Genetic Diversity of Brazilian Aedes aegypti: Patterns following an Eradication Program

Background Aedes aegypti is the most important vector of dengue fever in Brazil, where severe epidemics have recently taken place. Ae. aegypti in Brazil was the subject of an intense eradication program in the 1940s and 50s to control yellow fever. Brazil was the largest country declared free of this mosquito by the Pan-American Health Organization in 1958. Soon after relaxation of this program, Ae. aegypti reappeared in this country, and by the early 1980s dengue fever had been reported. The aim of this study is to analyze the present-day genetic patterns of Ae. aegypti populations in Brazil. Methodology/Principal Findings We studied the genetic variation in samples of 11 widely spread populations of Ae. aegypti in Brazil based on 12 well-established microsatellite loci. Our principal finding is that present-day Brazilian Ae. aegypti populations form two distinct groups, one in the northwest and one in the southeast of the country. These two groups have genetic affinities to northern South American countries and the Caribbean, respectively. This is consistent with what has been reported for other genetic markers such as mitochondrial DNA and allele frequencies at the insecticide resistance gene, kdr. Conclusions/Significance We conclude that the genetic patterns in present day populations of Ae. aegypti in Brazil are more consistent with a complete eradication of the species in the recent past followed by re-colonization, rather than the alternative possibility of expansion from residual pockets of refugia. At least two colonizations are likely to have taken place, one from northern South American countries (e.g., Venezuela) that founded the northwestern group, and one from the Caribbean that founded the southeastern group. The proposed source areas were never declared free of Ae. aegypti.

[1]  Correction: Genetic Diversity of Brazilian Aedes aegypti: Patterns following an Eradication Program , 2014, PLoS Neglected Tropical Diseases.

[2]  Hongyu Zhao,et al.  HUMAN IMPACTS HAVE SHAPED HISTORICAL AND RECENT EVOLUTION IN AEDES AEGYPTI, THE DENGUE AND YELLOW FEVER MOSQUITO , 2014, Evolution; international journal of organic evolution.

[3]  N. Beebe,et al.  Microsatellite and mitochondrial markers reveal strong gene flow barriers for Anopheles farauti in the Solomon Archipelago: implications for malaria vector control , 2014, International journal for parasitology.

[4]  J. Linss,et al.  Distribution and dissemination of the Val1016Ile and Phe1534Cys Kdr mutations in Aedes aegypti Brazilian natural populations , 2014, Parasites & Vectors.

[5]  John S. Brownstein,et al.  The global distribution and burden of dengue , 2013, Nature.

[6]  E. McGraw,et al.  Beyond insecticides: new thinking on an ancient problem , 2013, Nature Reviews Microbiology.

[7]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[8]  P. Ribolla,et al.  Gene flow networks among American Aedes aegypti populations , 2012, Evolutionary applications.

[9]  J. Pinto,et al.  Seasonal population dynamics and the genetic structure of the mosquito vector Aedes aegypti in São Paulo, Brazil , 2012, Ecology and evolution.

[10]  G. Dayan,et al.  The history of dengue outbreaks in the Americas. , 2012, The American journal of tropical medicine and hygiene.

[11]  C. Struchiner,et al.  Why do we need alternative tools to control mosquito-borne diseases in Latin America? , 2012, Memorias do Instituto Oswaldo Cruz.

[12]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[13]  Duane J. Gubler,et al.  The Economic Burden of Dengue , 2012, The American journal of tropical medicine and hygiene.

[14]  Alongkot Ponlawat,et al.  Worldwide patterns of genetic differentiation imply multiple ‘domestications’ of Aedes aegypti, a major vector of human diseases , 2011, Proceedings of the Royal Society B: Biological Sciences.

[15]  L. Field,et al.  Gene amplification and insecticide resistance. , 2011, Pest management science.

[16]  T. Sakurai,et al.  Multiple origins of outbreak populations of a native insect pest in an agro-ecosystem , 2010, Bulletin of Entomological Research.

[17]  Rosanna W. Peeling,et al.  Dengue: a continuing global threat , 2010, Nature Reviews Microbiology.

[18]  M. G. Castro,et al.  Seasonal dynamics of Aedes aegypti (Diptera: Culicidae) in the northernmost state of Brazil: a likely port-of-entry for dengue virus 4. , 2009, Memorias do Instituto Oswaldo Cruz.

[19]  J. Linss,et al.  Voltage-gated sodium channel polymorphism and metabolic resistance in pyrethroid-resistant Aedes aegypti from Brazil. , 2009, The American journal of tropical medicine and hygiene.

[20]  J. Carlsson Effects of microsatellite null alleles on assignment testing. , 2008, The Journal of heredity.

[21]  A. Estoup,et al.  Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles , 2008, Molecular ecology.

[22]  V. M. Scarpassa,et al.  Population genetics and phylogeography of Aedes aegypti (Diptera: Culicidae) from Brazil. , 2008, The American journal of tropical medicine and hygiene.

[23]  F. Naveca,et al.  Dengue Virus Type 4, Manaus, Brazil , 2008, Emerging infectious diseases.

[24]  F. Herrera,et al.  Genetic relationships among Aedes aegypti collections in Venezuela as determined by mitochondrial DNA variation and nuclear single nucleotide polymorphisms. , 2008, The American journal of tropical medicine and hygiene.

[25]  F. Rousset genepop’007: a complete re‐implementation of the genepop software for Windows and Linux , 2008, Molecular ecology resources.

[26]  Ima Aparecida Braga,et al.  Aedes aegypti: inseticidas, mecanismos de ação e resistência , 2007 .

[27]  A. Martins,et al.  Insecticide resistance mechanisms of Brazilian Aedes aegypti populations from 2001 to 2004. , 2007, The American journal of tropical medicine and hygiene.

[28]  M. Capurro,et al.  Genetic Variability of Aedes Aegypti in the Americas Using a Mitochondrial Gene: Evidence of Multiple Introductions , 2022 .

[29]  R. Lourenço-de-Oliveira,et al.  Low gene flow of Aedes aegypti between dengue-endemic and dengue-free areas in southeastern and southern Brazil. , 2007, The American journal of tropical medicine and hygiene.

[30]  Noah A. Rosenberg,et al.  CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure , 2007, Bioinform..

[31]  Ralf Nauen,et al.  Insecticide resistance in disease vectors of public health importance. , 2007, Pest management science.

[32]  Ima Aparecida Braga,et al.  Aedes aegypti: histórico do controle no Brasil , 2007 .

[33]  A. Estoup,et al.  Microsatellite null alleles and estimation of population differentiation. , 2007, Molecular biology and evolution.

[34]  R. Lourenço-de-Oliveira,et al.  Higher genetic variation estimated by microsatellites compared to isoenzyme markers in Aedes aegypti from Rio de Janeiro. , 2006, Memorias do Instituto Oswaldo Cruz.

[35]  James W. Jones,et al.  Polymorphic microsatellite markers for studies of Aedes aegypti (Diptera: Culicidae), the vector of dengue and yellow fever , 2006 .

[36]  R. Lourenço-de-Oliveira,et al.  Geographic and temporal genetic patterns of Aedes aegypti populations in Rio de Janeiro, Brazil , 2006, Tropical medicine & international health : TM & IH.

[37]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[38]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[39]  W. Brogdon,et al.  Monitoring of resistance to the pyrethroid cypermethrin in Brazilian Aedes aegypti (Diptera: Culicidae) populations collected between 2001 and 2003. , 2005, Memorias do Instituto Oswaldo Cruz.

[40]  S. Kelley,et al.  Isolation by distance, web service , 2005, BMC Genetics.

[41]  S. Kalinowski hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness , 2005 .

[42]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[43]  A. Solé-Cava,et al.  Genetic structure of natural populations of Aedes aegypti at the micro- and macrogeographic levels in Brazil. , 2004, Journal of the American Mosquito Control Association.

[44]  J. Cornuet,et al.  GENECLASS2: a software for genetic assignment and first-generation migrant detection. , 2004, The Journal of heredity.

[45]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[46]  S. Kalinowski Counting Alleles with Rarefaction: Private Alleles and Hierarchical Sampling Designs , 2004, Conservation Genetics.

[47]  N. Rosenberg distruct: a program for the graphical display of population structure , 2003 .

[48]  A. Solé-Cava,et al.  Genetic Differentiation of Aedes aegypti (Diptera: Culicidae), the Major Dengue Vector in Brazil , 2003, Journal of medical entomology.

[49]  D. Gubler Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. , 2002, Trends in microbiology.

[50]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[51]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[52]  J. L. Montagne,et al.  Emerging infectious diseases. , 1994, The Journal of infectious diseases.

[53]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[54]  P. Ribolla,et al.  Mitochondrial DNA Polymorphism and Heteroplasmy in Populations of Aedes aegypti in Brazil , 2008, Journal of medical entomology.

[55]  S. Halstead,et al.  Dengue virus-mosquito interactions. , 2008, Annual review of entomology.

[56]  May R Berenbaum,et al.  Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. , 2007, Annual review of entomology.

[57]  P. Ribolla,et al.  Genetic variability in geographical populations of Aedes aegypti (Diptera, Culicidae) in Brazil elucidated by molecular markers , 2006 .

[58]  R. Lourenço-de-Oliveira,et al.  Aedes aegypti in Brazil: genetically differentiated populations with high susceptibility to dengue and yellow fever viruses. , 2004, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[59]  S. Rodrigues,et al.  Aedes aegypti, Dengue and Re-urbanization of Yellow Fever in Brazil and other South American Countries - Past and Present Situation and Future Perspectives , 1999 .

[60]  The feasibility of eradicating Aedes aegypti in the Americas. , 1997, Revista panamericana de salud publica = Pan American journal of public health.

[61]  F. Bonhomme,et al.  GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. , 1996 .

[62]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[63]  O. P. Forattini,et al.  Principais mosquitos de importância sanitária no Brasil , 1995 .

[64]  A. Risterucci,et al.  Molecular Sciences Isolation and Characterization of Twelve Polymorphic Microsatellite Loci for the Cocoa Mirid Bug Sahlbergella Singularis , 2022 .