Impact of Long-Term Pyriproxyfen Exposure on the Genetic Structure and Diversity of Aedes aegypti and Aedes albopictus in Manaus, Amazonas, Brazil
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area and Mosquito Surveillance
2.2. Sample Preparation and Sequencing
2.3. Species Identification
2.4. Variant Calling
2.5. Population Genetics Structure Inferences
3. Results
3.1. Data Collection and DNA Extraction
3.2. Double Digest Restriction-Site Associated DNA Sequencing (ddRADseq) Performance
3.3. Statistical and Structural Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kraemer, M.U.; Sinka, M.E.; Duda, K.A.; Mylne, A.Q.; Shearer, F.M.; Barker, C.M.; Moore, C.G.; Carvalho, R.G.; Coelho, G.E.; Van Bortel, W.; et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife 2015, 4, e08347. [Google Scholar] [CrossRef]
- Espinal, M.A.; Andrus, J.K.; Jauregui, B.; Waterman, S.H.; Morens, D.M.; Santos, J.I.; Horstick, O.; Francis, L.A.; Olson, D. Emerging and Reemerging Aedes-Transmitted Arbovirus Infections in the Region of the Americas: Implications for Health Policy. Am. J. Public Health 2019, 109, 387–392. [Google Scholar] [CrossRef]
- Evans, B.R.; Gloria-Soria, A.; Hou, L.; McBride, C.; Bonizzoni, M.; Zhao, H.; Powell, J.R. A multipurpose, high-throughput single-nucleotide polymorphism chip for the dengue and yellow fever mosquito, Aedes aegypti. G3-Genes Genomes Genet. 2015, 26, 711–718. [Google Scholar] [CrossRef]
- BRASIL. Ministério da Saúde. Relatório da Reunião Internacional para Implementação de Alternativas para o Controle do Aedes aegypti no Brasil. Bol. Epidemiológico 2016, 47, 2358–9450. [Google Scholar]
- ISGBLOBAL—Annual Report ISGlobal. Barcelona Institute for Global Health. Barcelona. 2018. Available online: https://www.isglobal.org (accessed on 2 July 2024).
- Devine, G.J.; Perea, E.Z.; Killeen, G.F.; Stancil, J.D.; Clark, S.J.; Morrison, A.C. Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc. Natl. Acad. Sci. USA 2009, 106, 11530–11534. [Google Scholar] [CrossRef] [PubMed]
- Garcia, K.K.S.; Versiani, H.S.; Araújo, T.O.; Conceição, J.P.A.; Obara, M.T.; Ramalho, W.M.; Minuzzi-Souza, T.T.C.; Gomes, G.D.; Vianna, E.N.; Timbó, R.V.; et al. Measuring mosquito control: Adult-mosquito catches vs egg-trap data as endpoints of a cluster-randomized controlled trial of mosquito-disseminated pyriproxyfen. Parasites Vectors 2020, 13, 352. [Google Scholar] [CrossRef]
- Abad-Franch, F.; Zamora-Perea, E.; Luz, S.L.B. Mosquito-disseminated insecticide for citywide vector control and its potential to block arbovirus epidemics: Entomological observations and modeling results from Amazonian Brazil. PLoS Med. 2017, 14, e1002213. [Google Scholar] [CrossRef] [PubMed]
- Abad-Franch, F.; Zamora-Perea, E.; Ferraz, G.; Padilla-Torres, S.D.; Luz, S.L.B. Mosquito-disseminated pyriproxyfen yields high breeding-site coverage and boosts juvenile mosquito mortality at the neighborhood scale. PLoS Negl. Trop. Dis. 2015, 9, e0003702. [Google Scholar] [CrossRef]
- Leles, L.F.d.O.; Alvarez, M.V.N.; Cortés, J.J.C.; Alonso, D.P.; Ribolla, P.E.M.; Luz, S.L.B. Evaluation of Aedes aegypti control intervention with pyriproxyfen by lcWGS in Manacapuru, Amazonas, Brasil. PLoS Negl. Trop. Dis. 2024. submitted for publication. [Google Scholar]
- Seixas, G.; Salgueiro, P.; Silva, A.C.; Campos, M.; Spenassatto, C.; Reyes-Lugo, M.; Novo, M.T.; Ribolla, P.E.M.; Da Pinto, J.P.S.D.; Sousa, C.A. Aedes aegypti on Madeira Island (Portugal): Genetic variation of a recently introduced dengue vector. Mem. Inst. Oswaldo Cruz 2013, 108 (Suppl. S1), 3–10. [Google Scholar] [CrossRef]
- Rahman, R.U.; Cosme, L.V.; Costa, M.M.; Carrara, L.; Lima, J.B.P.; Martins, A.J. Insecticide resistance and genetic structure of Aedes aegypti populations from Rio de Janeiro State, Brazil. PLoS Negl. Trop. Dis. 2021, 15, e0008492. [Google Scholar] [CrossRef] [PubMed]
- Steffler, L.M.; Dolabella, S.S.; Ribolla, P.E.M.; Dreyer, C.S.; Araújo, E.D.; Oliveira, R.G.; Martins, W.F.S.; La Corte, R. Genetic variability and spatial distribution in small geographic scale of Aedes aegypti (Diptera: Culicidae) under different climatic conditions in Northeastern Brazil. Parasites Vectors 2016, 9, 530. [Google Scholar] [CrossRef]
- Brito, L.P.; Carrara, L.; De Freitas, R.M.; Lima, J.B.P.; Martins, A.J. Levels of Resistance to Pyrethroid among Distinct kdr Alleles in Aedes aegypti Laboratory Lines and Frequency of kdr Alleles in 27 Natural Populations from Rio de Janeiro, Brazil. BioMed Res. Int. 2018, 2018, 2410819. [Google Scholar] [CrossRef]
- Campos, M.; Conn, J.E.; Alonso, D.P.; Vinetz, J.M.; Emerson, K.J.; Ribolla, P.E.M. Microgeographical structure in the major Neotropical malaria vector Anopheles darlingi using microsatellites and SNP markers. Parasites Vectors 2017, 10, 76. [Google Scholar] [CrossRef]
- Matthews, B.J.; Dudchenko, O.; Kingan, S.B.; Koren, S.; Antoshechkin, I.; Crawford, J.E.; Glassford, W.J.; Herre, M.; Redmond, S.N.; Rose, N.H.; et al. Improved reference genome of Aedes aegypti informs arbovirus vector control. Nature 2018, 563, 501–507. [Google Scholar] [CrossRef] [PubMed]
- Boyle, J.H.; Rastas, P.M.A.; Huang, X.; Garner, A.G.; Vythilingam, I.; Armbruster, P.A. A Linkage-Based Genome Assembly for the Mosquito Aedes albopictus and Identification of Chromosomal Regions Affecting Diapause. Insects 2021, 12, 167. [Google Scholar] [CrossRef] [PubMed]
- Goodwin, S.; McPherson, J.D.; McCombie, W.R. Coming of age: Ten years of next-generation sequencing technologies. Nat. Rev. Genet. 2016, 17, 333–351. [Google Scholar] [CrossRef]
- Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 2 July 2024).
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows—Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef]
- Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011, 27, 2987–2993. [Google Scholar] [CrossRef]
- Altschul, S.F.; Gish, W. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Purcell, S.; Neale, B.; Todd-Brown, K.; Thomas, L.; Ferreira, M.A.R.; Bender, D.; Maller, J.; Sklar, P.; De Bakker, P.I.W.; Daly, M.J.; et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007, 81, 559–575. [Google Scholar] [CrossRef] [PubMed]
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis, 3.5.0 ed.; Springer: Berlin/Heidelberg, Germany, 2023. [Google Scholar]
- Rstudio Team. RStudio: Integrated Development Environment for R; RStudio, PBC. Inc.: Boston, MA, USA, 2015; Volume 42, p. 14. Available online: http://www.rstudio.com/ (accessed on 2 July 2024).
- Excoffier, L.; Lischer, H.E.L. Arlequin suite ver 3. 5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10, 564–567. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, R.; Shimodaira, H. pvclust: Hierarchical Clustering with P-Values. R Package Version 2.2-0. 2020. Available online: https://cran.r-project.org/package=pvclust (accessed on 2 July 2024).
- Rstudio Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2023; Volume 55, pp. 275–286. Available online: http://www.R-project.org/ (accessed on 2 July 2024).
- Oksanen, J.; Simpson, G.L.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Solymos, P.; Stevens, M.H.H.; Szoecs, E.; et al. Vegan: Community Ecology Package. R Package Version 2.6.4. 2001. Available online: https://cran.r-project.org/package=vegan (accessed on 2 July 2024).
- Alvarez, M.V.N. LCVCFtools v0.1.16. Zenodo 2021. [Google Scholar] [CrossRef]
- Alvarez, M.V.N.; Alonso, D.P.; Kadri, S.M.; Rufalco-Moutinho, P.; Bernardes, I.A.F.; Mello, A.C.F.; Souto, A.C.; Carras-co-Escobar, G.; Moreno, M.; Gamboa, D.; et al. Nyssorhynchus darlingi genome-wide studies related to microgeographic dispersion and blood-seeking behavior. Parasites Vectors 2022, 15, 106. [Google Scholar] [CrossRef] [PubMed]
- Alonso, D.P.; Alvarez, M.V.N.; Ribolla, P.E.M.; Conn, J.E.; Oliveira, T.M.P.; Sallum, M.A.M. Susceptibility of Field-Collected Nyssorhynchus darlingi to Plasmodium spp. in Western Amazonian Brazil. Genes 2021, 12, 1693. [Google Scholar] [CrossRef] [PubMed]
- Segarra, A.J.G.; Pontes, G.; Jourjine, N.; Del Toro, A.; Scott, K. Hunger-and thirst-sensing neurons modulate a neuroendocrine network to coordinate sugar and water ingestion. ELife 2023, 12, RP88143. [Google Scholar] [CrossRef]
- Havula, E.; Ghazanfar, S.; Lamichane, N.; Francis, D.; Hasygar, K.; Liu, Y.; Alton, L.A.; Johnstone, J.; Needham, E.J.; Pulpitel, T.; et al. Genetic variation of macronutrient tolerance in Drosophila melanogaster. Nat. Commun. 2022, 13, 1637. [Google Scholar] [CrossRef] [PubMed]
- Shahid, S.; Shi, Y.; Yang, C.; Li, J.; Ali, M.Y.; Smagghe, G.; Liu, T.-X. CCHamide2-receptor regulates feeding behavior in the pea aphid, Acyrthosiphon pisum. Peptides 2021, 143, 170596. [Google Scholar] [CrossRef]
- Wang, Z.; Zhou, W.; Hameed, M.S.; Liu, J.; Zeng, X. Characterization and Expression Profiling of Neuropeptides and G-Protein-Coupled Receptors (GPCRs) for Neuropeptides in the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae). Int. J. Mol. Sci. 2018, 19, 3912. [Google Scholar] [CrossRef]
- Yamagata, N.; Imanishi, Y.; Wu, H.; Kondo, S.; Sano, H.; Tanimoto, H. Nutrient responding peptide hormone CCHamide-2 consolidates appetitive memory. Front. Behav. Neurosci. 2022, 16, 986064. [Google Scholar] [CrossRef] [PubMed]
- Hobin, M.; Dorfman, K.; Adel, M.; Rivera-Rodriguez, E.J.; Kuklin, E.A.; Ma, D.; Griffith, L.C. The Drosophila microRNA bantam regulates excitability in adult mushroom body output neurons to promote early night sleep. iScience 2022, 25, 104874. [Google Scholar] [CrossRef] [PubMed]
- Nagata, S.; Takei, Y. Chapter 84—CCHamide: Handbook of Hormones; Academic Press: Cambridge, MA, USA, 2016; pp. 475–476. [Google Scholar]
- Bargielowski, I.E.; Lounibos, L.P.; Carrasquilla, M.C. Evolution of resistance to satyrization through reproductive character displacement in populations of invasive dengue vectors. Proc. Natl. Acad. Sci. USA 2013, 110, 2888–2892. [Google Scholar] [CrossRef] [PubMed]
- Honório, N.A.; Da Silva, W.D.; Leite, P.J.; Gonçalves, J.M.; Lounibos, L.P.; Lourenço-De-Oliveira, R. Dispersal of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in an urban endemic dengue area in the State of Rio de Janeiro, Brazil. Mem. Inst. Oswaldo Cruz 2003, 98, 191–198. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Kamara, F.; Zhou, G.; Puthiyakunnon, S.; Li, C.; Liu, Y.; Zhou, Y.; Yao, L.; Yan, G.; Chen, X.-G. Urbanization Increases Aedes albopictus Larval Habitats and Accelerates Mosquito Development and Survivorship. PLoS Negl. Trop. Dis. 2014, 8, e3301. [Google Scholar] [CrossRef] [PubMed]
- Consoli, R.A.G.B.; Oliveira, R.L. Principais Mosquitos de Importância Sanitária no Brasil; Editora FIOCRUZ: Rio de Janeiro, Brasil, 1994; 228p, Available online: http://books.scielo.org (accessed on 2 July 2024).
- Verdonschot, P.F.M.; Besse-Lototskaya, A.A. Flight distance of mosquitoes (Culicidae): A metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica 2014, 45, 69–79. [Google Scholar] [CrossRef]
- Guerra, C.A.; Reiner, R.C.; Perkins, T.A.; Lindsay, S.W.; Midega, J.T.; Brady, O.J.; Barker, C.M.; Reisen, W.K.; Harrington, L.C.; Takken, W.; et al. A global assembly of adult female mosquito mark-release-recapture data to inform the control of mosquito-borne pathogens. Parasites Vectors 2014, 7, 276. [Google Scholar] [CrossRef]
- Harrington, L.C.; Edman, J.D.; Kittayapong, P.; Coleman, R.C.; Clark, G.G.; Sithiprasasna, R.; Kitthawee, S.; Lerdthusnee, K.; Scott, T.W.; Costero, A.; et al. Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am. J. Trop. Med. Hyg. 2005, 72, 209–220. [Google Scholar] [CrossRef] [PubMed]
Ae. aegypti | Ae. albopictus | |||
---|---|---|---|---|
AdAl—Control | Total | Selected | Total | Selected |
JAN/FEB—2018 to 2020 | 28,311 | 28 | 16,820 | 23 |
Glória—Experimental | Total | Selected | Total | Selected |
JAN/FEB—2018 to 2020 | 27,161 | 25 | 2900 | 25 |
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Leles, L.F.d.O.; Alvarez, M.V.N.; Cortes, J.J.C.; Alonso, D.P.; Ribolla, P.E.M.; Luz, S.L.B. Impact of Long-Term Pyriproxyfen Exposure on the Genetic Structure and Diversity of Aedes aegypti and Aedes albopictus in Manaus, Amazonas, Brazil. Genes 2024, 15, 1046. https://doi.org/10.3390/genes15081046
Leles LFdO, Alvarez MVN, Cortes JJC, Alonso DP, Ribolla PEM, Luz SLB. Impact of Long-Term Pyriproxyfen Exposure on the Genetic Structure and Diversity of Aedes aegypti and Aedes albopictus in Manaus, Amazonas, Brazil. Genes. 2024; 15(8):1046. https://doi.org/10.3390/genes15081046
Chicago/Turabian StyleLeles, Lorena Ferreira de Oliveira, Marcus Vinícius Niz Alvarez, Jose Joaquin Carvajal Cortes, Diego Peres Alonso, Paulo Eduardo Martins Ribolla, and Sérgio Luiz Bessa Luz. 2024. "Impact of Long-Term Pyriproxyfen Exposure on the Genetic Structure and Diversity of Aedes aegypti and Aedes albopictus in Manaus, Amazonas, Brazil" Genes 15, no. 8: 1046. https://doi.org/10.3390/genes15081046