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      Cryptic diversity in an Atlantic Forest malaria vector from the mountains of South-East Brazil

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          Abstract

          Background

          Anopheles ( Kerteszia) cruzii is the primary vector of human and simian malarias in Brazilian regions covered by the Atlantic Rainforest. Previous studies found that An. cruzii presents high levels of behavioural, chromosomal and molecular polymorphisms, which led to the hypothesis that it may be a complex of cryptic species. Here, An. cruzii specimens were collected in five sites in South-East Brazil located at different altitudes on the inner and coastal slopes of two mountain ranges covered by Atlantic Rainforest, known as Serra do Mar and Serra da Mantiqueria. Partial sequences for two genes ( Clock and cpr) were generated and compared with previously published sequences from Florianópolis (southern Brazil). Genetic diversity was analysed with estimates of population structure ( F ST ) and haplotype phylogenetic trees in order to understand how many species of the complex may occur in this biome and how populations across the species distribution are related.

          Results

          The sequences from specimens collected at sites located on the lower coastal slopes of Serra do Mar (Guapimirim, Tinguá and Sana) clustered together in the phylogenetic analysis, while the major haplotypes from sites located on higher altitude and at the continental side of the same mountains (Bocaina) clustered with those from Serra da Mantiqueira (Itatiaia), an inner mountain range. These two An. cruzii lineages showed statistically significant genetic differentiation and fixed characters, and have high F ST values typical of between species comparisons. Finally, in Bocaina, where the two lineages occur in sympatry, we found deviations from Hardy-Weinberg equilibrium due to a deficit of heterozygotes, indicating partial reproductive isolation. These results strongly suggest that at least two distinct lineages of An. cruzii (provisorily named “Group 1” and “Group 2”) occur in the mountains of South-East Brazil.

          Conclusions

          At least two genetically distinct An. cruzii lineages occur in the Atlantic Forest covered mountains of South-East Brazil. The co-occurrence of distinct lineages of An. cruzii (possibly incipient species) in those mountains is an interesting biological phenomenon and may have important implications for malaria prevalence, Plasmodium transmission dynamics and control.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-018-2615-0) contains supplementary material, which is available to authorized users.

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          Most cited references 52

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            R: language and environment for statistical computing

             RC Team,  R Rteam,  R Team (2014)
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              Odor-mediated behavior of Afrotropical malaria mosquitoes.

              The African mosquito species Anopheles gambiae sensu lato s.l. and Anopheles funestus rank among the world's most efficient vectors of human malaria. Their unique bionomics, particularly their anthropophilic, endophagic and endophilic characters, guarantee a strong mosquito-host interaction, favorable to malaria transmission. Olfactory cues govern the various behaviors of female mosquitoes and here we review the role of semiochemicals in the life history of African malaria vectors. Recent evidence points towards the existence of human-specific kairomones affecting host-seeking A. gambiae s.l., and efforts are under way to identify the volatiles mediating this behavior. Based on examples from other Culicidae spp., it is argued that there is good reason to assume that mating, sugar feeding, and oviposition behavior in Afrotropical malaria vectors may also be mediated by semiochemicals. It is foreseen that increased knowledge of odor-mediated behaviors will be applied in the development of novel sampling techniques and possibly alternative methods of intervention to control malaria.
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                Author and article information

                Contributors
                guilhermedrdias@gmail.com
                thaistenoriosoares@gmail.com
                bfogel.biotec@gmail.com
                lourenco@ioc.fiocruz.br
                tsilva@ioc.fiocruz.br
                anpitaluga@gmail.com
                carlospinto@ccb.ufsc.br
                bernardo1963@gmail.com
                luisa.rona@imperial.ac.uk , luisa.rona@ufsc.br
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                15 January 2018
                15 January 2018
                2018
                : 11
                Affiliations
                [1 ]ISNI 0000 0001 2294 473X, GRID grid.8536.8, Universidade Federal do Rio de Janeiro, IB, PPGBBE, ; Rio de Janeiro, RJ Brazil
                [2 ]ISNI 0000 0001 2294 473X, GRID grid.8536.8, Universidade Federal do Rio de Janeiro, Polo de Xerém, ; Duque de Caxias, RJ Brazil
                [3 ]ISNI 0000 0001 0723 0931, GRID grid.418068.3, Laboratório de Biologia Molecular de Insetos, IOC, FIOCRUZ, ; Rio de Janeiro, RJ Brazil
                [4 ]ISNI 0000 0001 0723 0931, GRID grid.418068.3, Laboratório de Mosquitos Transmissores de Hematozoários, IOC, FIOCRUZ, ; Rio de Janeiro, RJ Brazil
                [5 ]ISNI 0000 0001 0723 0931, GRID grid.418068.3, Laboratório de Biologia Molecular de Parasitas e Vetores, IOC, FIOCRUZ, ; Rio de Janeiro, RJ Brazil
                [6 ]ISNI 0000 0001 2188 7235, GRID grid.411237.2, Universidade Federal de Santa Catarina, MIP, CCB, ; Florianópolis, SC Brazil
                [7 ]ISNI 0000 0001 2294 473X, GRID grid.8536.8, Departamento de Genética, , Universidade Federal do Rio de Janeiro, ; Rio de Janeiro, RJ Brazil
                [8 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Department of Life Sciences, , Imperial College London, ; London, UK
                [9 ]ISNI 0000 0001 2188 7235, GRID grid.411237.2, Universidade Federal de Santa Catarina, BEG, CCB, ; Florianópolis, SC Brazil
                [10 ]ISNI 0000 0001 2294 473X, GRID grid.8536.8, Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM, CNPq), ; Rio de Janeiro, RJ Brazil
                Article
                2615
                10.1186/s13071-018-2615-0
                5769553
                29335015
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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                © The Author(s) 2018

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