Vector competence of Aedes albopictus populations for chikungunya virus is shaped by their demographic history.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
24 06 2020
24 06 2020
Historique:
received:
14
01
2020
accepted:
26
05
2020
entrez:
26
6
2020
pubmed:
26
6
2020
medline:
24
6
2021
Statut:
epublish
Résumé
The mosquito Aedes albopictus is one of the most dangerous invasive species. Its worldwide spread has created health concerns as it is a major vector of arboviruses of public health significance such as chikungunya (CHIKV). Dynamics of different genetic backgrounds and admixture events may have impacted competence for CHIKV in adventive populations. Using microsatellites, we infer the genetic structure of populations across the expansion areas that we then associate with their competence for different CHIKV genotypes. Here we show that the demographic history of Ae. albopictus populations is a consequence of rapid complex patterns of historical lineage diversification and divergence that influenced their competence for CHIKV. The history of adventive populations is associated with CHIKV genotypes in a genotype-by-genotype interaction that impacts their vector competence. Thus, knowledge of the demographic history and vector competence of invasive mosquitoes is pivotal for assessing the risk of arbovirus outbreaks in newly colonized areas.
Identifiants
pubmed: 32581265
doi: 10.1038/s42003-020-1046-6
pii: 10.1038/s42003-020-1046-6
pmc: PMC7314749
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
326Références
Kraemer, M. U. et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife 4, e08347 (2015).
pubmed: 26126267
pmcid: 4493616
doi: 10.7554/eLife.08347
Mogi, M., Armbruster, P., Tuno, N., Campos, R. & Eritja, R. Simple indices provide insight to climate attributes delineating the geographic range of Aedes albopictus (Diptera: Culicidae) prior to worldwide invasion. J. Med. Entomol. 52, 647–657 (2015).
pubmed: 26335471
doi: 10.1093/jme/tjv038
pmcid: 26335471
Delatte, H., Gimonneau, G., Triboire, A. & Fontenille, D. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J. Med. Entomol. 46, 33–41 (2009).
pubmed: 19198515
doi: 10.1603/033.046.0105
pmcid: 19198515
Medlock, J. M. et al. A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Dis. 12, 435–447 (2012).
pubmed: 22448724
pmcid: 3366101
doi: 10.1089/vbz.2011.0814
Brady, O. J. et al. Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission. Parasit. Vectors 7, 1–17 (2014).
doi: 10.1186/1756-3305-7-1
Schmidt, C. A., Comeau, G., Monaghan, A. J., Williamson, D. J. & Ernst, K. C. Effects of desiccation stress on adult female longevity in Aedes aegypti and Ae. albopictus (Diptera: Culicidae): results of a systematic review and pooled survival analysis. Parasit. Vectors 11, 267 (2018).
pubmed: 29695282
pmcid: 5918765
doi: 10.1186/s13071-018-2808-6
Lounibos, L. P. & Kramer, L. D. Invasiveness of Aedes aegypti and Aedes albopictus and vectorial capacity for chikungunya virus. J. Infect. Dis. 214, S453–S458 (2016).
pubmed: 27920173
pmcid: 5137242
doi: 10.1093/infdis/jiw285
Poelchau, M. F., Reynolds, J. A., Elsik, C. G., Denlinger, D. L. & Armbruster, P. A. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B: Biol. Sci. 280, 1–9 (2013).
doi: 10.1098/rspb.2013.0143
Urbanski, J. et al. Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am. Naturalist 179, 490–500 (2012).
doi: 10.1086/664709
Lacour, G., Chanaud, L., L’Ambert, G. & Hance, T. Seasonal synchronization of diapause phases in Aedes albopictus (Diptera: Culicidae). PLoS ONE 10, e0145311 (2015).
pubmed: 26683460
pmcid: 4686165
doi: 10.1371/journal.pone.0145311
Juliano, S. A. & Lounibos, L. P. Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol. Lett. 8, 558–574 (2005).
pubmed: 17637849
pmcid: 1920178
doi: 10.1111/j.1461-0248.2005.00755.x
Invasive Species Specialist Group (2020) Species profile: Aedes albopictus. Downloaded from http://www.iucngisd.org/gisd/species.php?sc=109 on 15-06-2020.
Paupy, C., Delatte, H., Bagny, L., Corbel, V. & Fontenille, D. Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes Infect. 11, 1177–1185 (2009).
pubmed: 19450706
doi: 10.1016/j.micinf.2009.05.005
pmcid: 19450706
Gasperi, G. et al. A new threat looming over the Mediterranean basin: emergence of viral diseases transmitted by Aedes albopictus mosquitoes. PLoS Negl. Trop. Dis. 6, e1836 (2012).
pubmed: 23029593
pmcid: 3459824
doi: 10.1371/journal.pntd.0001836
Vega-Rua, A. et al. Chikungunya virus transmission potential by local Aedes mosquitoes in the Americas and Europe. PLoS Negl. Trop. Dis. 9, e0003780 (2015).
pubmed: 25993633
pmcid: 4439146
doi: 10.1371/journal.pntd.0003780
Wong, P. S. J., Li, M. Z. I., Chong, C. S., Ng, L. C. & Tan, C. H. Aedes (Stegomyia) albopictus (Skuse): a potential vector of Zika virus in Singapore. PLos Neg. Trop. Dis. 7, e2348 (2013).
doi: 10.1371/journal.pntd.0002348
Gratz, N. G. Critical review of the vector status of Aedes albopictus. Med Vet. Entomol. 18, 215–227 (2004).
pubmed: 15347388
doi: 10.1111/j.0269-283X.2004.00513.x
pmcid: 15347388
Chouin-Carneiro, T. et al. Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika virus. PLoS Negl. Trop. Dis. 10, e0004543 (2016).
pubmed: 26938868
pmcid: 4777396
doi: 10.1371/journal.pntd.0004543
Grard, G. et al. Zika virus in Gabon (Central Africa)-2007: a new threat from Aedes albopictus? PLoS Negl.Trop. Dis. 8, e2681 (2014).
pubmed: 24516683
pmcid: 3916288
doi: 10.1371/journal.pntd.0002681
Jupille, H., Seixas, G., Mousson, L., Sousa, C. A. & Failloux, A. B. Zika virus, a new threat for Europe? PLoS Negl. Trop. Dis. 10, e0004901 (2016).
pubmed: 27505002
pmcid: 4978396
doi: 10.1371/journal.pntd.0004901
Armstrong, P. M. et al. Successive blood meals enhance virus dissemination within mosquitoes and increase transmission potential. Nat. Microbiol. https://doi.org/10.1038/s41564-019-0619-y (2019).
Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol 4, 854–863 (2019).
pubmed: 30833735
pmcid: 6522366
doi: 10.1038/s41564-019-0376-y
Cunze, S., Kochmann, J., Koch, L. K. & Klimpel, S. Niche conservatism of Aedes albopictus and Aedes aegypti - two mosquito species with different invasion histories. Sci. Rep. 8, 7733 (2018).
pubmed: 29769652
pmcid: 5955948
doi: 10.1038/s41598-018-26092-2
Zeller, H., Van Bortel, W. & Sudre, B. Chikungunya: its History in Africa and Asia and its spread to new regions in 2013–2014. J. Infect. Dis. 214, S436–S440 (2016).
pubmed: 27920169
doi: 10.1093/infdis/jiw391
pmcid: 27920169
Gould, E. A., Gallian, P., De Lamballerie, X. & Charrel, R. N. First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality! Clin. Microbiol. Infect. 16, 1702–1704 (2010).
pubmed: 21040155
doi: 10.1111/j.1469-0691.2010.03386.x
pmcid: 21040155
Gjenero-Margan, I. et al. Autochthonous dengue fever in Croatia, August-September 2010. Eur. Surveill. 16, pii=19805 (2011).
Martinet, J. P., Ferté, H., Failloux, A. B., Schaffner, F. & Depaquit, J. Mosquitoes of North-Western Europe as potential vectors of arboviruses: a review. Viruses, https://doi.org/10.3390/v11111059 (2019).
Robinson, M. C. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans. R. Soc. Trop. Med Hyg. 49, 28–32 (1955).
pubmed: 14373834
doi: 10.1016/0035-9203(55)90080-8
pmcid: 14373834
Volk, S. M. et al. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J. Virol. 84, 6497–6504 (2010).
pubmed: 20410280
pmcid: 2903258
doi: 10.1128/JVI.01603-09
Goubert, C., Minard, G., Vieira, C. & Boulesteix, M. Population genetics of the Asian tiger mosquito Aedes albopictus, an invasive vector of human diseases. Heredity (Edinb.) 117, 125–134 (2016).
doi: 10.1038/hdy.2016.35
Manni, M. et al. Molecular markers for analyses of intraspecific genetic diversity in the Asian Tiger mosquito, Aedes albopictus. Parasit. Vectors 8, 188 (2015).
pubmed: 25890257
pmcid: 4404008
doi: 10.1186/s13071-015-0794-5
Manni, M. et al. Genetic evidence for a worldwide chaotic dispersion pattern of the arbovirus vector, Aedes albopictus. PLoS Negl. Trop. Dis. 11, e0005332 (2017).
pubmed: 28135274
pmcid: 5300280
doi: 10.1371/journal.pntd.0005332
Sherpa, S., Blum, M. G. B. & Després, L. Cold adaptation in the Asian tiger mosquito’s native range precedes its invasion success in temperate regions. Evolution, https://doi.org/10.1111/evo.13801 (2019).
Sherpa, S. et al. Unravelling the invasion history of the Asian tiger mosquito in Europe. Mol. Ecol. 28, 2360–2377 (2019).
pubmed: 30849200
doi: 10.1111/mec.15071
pmcid: 30849200
Kotsakiozi, P. et al. Population genomics of the Asian tiger mosquito, Aedes albopictus: insights into the recent worldwide invasion. Ecol. Evol. 7, 10143–10157 (2017).
pubmed: 29238544
pmcid: 5723592
doi: 10.1002/ece3.3514
Pichler, V. et al. Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe. PLoS Negl. Trop. Dis. 13, e0007554 (2019).
pubmed: 31437154
pmcid: 6705758
doi: 10.1371/journal.pntd.0007554
Vega-Rúa, A., Zouache, K., Girod, R., Failloux, A. B. & Lourenço-de-Oliveira, R. High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus. J. Virol. 88, 6294–6306 (2014).
pubmed: 24672026
pmcid: 4093877
doi: 10.1128/JVI.00370-14
Vazeille, M. et al. Importance of mosquito “quasispecies” in selecting an epidemic arthropod-borne virus. Sci. Rep. 6, 29564 (2016).
pubmed: 27383735
pmcid: 4935986
doi: 10.1038/srep29564
Zouache, K. & Failloux, A. B. Insect-pathogen interactions: contribution of viral adaptation to the emergence of vector-borne diseases, the example of chikungunya. Curr. Opin. Insect Sci. 10, 14–21 (2015).
pubmed: 29588001
doi: 10.1016/j.cois.2015.04.010
Hawley, W. A., Reiter, P., Copeland, R. S., Pumpuni, C. B. & Craig, G. B. Aedes albopictus in North America: probable introduction in used tires from northern Asia. Science 236, 1114–1116 (1987).
pubmed: 3576225
doi: 10.1126/science.3576225
pmcid: 3576225
Paupy, C., Girod, R., Salvan, M., Rodhain, F. & Failloux, A. B. Population structure of Aedes albopictus from La Réunion Island (Indian Ocean) with respect to susceptibility to a dengue virus. Heredity (Edinb.) 87, 273–283 (2001).
doi: 10.1046/j.1365-2540.2001.00866.x
Delatte, H. et al. Evidence of habitat structuring Aedes albopictus populations in Réunion Island. PLoS Negl. Trop. Dis. 7, e2111 (2013).
pubmed: 23556012
pmcid: 3605158
doi: 10.1371/journal.pntd.0002111
Sprenger, D. & Wuithiranyagool, T. The discovery and distribution of Aedes albopictus in Harris County, Texas. J. Am. Mosq. Control Assoc. 2, 217–219 (1986).
pubmed: 3507493
pmcid: 3507493
Casas-Martínez, M. & Torres-Estrada, J. L. First evidence of Aedes albopictus (Skuse) in southern Chiapas, Mexico. Emerg. Infect. Dis. 9, 606–607 (2003).
pubmed: 12737750
doi: 10.3201/eid0905.020678
pmcid: 12737750
Eskildsen, G. A. et al. Maternal invasion history of Aedes aegypti and Aedes albopictus into the Isthmus of Panama: implications for the control of emergent viral disease agents. PLoS ONE 13, e0194874 (2018).
pubmed: 29579112
pmcid: 5868824
doi: 10.1371/journal.pone.0194874
Maia, R. T., Scarpassa, V. M., Maciel-Litaiff, L. H. & Tadei, W. P. Reduced levels of genetic variation in Aedes albopictus (Diptera: Culicidae) from Manaus, Amazonas State, Brazil, based on analysis of the mitochondrial DNA ND5 gene. Genet Mol. Res. 8, 998–1007 (2009).
pubmed: 19731220
doi: 10.4238/vol8-3gmr624
pmcid: 19731220
Honório, N. A., Wiggins, K., Câmara, D. C. P., Eastmond, B. & Alto, B. W. Chikungunya virus vector competency of Brazilian and Florida mosquito vectors. PLoS Negl. Trop. Dis. 12, e0006521 (2018).
pubmed: 29879121
pmcid: 6007930
doi: 10.1371/journal.pntd.0006521
Glushakova, L. G. et al. Multiplexed kit based on Luminex technology and achievements in synthetic biology discriminates Zika, chikungunya, and dengue viruses in mosquitoes. BMC Infect. Dis. 19, 418 (2019).
pubmed: 31088375
pmcid: 6518713
doi: 10.1186/s12879-019-3998-z
Tsetsarkin, K. A. et al. Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc. Natl Acad. Sci. USA 108, 7872–7877 (2011).
pubmed: 21518887
pmcid: 21518887
doi: 10.1073/pnas.1018344108
Vazeille, M. et al. Two Chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS ONE 2, e1168 (2007).
pubmed: 18000540
pmcid: 18000540
doi: 10.1371/journal.pone.0001168
Tsetsarkin, K. A., Vanlandingham, D. L., McGee, C. E. & Higgs, S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3, e201 (2007).
pubmed: 18069894
pmcid: 18069894
doi: 10.1371/journal.ppat.0030201
Coffey, L. L., Forrester, N., Tsetsarkin, K., Vasilakis, N. & Weaver, S. C. Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease. Future Microbiol. 8, 155–176 (2013).
pubmed: 23374123
pmcid: 3621119
doi: 10.2217/fmb.12.139
Theamboonlers, A., Rianthavorn, P., Praianantathavorn, K., Wuttirattanakowit, N. & Poovorawan, Y. Clinical and molecular characterization of chikungunya virus in South Thailand. Jpn J. Infect. Dis. 62, 303–305 (2009).
pubmed: 19628911
pmcid: 19628911
Zouache, K. et al. Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2014.1078 (2014).
Enserink, M. Infectious diseases. chikungunya: no longer a third world disease. Science 318, 1860–1861 (2007).
pubmed: 18096785
doi: 10.1126/science.318.5858.1860
pmcid: 18096785
Grandadam, M. et al. Chikungunya virus, southeastern France. Emerg. Infect. Dis. 17, 910–913 (2011).
pubmed: 21529410
pmcid: 3321794
doi: 10.3201/eid1705.101873
Delisle, E. et al. Chikungunya outbreak in Montpellier, France, September to October 2014. Euro Surveill 20, 21108 (2015).
Calba, C. et al. Preliminary report of an autochthonous chikungunya outbreak in France, July to September 2017. Euro Surveill. 22, https://doi.org/10.2807/1560-7917.ES.2017.22.39.17-00647 (2017).
Angelini, R. et al. An outbreak of chikungunya fever in the province of Ravenna, Italy. Euro Surveill 12, E070906.070901, https://doi.org/10.2807/esw.12.36.03260-en (2007).
Rezza, G. et al. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370, 1840–1846 (2007).
pubmed: 18061059
pmcid: 18061059
doi: 10.1016/S0140-6736(07)61779-6
Rezza, G. Chikungunya is back in Italy: 2007-2017. J. Travel Med. https://doi.org/10.1093/jtm/tay004 (2018).
Fortuna, C. et al. Vector competence of Aedes albopictus for the Indian Ocean lineage (IOL) chikungunya viruses of the 2007 and 2017 outbreaks in Italy: a comparison between strains with and without the E1:A226V mutation. Euro Surveill. https://doi.org/10.2807/1560-7917.ES.2018.23.22.1800246 (2018).
Mariconti, M. et al. Estimating the risk of arbovirus transmission in Southern Europe using vector competence data. Sci. Rep. 9, 17852 (2019).
pubmed: 31780744
pmcid: 6882796
doi: 10.1038/s41598-019-54395-5
Machado, L. C. et al. Genome sequencing reveals coinfection by multiple chikungunya virus genotypes in a recent outbreak in Brazil. PLoS Negl. Trop. Dis. 13, e0007332 (2019).
pubmed: 31095561
pmcid: 31095561
doi: 10.1371/journal.pntd.0007332
Naveca, F. G. et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Negl. Trop. Dis. 13, e0007065 (2019).
pubmed: 30845267
pmcid: 6424459
doi: 10.1371/journal.pntd.0007065
Ketkar, H., Herman, D. & Wang, P. Genetic determinants of the re-emergence of arboviral diseases. Viruses, https://doi.org/10.3390/v11020150 (2019).
Caragata, E. P., Tikhe, C. V. & Dimopoulos, G. Curious entanglements: interactions between mosquitoes, their microbiota, and arboviruses. Curr. Opin. Virol. 37, 26–36 (2019).
pubmed: 31176069
pmcid: 6768729
doi: 10.1016/j.coviro.2019.05.005
Rueda, L. Pictorial keys for the identification of mosquitoes (Diptera: Culicidae) associated with dengue virus transmission. Zootaxa 589, 61 (2004).
doi: 10.11646/zootaxa.589.1.1
Guichoux, E. et al. Current trends in microsatellite genotyping. Mol. Ecol. Resour. 11, 591–611 (2011).
pubmed: 21565126
doi: 10.1111/j.1755-0998.2011.03014.x
pmcid: 21565126
Baruffi, L. et al. Polymorphism within and between populations of Ceratitis capitata: comparison between RAPD and multilocus enzyme electrophoresis data. Heredity (Edinb.) 74(Pt 4), 425–437 (1995).
doi: 10.1038/hdy.1995.60
Chen, X. G. et al. Genome sequence of the Asian Tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution. Proc. Natl Acad. Sci. USA 112, E5907–E5915 (2015).
pubmed: 26483478
doi: 10.1073/pnas.1516410112
pmcid: 26483478
Matschiner, M. & Salzburger, W. TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25, 1982–1983 (2009).
pubmed: 19420055
doi: 10.1093/bioinformatics/btp303
pmcid: 19420055
Buschiazzo, E. & Gemmell, N. J. The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 28, 1040–1050 (2006).
pubmed: 16998838
doi: 10.1002/bies.20470
pmcid: 16998838
Raymond, M. & Rousset, F. Genepop (Version-1.2) Population-genetics software for exact tests and ecumenicism. J. Hered. 86, 2 (1995).
doi: 10.1093/oxfordjournals.jhered.a111573
Rice, W. R. Analyzing tables of statistical tests. Evolution 43, 223–225 (1989).
pubmed: 28568501
doi: 10.1111/j.1558-5646.1989.tb04220.x
pmcid: 28568501
Peakall, R. & Smouse, P. E. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539 (2012).
pubmed: 22820204
pmcid: 3463245
doi: 10.1093/bioinformatics/bts460
FSTAT, a program to estimate and test gene diversities and fixation indices v. 2.9.3 (2002).
Dieringer, D. & Schlotterer, C. MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3, 3 (2003).
doi: 10.1046/j.1471-8286.2003.00351.x
Earl, D. & vonHoldt, B. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 4, 3 (2012).
doi: 10.1007/s12686-011-9548-7
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
pubmed: 10835412
pmcid: 10835412
Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).
doi: 10.1111/j.1365-294X.2005.02553.x
pubmed: 15969739
pmcid: 15969739
Jakobsson, M. & Rosenberg, N. A. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806 (2007).
doi: 10.1093/bioinformatics/btm233
pubmed: 17485429
Rosenberg, N. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 4, 2 (2004).
Pudlo, P. et al. Reliable ABC model choice via random forests. Bioinformatics 32, 859–866 (2016).
pubmed: 26589278
doi: 10.1093/bioinformatics/btv684
pmcid: 26589278
Fraimout, A. et al. Deciphering the routes of invasion of Drosophila suzukii by Means of ABC Random Forest. Mol. Biol. Evol. 34, 980–996 (2017).
pubmed: 28122970
pmcid: 5400373
Alto, B. W. & Juliano, S. A. Temperature effects on the dynamics of Aedes albopictus (Diptera: Culicidae) populations in the laboratory. J. Med Entomol. 38, 548–556 (2001).
pubmed: 11476335
pmcid: 2579928
doi: 10.1603/0022-2585-38.4.548
Garza, J. C. & Williamson, E. G. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10, 305–318 (2001).
pubmed: 11298947
doi: 10.1046/j.1365-294x.2001.01190.x
pmcid: 11298947
Cornuet, J. M. et al. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24, 2713–2719 (2008).
pubmed: 18842597
pmcid: 2639274
doi: 10.1093/bioinformatics/btn514
Cornuet, J. M., Ravigné, V. & Estoup, A. Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinforma. 11, 401 (2010).
doi: 10.1186/1471-2105-11-401
Dubrulle, M., Mousson, L., Moutailler, S., Vazeille, M. & Failloux, A. B. Chikungunya virus and Aedes mosquitoes: saliva is infectious as soon as two days after oral infection. PLoS ONE 4, e5895 (2009).
pubmed: 2690823
pmcid: 2690823
doi: 10.1371/journal.pone.0005895
FIRTHLOGIT: Stata module to calculate bias reduction in logistic regression v. revised 25 Jul 2015 (Boston College Department of Economics, Boston, MA, USA, 2015).
Adhami, J. & Reiter, P. Introduction and establishment of Aedes (Stegomyia) albopictus skuse (Diptera: Culicidae) in Albania. J. Am. Mosq. Control Assoc. 14, 340–343 (1998).
pubmed: 9813831
pmcid: 9813831
Sabatini, A., Raineri, V., Trovato, G. & Coluzzi, M. [Aedes albopictus in Italy and possible diffusion of the species into the Mediterranean area]. Parassitologia 32, 301–304 (1990).
pubmed: 2132441
pmcid: 2132441
Delaunay, P., Jeannin, C., Schaffner, F. & Marty, P. [News on the presence of the tiger mosquito Aedes albopictus in metropolitan France]. Arch. Pediatr. 16(Suppl 2), S66–S71 (2009).
pubmed: 19836679
doi: 10.1016/S0929-693X(09)75304-7
pmcid: 19836679
Leong, M. & Grace, J. Occurrence and distribution of mosquitoes (Diptera: Culicidae) of public health importance on the Island of Oahu. Proc. Hawaii. Entomol. Soc. 41, 14 (2009).
Moore, C. G., Francy, D. B., Eliason, D. A. & Monath, T. P. Aedes albopictus in the United States: rapid spread of a potential disease vector. J. Am. Mosq. Control Assoc. 4, 356–361 (1988).
pubmed: 3058869
pmcid: 3058869
O’Meara, G. F., Evans, L. F., Gettman, A. D. & Cuda, J. P. Spread of Aedes albopictus and decline of Ae. aegypti (Diptera: Culicidae) in Florida. J. Med Entomol. 32, 554–562 (1995).
pubmed: 7650719
doi: 10.1093/jmedent/32.4.554
pmcid: 7650719
Forattini, O. P. Identification of Aedes (Stegomyia) albopictus (Skuse) in Brazil. Rev. Saude Publica 20, 244–245 (1986).
pubmed: 3809982
doi: 10.1590/S0034-89101986000300009
pmcid: 3809982
Fé, N. F., das Graças Vale Barbosa, M., Alecrim, W. D. & Guerra, M. V. [Registration of the occurrence of Aedes albopictus in an urban zone in Manaus, Amazonas, Brazil]. Rev. Saude Publica 37, 674–675 (2003).
pubmed: 14569347
doi: 10.1590/S0034-89102003000500020
pmcid: 14569347
Pancetti, F. G., Honório, N. A., Urbinatti, P. R. & Lima-Camara, T. N. Twenty-eight years of Aedes albopictus in Brazil: a rationale to maintain active entomological and epidemiological surveillance. Rev. Soc. Bras. Med Trop. 48, 87–89 (2015).
pubmed: 25860470
doi: 10.1590/0037-8682-0155-2014
pmcid: 25860470
Schweigmann, N., Vezzani, D., Orellano, P., Kuruc, J. & Boffi, R. Aedes albopictus in an area of Misiones, Argentina. Rev. Saude Publica 38, 136–138 (2004).
pubmed: 14963554
doi: 10.1590/S0034-89102004000100020
pmcid: 14963554
Ngoagouni, C., Kamgang, B., Nakouné, E., Paupy, C. & Kazanji, M. Invasion of Aedes albopictus (Diptera: Culicidae) into central Africa: what consequences for emerging diseases? Parasit. Vectors 8, 191 (2015).
pubmed: 25885461
pmcid: 4381565
doi: 10.1186/s13071-015-0808-3