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The genome of Anopheles darlingi, the main neotropical malaria vector.

ABSTRACT: Anopheles darlingi is the principal neotropical malaria vector, responsible for more than a million cases of malaria per year on the American continent. Anopheles darlingi diverged from the African and Asian malaria vectors ?100 million years ago (mya) and successfully adapted to the New World environment. Here we present an annotated reference A. darlingi genome, sequenced from a wild population of males and females collected in the Brazilian Amazon. A total of 10 481 predicted protein-coding genes were annotated, 72% of which have their closest counterpart in Anopheles gambiae and 21% have highest similarity with other mosquito species. In spite of a long period of divergent evolution, conserved gene synteny was observed between A. darlingi and A. gambiae. More than 10 million single nucleotide polymorphisms and short indels with potential use as genetic markers were identified. Transposable elements correspond to 2.3% of the A. darlingi genome. Genes associated with hematophagy, immunity and insecticide resistance, directly involved in vector-human and vector-parasite interactions, were identified and discussed. This study represents the first effort to sequence the genome of a neotropical malaria vector, and opens a new window through which we can contemplate the evolutionary history of anopheline mosquitoes. It also provides valuable information that may lead to novel strategies to reduce malaria transmission on the South American continent. The A. darlingi genome is accessible at www.labinfo.lncc.br/index.php/anopheles-darlingi.

SUBMITTER: Marinotti O

PROVIDER: S-EPMC3753621 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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The genome of Anopheles darlingi, the main neotropical malaria vector.

Marinotti Osvaldo O Cerqueira Gustavo C GC de Almeida Luiz Gonzaga Paula LG Ferro Maria Inês Tiraboschi MI Loreto Elgion Lucio da Silva EL Zaha Arnaldo A Teixeira Santuza M R SM Wespiser Adam R AR Almeida E Silva Alexandre A Schlindwein Aline Daiane AD Pacheco Ana Carolina Landim AC Silva Artur Luiz da Costa da AL Graveley Brenton R BR Walenz Brian P BP Lima Bruna de Araujo Bde A Ribeiro Carlos Alexandre Gomes CA Nunes-Silva Carlos Gustavo CG de Carvalho Carlos Roberto CR Soares Célia Maria de Almeida CM de Menezes Claudia Beatriz Afonso CB Matiolli Cleverson C Caffrey Daniel D Araújo Demetrius Antonio M DA de Oliveira Diana Magalhães DM Golenbock Douglas D Grisard Edmundo Carlos EC Fantinatti-Garboggini Fabiana F de Carvalho Fabíola Marques FM Barcellos Fernando Gomes FG Prosdocimi Francisco F May Gemma G Azevedo Junior Gilson Martins de GM Guimarães Giselle Moura GM Goldman Gustavo Henrique GH Padilha Itácio Q M IQ Batista Jacqueline da Silva Jda S Ferro Jesus Aparecido JA Ribeiro José M C JM Fietto Juliana Lopes Rangel JL Dabbas Karina Maia KM Cerdeira Louise L Agnez-Lima Lucymara Fassarella LF Brocchi Marcelo M de Carvalho Marcos Oliveira MO Teixeira Marcus de Melo Mde M Diniz Maia Maria de Mascena Mde M Goldman Maria Helena S MH Cruz Schneider Maria Paula MP Felipe Maria Sueli Soares MS Hungria Mariangela M Nicolás Marisa Fabiana MF Pereira Maristela M Montes Martín Alejandro MA Cantão Maurício E ME Vincentz Michel M Rafael Miriam Silva MS Silverman Neal N Stoco Patrícia Hermes PH Souza Rangel Celso RC Vicentini Renato R Gazzinelli Ricardo Tostes RT Neves Rogério de Oliveira Rde O Silva Rosane R Astolfi-Filho Spartaco S Maciel Talles Eduardo Ferreira TE Urményi Turán P TP Tadei Wanderli Pedro WP Camargo Erney Plessmann EP de Vasconcelos Ana Tereza Ribeiro AT

Nucleic acids research 20130612 15

Anopheles darlingi is the principal neotropical malaria vector, responsible for more than a million cases of malaria per year on the American continent. Anopheles darlingi diverged from the African and Asian malaria vectors ∼100 million years ago (mya) and successfully adapted to the New World environment. Here we present an annotated reference A. darlingi genome, sequenced from a wild population of males and females collected in the Brazilian Amazon. A total of 10 481 predicted protein-coding g ...[more]

PMID: 23761445

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Project description:BackgroundOutdoor malaria transmission hinders malaria elimination efforts in the Amazon region and novel vector control tools are needed. Ivermectin mass drug administration (MDA) to humans kills wild Anopheles, targets outdoor-feeding vectors, and can suppress malaria parasite transmission. Laboratory investigations were performed to determine ivermectin susceptibility, sporontocidal effect and inhibition of time to re-feed for the primary Amazonian malaria vector, Anopheles darlingi.MethodsTo assess ivermectin susceptibility, various concentrations of ivermectin were mixed in human blood and fed to An. darlingi. Mosquito survival was monitored daily for 7 days and a non-linear mixed effects model with Probit analysis was used to calculate lethal concentrations of ivermectin that killed 50% (LC50), 25% (LC25) and 5% (LC5) of mosquitoes. To examine ivermectin sporonticidal effect, Plasmodium vivax blood samples were collected from malaria patients and offered to mosquitoes without or with ivermectin at the LC50, LC25 or LC5. To assess ivermectin inhibition of mosquito time to re-feed, concentrations of ivermectin predicted to occur after a single oral dose of 200 μg/kg ivermectin were fed to An. darlingi. Every day for 12 days thereafter, individual mosquitoes were given the opportunity to re-feed on a volunteer. Any mosquitoes that re-blood fed or died were removed from the study.ResultsIvermectin significantly reduced An. darlingi survivorship: 7-day-LC50 = 43.2 ng/ml [37.5, 48.6], -LC25 = 27.8 ng/ml [20.4, 32.9] and -LC5 = 14.8 ng/ml [7.9, 20.2]. Ivermectin compound was sporontocidal to P. vivax in An. darlingi at the LC50 and LC25 concentrations reducing prevalence by 22.6 and 17.1%, respectively, but not at the LC5. Oocyst intensity was not altered at any concentration. Ivermectin significantly delayed time to re-feed at the 4-h (48.7 ng/ml) and 12-h (26.9 ng/ml) concentrations but not 36-h (10.6 ng/ml) or 60-h (6.3 ng/ml).ConclusionsIvermectin is lethal to An. darlingi, modestly inhibits sporogony of P. vivax, and delays time to re-feed at concentrations found in humans up to 12 h post drug ingestion. The LC50 value suggests that a higher than standard dose (400-μg/kg) is necessary to target An. darlingi. These results suggest that ivermectin MDA has potential in the Amazon region to aid malaria elimination efforts.

Project description:BackgroundAnopheles darlingi is the most important malaria vector in the Neotropics. An understanding of A. darlingi's population structure and contemporary gene flow patterns is necessary if vector populations are to be successfully controlled. We assessed population genetic structure and levels of differentiation based on 1,376 samples from 31 localities throughout the Peruvian and Brazilian Amazon and Central America using 5-8 microsatellite loci.ResultsWe found high levels of polymorphism for all of the Amazonian populations (mean RS = 7.62, mean HO = 0.742), and low levels for the Belize and Guatemalan populations (mean RS = 4.3, mean HO = 0.457). The Bayesian clustering analysis revealed five population clusters: northeastern Amazonian Brazil, southeastern and central Amazonian Brazil, western and central Amazonian Brazil, Peruvian Amazon, and the Central American populations. Within Central America there was low non-significant differentiation, except for between the populations separated by the Maya Mountains. Within Amazonia there was a moderate level of significant differentiation attributed to isolation by distance. Within Peru there was no significant population structure and low differentiation, and some evidence of a population expansion. The pairwise estimates of genetic differentiation between Central America and Amazonian populations were all very high and highly significant (FST = 0.1859 - 0.3901, P < 0.05). Both the DA and FST distance-based trees illustrated the main division to be between Central America and Amazonia.ConclusionWe detected a large amount of population structure in Amazonia, with three population clusters within Brazil and one including the Peru populations. The considerable differences in Ne among the populations may have contributed to the observed genetic differentiation. All of the data suggest that the primary division within A. darlingi corresponds to two white gene genotypes between Amazonia (genotype 1) and Central America, parts of Colombia and Venezuela (genotype 2), and are in agreement with previously published mitochondrial COI gene sequences interpreted as incipient species. Overall, it appears that two main factors have contributed to the genetic differentiation between the population clusters: physical distance between the populations and the differences in effective population sizes among the subpopulations.

Project description:BackgroundStudies on vector behaviour should be conducted in order to evaluate the effectiveness of vector control measures on malaria protection in endemic areas of Latin America, where P. vivax predominates. This work aims to investigate the fauna of anopheline mosquitoes and verify the impact of integrated vector management in two colonization projects in the Careiro Municipality, Western Brazilian Amazon.MethodsFour mosquitoes' captures were carried out from August 2008 to March 2010, with an interval of six months between each collection. Since September 2009 a large programme to reduce the burden of malaria has started in the two communities by distribution of insecticide-treated bed nets (ITN) and intensification of indoor residual spraying (IRS). Human biting rates (HBRs), entomological inoculation rates (EIRs), malaria incidence rate (MIR) and Plasmodium carrier's prevalence were used as outcomes to estimate the impact of the control measures.ResultsA total of 3,189 anophelines were collected, belonging to 13 species. Anopheles darlingi was the predominant species in the period (42.6%), followed by Anopheles albitarsis (38.4%). An. darlingi HBRs showed a notable decreasing trend from the start to the end of the study. Conversely, An. albitarsis increased its contribution to overall HBRs throughout the study. For An. darlingi there was a significant positive correlation between HBRs and MIR (p?=?0.002). Anopheles albitarsis HBRs showed a significant negative correlation with the corresponding MIR (p?=?0.045). EIR from total anophelines and from An. darlingi and An. albitarsis presented decreasing patterns in the successive collections. Four species of anophelines (An. darlingi, An. albitarsis, Anopheles braziliensis and Anopheles nuneztovari) were naturally infected with Plasmodium, albeit at very low infection rates. There were a decrease in the MIR for both vivax and falciparum malaria and in the prevalence of Plasmodium vivax and Plasmodium falciparum carriers during the period of study.ConclusionsThere is strong evidence of association between the density of An. darlingi and the incidence of malaria in the studies sites, further highlighting the importance of this vector in malaria transmission in this region. An. darlingi susceptibility to control using ITN and IRS is likely to be high in the rural settlements studied.

Dataset Information

The genome of Anopheles darlingi, the main neotropical malaria vector.

Publications

The genome of Anopheles darlingi, the main neotropical malaria vector.

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