Microevolution of Aedes aegypti

PLOS ONE, Sep 2015

Scientific research into the epidemiology of dengue frequently focuses on the microevolution and dispersion of the mosquito Aedes aegypti. One of the world’s largest urban agglomerations infested by Ae. aegypti is the Brazilian megalopolis of Sao Paulo, where >26,900 cases of dengue were reported until June 2015. Unfortunately, the dynamics of the genetic variability of Ae. aegypti in the Sao Paulo area have not been well studied. To reduce this knowledge gap, we assessed the morphogenetic variability of a population of Ae. aegypti from a densely urbanised neighbourhood of Sao Paulo. We tested if allelic patterns could vary over a short term and if wing shape could be a predictor of the genetic variation. Over a period of 14 months, we examined the variation of genetic (microsatellites loci) and morphological (wing geometry) markers in Ae. aegypti. Polymorphisms were detected, as revealed by the variability of 20 microsatellite loci (115 alleles combined; overall Fst = 0.0358) and 18 wing landmarks (quantitative estimator Qst = 0.4732). These levels of polymorphism are higher than typically expected to an exotic species. Allelic frequencies of the loci changed over time and temporal variation in the wing shape was even more pronounced, permitting high reclassification levels of chronological samples. In spite of the fact that both markers underwent temporal variation, no correlation was detected between their dynamics. We concluded that microevolution was detected despite the short observational period, but the intensities of change of the markers were discrepant. Wing shape failed from predicting allelic temporal variation. Possibly, natural selection (Qst>Fst) or variance of expressivity of wing phenotype are involved in this discrepancy. Other possibly influential factors on microevolution of Ae. aegypti are worth searching. Additionally, the implications of the rapid evolution and high polymorphism of this mosquito vector on the efficacy of control methods have yet to be investigated.

Microevolution of Aedes aegypti

RESEARCH ARTICLE Microevolution of Aedes aegypti Caroline Louise1,2, Paloma Oliveira Vidal1,3, Lincoln Suesdek1,2* 1 Laboratório Parasitologia, Instituto Butantan, São Paulo, SP, Brasil, 2 Programa de Pós-Graduação em Medicina Tropical, Instituto de Medicina Tropical, Universidade de São Paulo, São Paulo, SP, Brasil, 3 Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, Brasil * Abstract a11111 OPEN ACCESS Citation: Louise C, Vidal PO, Suesdek L (2015) Microevolution of Aedes aegypti. PLoS ONE 10(9): e0137851. doi:10.1371/journal.pone.0137851 Editor: Pedro L. Oliveira, Universidade Federal do Rio de Janeiro, BRAZIL Received: September 19, 2014 Accepted: August 23, 2015 Published: September 11, 2015 Copyright: © 2015 Louise et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This research was supported by FAPESP Grants 2011/18962-8 (CL) and 2010/15039-1 (POV) and CAPES Grants #23038.005274/2011-24 and #1275/2011. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Scientific research into the epidemiology of dengue frequently focuses on the microevolution and dispersion of the mosquito Aedes aegypti. One of the world’s largest urban agglomerations infested by Ae. aegypti is the Brazilian megalopolis of Sao Paulo, where >26,900 cases of dengue were reported until June 2015. Unfortunately, the dynamics of the genetic variability of Ae. aegypti in the Sao Paulo area have not been well studied. To reduce this knowledge gap, we assessed the morphogenetic variability of a population of Ae. aegypti from a densely urbanised neighbourhood of Sao Paulo. We tested if allelic patterns could vary over a short term and if wing shape could be a predictor of the genetic variation. Over a period of 14 months, we examined the variation of genetic (microsatellites loci) and morphological (wing geometry) markers in Ae. aegypti. Polymorphisms were detected, as revealed by the variability of 20 microsatellite loci (115 alleles combined; overall Fst = 0.0358) and 18 wing landmarks (quantitative estimator Qst = 0.4732). These levels of polymorphism are higher than typically expected to an exotic species. Allelic frequencies of the loci changed over time and temporal variation in the wing shape was even more pronounced, permitting high reclassification levels of chronological samples. In spite of the fact that both markers underwent temporal variation, no correlation was detected between their dynamics. We concluded that microevolution was detected despite the short observational period, but the intensities of change of the markers were discrepant. Wing shape failed from predicting allelic temporal variation. Possibly, natural selection (Qst>Fst) or variance of expressivity of wing phenotype are involved in this discrepancy. Other possibly influential factors on microevolution of Ae. aegypti are worth searching. Additionally, the implications of the rapid evolution and high polymorphism of this mosquito vector on the efficacy of control methods have yet to be investigated. Introduction Aedes (Stegomyia) aegypti Linnaeus 1762 is a widely distributed mosquito vector of dengue, the most important arboviral disease in humans. The prevention and control of the dengue virus currently depend on controlling its mosquito vector. Different methods have been PLOS ONE | DOI:10.1371/journal.pone.0137851 September 11, 2015 1 / 16 Microevolution of Ae. aegypti proposed for dengue vector control, but many of these methods are limited by the microevolution of mosquitoes. In this context, the demography, dispersion, and evolution of these insects within urban areas have been frequently investigated. Additionally, these biological issues are of importance to professionals engaged in vector control and surveillance initiatives but are far from being satisfactorily understood. Dispersal is preferably estimated by population genetics indicators, such as gene flow, migration and genetic variability, given the difficulty and low reproducibility of mark-release-recapture methods for small mosquitoes [1–3]. Genotypic markers such as Single Nucleotide Polymorphisms (SNPs) and microsatellite loci have been largely used to investigate the microevolution of Ae. aegypti throughout the world [4–8], but the changes in the rates of allelic frequencies are variable and unique to each study case. Phenotypes may also help to describe microevolution, as in the example of wing geometry. Wing shape in insects is heritable and evolutionarily informative [9, 10]. Wing morphometrics alone were sensitive enough to detect microevolution and geographical variation in species of Aedes [10–12]. Despite the usefulness of microsatellite loci and wing shape, these markers have been seldom combined in a single study of biological patterns of Aedes spp. [12], and as far as we know, they have not been associated in microevolutionary investigations. After the publication of Vidal and Suesdek [12] and Vidal et al. [10], we formulated the following related hypotheses: 1) allelic profiles of Ae. aegypti changes over short evolutionary time periods; 2) genetic microevolution can be assessed based on wing phenotype. To test these hypotheses, we evaluated the temporal morphogenetic variations of a single population of Ae. aegypti over 14 months using microsatellites and wing geometry as biological markers. The chosen population came from "Subprefeitura Butanta", a small, homogeneous and densely urbanised neighbourhood of Sao Paulo City (Brazil). Globally, this city is one of the largest urban agglomerations infested by Ae. aegypti, with approximately 11,000,000 people distributed over an area of 1,523 sq. km. There were 31,101 cases of dengue reported in this City in 2014, and more than 26,900 cases were reported from January to June 2015 [13]. Materials and Methods Specimen collection Eggs, pupae and larvae of Ae. aegypti were collected in “Subprefeitura Butanta”, a relatively small, geopolitically delimited neighbourhood comprising approximately 3% of the Sao Paulo municipality, which is homogeneously and densely urbanised (visualisation available at https:// www.google.com.br/maps). Specimens were obtained from six traps placed throughout the neighbourhood (see map in Fig 1). Each trap consisted of grouped water containers comprising ~1 L volume. SUVIS is a governmental entity which helped us in the field collecting and it has a permanent authorization to collect in the private properties wher (...truncated)


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Caroline Louise, Paloma Oliveira Vidal, Lincoln Suesdek. Microevolution of Aedes aegypti, PLOS ONE, 2015, 9, DOI: 10.1371/journal.pone.0137851