Abstract
Anopheles darlingi is the main malaria vector in humans in South America. In the Amazon basin, it lives along the banks of rivers and lakes, which responds to the annual hydrological cycle (dry season and rainy season). In these breeding sites, the larvae of this mosquito feed on decomposing organic and microorganisms, which can be pathogenic and trigger the activation of innate immune system pathways, such as proteins Gram-negative binding protein (GNBP). Such environmental changes affect the occurrence of polymorphic inversions especially at the heterozygote frequency, which confer adaptative advantage compared to homozygous inversions. We mapped the GNBP probe to the An. darlingi 2Rd inversion by fluorescent in situ hybridization (FISH), which was a good indicator of the GNBP immune response related to the chromosomal polymorphic inversions and adaptative evolution. To better understand the evolutionary relations and time of divergence of the GNBP of An. darlingi, we compared it with nine other mosquito GNBPs. The results of the phylogenetic analysis of the GNBP sequence between the species of mosquitoes demonstrated three clades. Clade I and II included the GNBPB5 sequence, and clade III the sequence of GNBPB1. Most of these sequences of GNBP analyzed were homologous with that of subfamily B, including that of An. gambiae (87 %), therefore suggesting that GNBP of An. darling belongs to subfamily B. This work helps us understand the role of inversion polymorphism in evolution of An. darlingi.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ananina GA, Peixoto AA, Blanche-Mathé BC, Souza WN, da Silva LB, Valente VLS, Klaczko LB (2004) Chromosomal inversion polymorphism in Drosophila mediopunctata: seasonal, altitudinal and latitudinal variation. Genet Mol Biol 97:61–69
Bridi LC, Sharakhova MV, Sharakhov IV, Cordeiro J, Azevedo Junior GM, Tadei WP, Rafael MS (2013) Chromosomal localization of actin genes in the malaria mosquito Anopheles darlingi. Med Vet Entomol 27:118–121
Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C et al (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298(5591):159–165
Clark AG, Wang L (1997) Molecular population genetics of Drosophila immune system genes. Genetics 147:713–724
Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L (2005) Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet 21:673–682
Coluzzi M (1982) Spatial distribution of chromosomal inversions and speciation in Anopheline mosquitoes. In: Barigozzi C (ed) Mechanisms of speciation. Liss, New York
Coluzzi M, Sabatini A, Petrarca V, Dideco MA (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 73:483–497
Coluzzi M, Petrarca V, Di Deco MA (1985) Chromosomal inversion intergradations and incipient speciation in Anopheles gambiae. Bollettino di Zoologia 52:45–63
Conn JA (1991) Cytogenetic analysis of the polytene chromosomes of Anopheles triannulatus (Diptera: Culicidae) from western Venezuela. Genome 34:267–272
Consoli RAGB, Lourenço-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. FIOCRUZ, Rio de Janeiro
Dimopoulos G, Richman A, Müller H-M, Kafatos FC (1997) Molecular immune response of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci USA 94:11508–11513
Dobzhansky T (1944) Chromosomal races in Drosophila pseudoobscura and Drosophila persimilis. Carnegie Inst Washington Publ 554:47–144
Forattini OP (1962) Entomologia médica. Faculdade de Saúde Pública da USP, São Paulo
Forattini OP (1987) Compartemento exofilo de Anopheles darlingi root, em regiáo meridional do Brasil. Exophilic. Rev Saúde Publ 21:291–304
French WL, Baker RH, Kitzmiller JB (1962) Preparation of mosquito chromosomes. Mosq News 22:377–383
Frizzi G, Holstein M (1956) Etude cytogenetique d’Anopheles gambiae. Bull World Health Organ 15:425–435
Guedes AS, Amorim EM, Schreiber G (1957) Análise dos cromossomos salivares em anofelinos brasileiros. Rev Bras Malar D Trop 9:247–250
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp 41:95–98
Hay SI, Sinka ME, Okara RM, Kabaria CW, Mbithi PM, Tago CT, Benz D, Gething PW, Howes RE, Patil AP, Temperley WH, Bangs MJ, Chareonviriyaphap T, Elyazar IRF, Harbach RE, Hemingway J, Manguin S, Mbogo CM, Rubio-Palis Y, Godfray HCJ (2010) Developing global maps of the dominant Anopheles vectors of human malaria. PLoS Med 7:e1000209
Hiwat H, Bretas G (2011) Ecology of Anopheles darlingi root with respect to vector importance: a review. Parasite Vector 4:177
Hoffmann AA, Danborn PJ (2007) Towards genetic markers in animal populations as biomonitors for human-induced environmental change. Ecol Lett 10:63–76
Hoffmann JA, Reichhart JM (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3:121–126
Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental changes. Nat Rev Genet 9:421–432
Hoffmann JA, Reichhart JM, Hetru C (1996) Innate immunity in higher insects. Curr Opin Immunol 8:8–13
Hoffmann AA, Sgro CM, Weeks AR (2004) Chromosomal inversion polymorphisms and adaptation. Trends Ecol Evol 19:482–488
Kamali M, Sharakhova MV, Baricheva E, Karagodin D, Tu Z, Sharakhov IV (2011) An integrated chromosome map of microsatellite markers and inversion breakpoints for an Asian malaria mosquito, Anopheles stephensi. J Hered 102(6):719–726
Kimbrell DA, Beutler B (2001) The evolution and genetics of innate immunity. Nature 2:256–267
Kitzmiller JB, Chow GW (1971) The salivary gland chromosomes of Anopheles aquasalis. Rev Bras Malariol Doencas Trop 23:65–85
Kitzmiller JB, Kreutzer RD, Tallaferro E (1973) Chromosomal differences in populations of Anopheles nuneztovari. Bull World Health Organ 48:435–445
Kreutzer RD, Kitzmiller JB, Ferreira E (1972) Inversion polymorphism in the salivary gland chromosomes of Anopheles darlingi root. Mosq News 32:555–565
Kreutzer RD, Kitzmiller JB, Rabbani MG (1975) The salivary gland chromosomes of Anopheles argyritarsis compared with those of certain other species in the subgenus Nyssorhynchus. Mosq News 35:354–365
Kumar V, Collins FH (1994) A technique for nucleic acid in situ hybridization to polytene chromosome of mosquitoes in the Anopheles gambiae complex. Insect Mol Biol 3(1):41–47
Lehmann T, Hume JCC, Licht M, Burns CS, Wollenberg K, Simard F, Ribeiro JMC (2009) Molecular evolution of immune genes in the malaria mosquito Anopheles gambiae. PLoS ONE 4(2):e4549. doi:10.1371/journal.pone.0004549
Liang J, Sharakhova MV, Lan Q, Zhu H, Sharakhov IV, Xia A (2014) A standard cytogenetic map for Anopheles sinensis and chromosome arm homology between the subgenera Anopheles and Cellia. Med Vet Entomol 28(Suppl. 1):26–32
Manoukis NC, Powell JR, Touré MB, Sacko A, Edillo FE, Coulibaly MB, Traoré SF, Taylor CE, Besansky NJ (2008) A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proc Natl Acad Sci USA 105:2940–2945
Marinotti O, Cerqueira GC, de Almeida LGP, Ferro MIT, Loreto ELS, Zaha A et al (2013) The Genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res 41(15):7387–7400
Meister M, Lemaitre B, Hoffmann JA (1997) Antimicrobial peptide defense in Drosophila. BioEssays 19:1019–1026
Mertz B, Gu X, Reilly PJ (2009) Analysis of functional divergence within two structurally related glycoside hydrolases families. Biopolymers 91(6):478–495
Ministério da Saúde—Portal da Saúde (2015) http://portalsaude.saude.gov.br/index.php?option=com_content&view=article&id=10933&Itemid=646. Accessed 26 May 2015
Moreno JE, Rubio-Palis Y, Paez E, Perez E, Sanchez V (2007) Abundance, biting behaviour and parous rate of anopheline mosquito species in relation to malaria incidence in gold-mining areas of southern Venezuela. Med Vet Entomol 21:339–349
Muller T, Vingron M (2000) Modeling amino acid replacement. J Comput Biol 7:761–776
Musset L, Pelleau S, Girord R, Ardillon V, Carvalho L, Dusfour I, Gomes MSM, Djossou F, Legrand E (2014) Malaria on the Guiana Shield: a review of the situation in French Guiana. Mem Inst Oswaldo Cruz Rio de Janeiro 109(5):525–533
Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA, Allen JE, Amon J, Arcà B et al (2015) Highly evolvable malária vectors: the genomes of 16 Anopheles mosquitoes. Science. doi:10.1126/Science.1258522
Osta MA, Christophides GK, Vlachou D, Kafatos FC (2004) Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. J Exp Biol 207:2551–2563
Peischl S, Kirkpatrick M (2012) Establishment of new mutations in changing environments. Genetics 191:895–906
Póvoa MM, Wirtz RA, Lacerda RNL, Miles MA, Warhurst D (2001) Malaria vectors in the municipality of Serra do Navio, state of Amapá, Amazon Region, Brazil. Mem Inst Oswaldo Cruz 96:179–184
Powell JR, Petrarca V, della Torre A, Caccone A, Coluzzi M (1999) Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia 41:101–113
Rafael MS, Tadei WP (1998) Metaphase karyotypes of Anopheles (Nyssorhynchus) darlingi Root and A. (N.) nuneztovari Gabaldón (Diptera: Culicidae). Genet Mol Biol 21:351–354
Rafael MS, Tadei WP, Recco-Pimentel SM (2003) Location of ribosomal genes in the chromosomes of Anopheles darlingi and Anopheles nuneztovari (Diptera, Culicidae) from the Brazilian Amazon. Mem Inst Oswaldo Cruz 98(5):629–635
Rafael MS, Tadei WP, Hunter FF (2004) The physical gene Hsp70 map on polytene chromosomes of Anopheles darlingi from the Brazilian Amazon. Genetica 121:89–94
Rafael MS, Rohde C, Bridi LC, Gaiesky VLSV, Tadei WP (2010) Salivary polytene chromosome map of Anopheles darlingi, the main vector of neotropical malaria. Am J Trop Med Hyg 83(2):241–249
Rambaut A (2014) FigTree v1.4.2. Computer program available from: http://tree.bio.ed.ac.uk/software/figtree/. Accessed 22 Oct 2015
Ramírez CCL, Dessen EMB (1994) Cytogenetic analysis of a natural population of Anopheles cruzii. Rev Bras Genet 17:41–46
Sharakhov IV, Serazin AC, Grushko OG, Dana A, Lobo N, Hillenmeyer ME, Westerman R, Romero-Severson J, Costantini C, Sagnon NF, Collins FH, Besansky NJ (2002) Inversions and gene order shuffling in Anopheles gambiae and A. funestus. Science 298:182–185
Sharakhov I, Braginets O, Grushko O, Cohuet A, Guelbeogo WM, Boccolini D, Weill M, Costantini C, Sagnon N, Fontenille D (2004) A microsatellite physical map of the African human malaria vector Anopheles funestus. J Hered 95:29–34
Sharakhova MV, Xia A, Leman SC, Sharakhov IV (2011) Arm specific dynamics of chromosome evolution in malaria mosquito. BMC Evol Biol 11:91
Slotman MA, Parmakelis A, Marshall JC, Awono-Ambene PH, Antonio-Nkondjo C, Simard F, Caccone A, Powell JR (2007) Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis. PLoS ONE 8:e793
Tadei WP, Dutary-Thatcher B (2000) Malaria vectors in the Brazilian amazon: Anopheles of the subgenus Nyssorhynchus. Rev Inst Med Trop São Paulo 42:87–94
Tadei WP, Santos JMM (1982) Biologia de anofelinos amazônicos VII. Estudo da variação de frequências das inversões cromossomicas de Anopheles darlingi Root (Diptera, Culicidae). Acta Amazônica 12(4):759–785
Tadei WP, Santos JM, Rabbani MG (1982) Biologia de anofelinos Amazônicos. V. Polimorfismo cromossômico de Anopheles darlingi Root (Diptera, Culicidae). Acta Amazonica 12:353–369
Tadei WP, Thatcher BD, Santos JM, Scarpassa VM, Rodrigues IB, Rafael MS (1998) Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg 59:325–335
Tadei WP, Passos RP, Rodrigues IB, Santos JMM, Rafael MS (2007) Indicadores entomológicos e o risco de transmissão de malária na área de abrangência do projeto PIATAM. In: Cavalcante KV, Rivas AAF, Freitas CEC (eds) Indicadores Socioambientais e Atributos de Referência para o trecho Urucu-Coari-Manaus. Rio Solimões, Amazônia, p 160
Tahar R, Boudin C, Thiery I, Bourgouin C (2002) Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J 21:6673–6680
Touré YT, Petrarca V, Traoré SF, Coulibaly A, Maïga HM, Sankaré O, Sow M, Di Deco MA, Coluzzi M (1994) Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s. str. in Mali, West Africa. Genetica 94:213–223
Walker ED, Merritt RW (1993) Bacterial enrichment in the surface microlayer of an Anopheles quadrimaculatus (Diptera: Culicidae) larval habitat. J Med Entomol 30:1050–1052
Wallace JR, Merritt RW (2004) Diel feeding periodicity of larval Anopheline mosquitoes on microorganisms and microinvertebrates: a spatial and temporal comparison of Anopheles quadrimaculatus (Diptera: Culicidae) diets in a michigan pond. J Med Entomol 41(5):853–860
Warr E, Das S, Dong Y, Dimopoulos G (2008) The Gram-negative bacteria binding protein gene family: its role in the innate imune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Mol Biol 17:39–51
Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC et al (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science. doi:10.1126/science.1139862
Wolfarth BR, Filizola N, Tadei WP, Durieux L (2013) Epidemiological analysis of malaria and its relationships with hydrological variables in four municipalities of the State of Amazonas, Brazil. Hydrol Sci J 58:1495–1504
Acknowledgments
This study was supported by Project PAPAC, Edital 020/2013, process number 1570/2013/FAPEAM awarded to MSR, and project ADAPTA II-CNPq. We thank Dr. Wanderli Pedro Tadei, CSAS, INPA and Dr. Felipe Rodrigues da Silva, Embrapa Bioinformática Agropecuária, UNICAMP, for technical support. Dr. A. Leyva helped with English translation and editing of the manuscript.
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Bridi, L.C., Rafael, M.S. GNBP domain of Anopheles darlingi: are polymorphic inversions and gene variation related to adaptive evolution?. Genetica 144, 99–106 (2016). https://doi.org/10.1007/s10709-016-9881-6
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DOI: https://doi.org/10.1007/s10709-016-9881-6