Parasit Vectors, 2013,6:225. |
| [48] | Stanczyk NM, Brookfield JF, Ignell R, et al. Behavioral insensitivity to DEET in Aedes aegypti is a genetically determined trait residing in changes in sensillum function[J]. Proc Natl Acad Sci USA, 2010,107(19):8575-8580. |
| [49] | Verhulst EC, van de Zande L, Beukeboom LW. Insect sex determination: it all evolves around transformer[J]. Curr Opin Genet Dev, 2010,20(4):376-383. |
| [50] | Day J. Mosquito oviposition behavior and vector control[J]. Insects, 2016,7(4):65. |
| [51] | Hall AB, Qi YM, Timoshevskiy V, et al. Six novel Y chromosome genes in Anopheles mosquitoes discovered by independently sequencing males and females[J]. BMC Genom, 2013,14:273. |
| [52] | Krzywinska E, Dennison NJ, Lycett GJ, et al. A maleness gene in the malaria mosquito Anopheles gambiae[J]. Science, 2016,353(6294):67-69. |
| [53] | Criscione F, Qi Y, Tu Z. GUY1 confers complete female lethality and is a strong candidate for a male-determining factor in Anopheles stephensi[J]. Elife, 2016,5. |
| [54] | Qi Y, Wu Y, Saunders R, et al. Guy1, a Y-linked embryonic signal, regulates dosage compensation in Anopheles stephensi by increasing X gene expression[J]. Elife, 2019,8. |
| [55] | Hall AB, Basu S, Jiang X, et al. Sex determination. A male-determining factor in the mosquito Aedes aegypti[J]. Science, 2015,348(6240):1268-1270. |
| [56] | Aryan A, Anderson MAE, Biedler JK, et al. Nix alone is sufficient to convert female Aedes aegypti into fertile males and myo-sex is needed for male flight[J]. Proc Natl Acad Sci USA, 2020,117(30):17702-17709. |
| [57] | Gomulski LM, Mariconti M, Di Cosimo A, et al. The Nix locus on the male-specific homologue of chromosome 1 in Aedes albopictus is a strong candidate for a male-determining factor[J]. Parasit Vectors, 2018,11(suppl 2):647. |
| [58] | Liu PW, Jin BB, Li XC, et al. Nix is a male-determining factor in the Asian tiger mosquito Aedes albopictus[J]. Insect Biochem Mol Biol, 2020,118:103311. |
| [59] | Jost E, Laven H. Meiosis in translocation heterozygotes in the mosquito Culex pipiens[J]. Chromosoma, 1971,35(2):184-205. |
| [60] | Baker RH, Sakai RK. Triploids and male determination in the mosquito, Anopheles culicifacies[J]. J Hered, 1979,70(5):345-346. |
| [61] | Ferdig MT, Taft AS, Severson DW, et al. Development of a comparative genetic linkage map for Armigeres subalbatus using Aedes aegypti RFLP markers[J]. Genome Res, 1998,8(1):41-47. |
| [62] | Newton ME, Southern DI, Wood RJ. X and Y chromosomes of Aedes aegypti (L.) distinguished by Giemsa C-banding[J]. Chromosoma, 1974,49(1):41-49. |
| [63] | Toups MA, Hahn MW. Retrogenes reveal the direction of sex-chromosome evolution in mosquitoes[J]. Genetics, 2010,186(2):763-766. |
| [64] | Motara MA, Rai KS. Chromosomal differentiation in two species of Aedes and their hybrids revealed by Giemsa C-banding[J]. Chromosoma, 1977,64(2):125-132. |
| [65] | Mori A, Tomita T, Hidoh O, et al. Comparative linkage map development and identification of an autosomal locus for insensitive acetylcholinesterase-mediated insecticide resistance in Culex tritaeniorhynchus[J]. Insect Mol Biol, 2001,10(3):197-203. |
| [66] | Malcolm CA, Bourguet D, Ascolillo A, et al. A sex-linked Ace gene, not linked to insensitive acetylcholinesterase-mediated insecticide resistance in Culex pipiens[J]. Insect Mol Biol, 1998,7(2):107-120. |
| [67] | Reidenbach KR, Cook S, Bertone MA, et al. Phylogenetic analysis and temporal diversification of mosquitoes (Diptera : Culicidae) based on nuclear genes and morphology[J]. BMC Evol Biol, 2009,9:298. |
| [68] | Krzywinski J, Grushko OG, Besansky NJ. Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution[J]. Mol Phylogenetics Evol, 2006,39(2):417-423. |
| [69] | Wang J, Na JK, Yu Q, et al. Sequencing Papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution[J]. Proc Natl Acad Sci USA, 2012,109(34):13710-13715. |
| [70] | Hall AB, Papathanos PA, Sharma A, et al. Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes[J]. Proc Natl Acad Sci USA, 2016,113(15):E2114-E2123. |
| [71] | Criscione F, Qi Y, Saunders R, et al. A unique Y gene in the Asian malaria mosquito Anopheles stephensi encodes a small lysine-rich protein and is transcribed at the onset of embryonic development[J]. Insect Mol Biol, 2013,22(4):433-441. |
| [72] | Salz H, Erickson JW. Sex determination in Drosophila: the view from the top[J]. Fly, 2010,4(1):60-70. |
| [73] | Biedler JK, Tu Z. Sex determination in mosquitoes[J]. Adv Insect Physiol, 2016,51:37-66. |
| [74] | Salvemini M, D’Amato R, Petrella V, et al. The orthologue of the fruitfly sex behaviour gene fruitless in the mosquito Aedes aegypti: evolution of genomic organisation and alternative splicing[J]. PLoS One, 2013,8(2):e48554. |
| [75] | Scali C, Catteruccia F, Li Q, et al. Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene[J]. J Exp Biol, 2005,208(pt 19):3701-3709. |
| [76] | Zheng X, Zhang D, Li Y, et al. Incompatible and sterile insect techniques combined eliminate mosquitoes[J]. Nature, 2019,572(7767):56-61. |
| [77] | Hammond A, Galizi R, Kyrou K, et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae[J]. Nat Biotechnol, 2016,34(1):78-83. |
| [78] | Eckhoff PA, Wenger EA, Godfray HC, et al. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics[J]. Proc Natl Acad Sci USA, 2017,114(2):E255-E264. |
| [79] | Crawford JE, Clarke DW, Criswell V, et al. Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations[J]. Nat Biotechnol, 2020,38(4):482-492. |
| [80] | Mains JW, Brelsfoard CL, Rose RI, et al. Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes[J]. Sci Rep, 2016,6:33846. |
| [81] | Kyrou K, Hammond AM, Galizi R, et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes[J]. Nat Biotechnol, 2018,36(11):1062-1066. |
/
| 〈 |
|
〉 |