Understanding the Spread of Insecticide Resistance through Population Genetic Approach: A Review
Article Sidebar
Main Article Content
Abstract
This review discusses the application of the population genetic approach in elucidating the deployment of insecticide resistance to mosquito vectors. Although there have been a lot of scientific work describing population genetic research and insecticide resistance, a study focusing on the spread of insecticide resistance using the population genetic approach needs to be done. Population genetics explains how a population is diverse in response to fitness and the cost of environmental factors. Thus, readers can relate this process to how insecticides spread in the population. Additionally, some fundamental mechanisms of insecticide resistance are also covered. As successive reproduction of advantageous phenotypic traits, such as resistance depends on many factors including continuous pressure, recombination rate, migration rate, genetic drift, and so on. Currently, genome-wide association studies involve chromosome-wide SNPs in which recombination hotspots occur or microsatellite flanking region of resistance gene target in which the fixation process can potentially serve as a suitable marker for elucidating the deployment. The information provided in this review to facilitate how the susceptible individual still exists despite the predominance of resistant individuals and how the resistance reverts to the vulnerable state.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright Transfer Statement
The copyright of this article is transferred to Current Applied Science and Technology journal with effect if and when the article is accepted for publication. The copyright transfer covers the exclusive right to reproduce and distribute the article, including reprints, translations, photographic reproductions, electronic form (offline, online) or any other reproductions of similar nature.
The author warrants that this contribution is original and that he/she has full power to make this grant. The author signs for and accepts responsibility for releasing this material on behalf of any and all co-authors.
Here is the link for download: Copyright transfer form.pdf
References
World Health Organization, 2014. WHO Recommendations for Achieving Universal Coverage with Long-lasting Insecticidal Nets in Malaria Control. [online] Available at: https://www.afro.who.int/publications/who-recommendations-achieving-universal-coverage-long-lasting-insecticidal-nets.
World Health Organization, 2017. Achieving and Maintaining Universal Coverage with Long-lasting Insecticidal Nets for Malaria Control (No. WHO/HTM/GMP/2017.20). [online] Available at: https://iris.who.int/bitstream/handle/10665/259478/WHO-HTM-GMP-2017.20-eng.pdf?sequence=1.
Hemingway, J., Field, L. and Vontas, J., 2002. An overview of insecticide resistance. Science, 298(5591), 96-97, https://doi.org/10.1126/science.1078052.
Kelvin, A.A., 2011. Outbreak of Chikungunya in the Republic of Congo and the global picture. The Journal of Infection in Developing Countries, 5(6), 441-4, https://doi.org/10.3855/jidc.2171.
Gjullin, C. and Peters, R., 1952. Recent Studies of Mosquito Resistance to Insecticides in California. [online] Available at: https://www.biodiversitylibrary.org/content/part/JAMCA/ MN_V12_N1_P001-007.pdf.
Li, T. and Liu, N., 2014. Inheritance of permethrin resistance in Culex quinquefasciatus. Journal of Medical Entomology, 47(6), 1127-1134, https://doi.org/10.1603/ME10142.
Liu, H., Xu, Q., Zhang, L. and Liu, N., 2005. Chlorpyrifos resistance in mosquito Culex quinquefasciatus. Journal of Medical Entomology, 42(5), 815-20, https://doi.org/10.1093/jmedent/42.5.815.
Liu, N., Li, T., Reid, W. R., Yang, T. and Zhang, L., 2011. Multiple cytochrome P450 genes: their constitutive overexpression and permethrin induction in insecticide resistant mosquitoes, Culex quinquefasciatus. Plos One, 6(8), https://doi.org/10.1371/journal.pone.0023403.
Liu, N., Liu, H., Zhu, F. and Zhang, L., 2007. Differential expression of genes in pyrethroid resistant and susceptible mosquitoes, Culex quinquefasciatus (S.). Gene, 394(1-2), 61-68, https://doi.org/10.1016/j.gene.2007.01.032.
Nabeshima, T., Mori, A., Kozaki, T., Iwata, Y., Hidoh, O., Harada, S., Kasai, S., Severson, D. W., Kono, Y. and Tomita, T., 2004. An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochemical and Biophysical Research Communications, 313(3), 794-801, https://doi.org/10.1016/j.bbrc.2003.11.141.
Raymond, M., Chevillon, C., Guillemaud, T., Lenormand, T. and Pasteur, N., 1998. An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Philosophical Transactions of the Royal Society of London, 353(1376), 1707-1711, https://doi.org/10.1098/rstb.1998.0322.
Vontas, J., Blass, C., Koutsos, A.C., David, J.P., Kafatos, F.C., Louis, C., Hemingway, J., Christophides, G.K. and Ranson, H., 2005. Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure. Insect Molecular Biology, 14(5), 509-521, https://doi.org/10.1111/j.1365-2583.2005.00582.x.
World Health Organization, 1957. Expert Committee on Insecticides: Seventh Report [of a Meeting Held in Geneva from 10 to 17 July 1956]. [online] Available at: https://iris.who.int/handle/10665/40380?&locale-attribute=pt.
Xu, Q., Zhang, L., Li, T., Zhang, L., He, L., Dong, K. and Liu, N., 2012. Evolutionary adaptation of the amino acid and codon usage of the mosquito sodium channel following insecticide selection in the field mosquitoes. PLoS One, 7(10), https://doi.org/10.1371/journal.pone.0047609.
Roush, R.,1990. Genetics and management of insecticide resistance: lessons for resistance in internal parasites. Resistance of Parasites to Antiparasitic Drugs: Round Table Conference ICOPA VII, Paris, France, pp. 197-211.
Yang, T. and Liu, N., 2014. Permethrin resistance variation and susceptible reference line isolation in a field population of the mosquito, Culex quinquefasciatus (Diptera: Culicidae). Insect Science, 21(5), 659-666, https://doi.org/10.1111/1744-7917.12071.
Casida, J.E. and Durkin, K.A., 2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99-117, https://doi.org/10.1146/annurev-ento-120811-153645.
Cole, L.M., Nicholson, R.A. and Casida, J.E., 1993. Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pesticide Biochemistry and Physiology, 46(1), 47-54, https://doi.org/10.1006/pest.1993.1035.
Cole, L.M., Roush, R.T. and Casida, J.E., 1995. Drosophila GABA-gated chloride channel: modified [3H]EBOB binding site associated with Ala-->Ser or Gly mutants of Rdl subunit. Life Sciences, 56(10), 757-765, https://doi.org/10.1016/0024-3205(95)00006-R.
Ffrench-Constant, R.H., Anthony, N., Aronstein, K., Rocheleau, T. and Stilwell, G., 2000. Cyclodiene insecticide resistance: from molecular to population genetics. Annual Review of Entomology, 45(1), 449-466, https://doi.org/10.1146/annurev.ento.45.1.449.
Narahashi, T., 1988. Molecular and cellular approaches to neurotoxicology: past, present and future. Proceedings of Neurotox '88, Molecular Basis of Drug and Pesticide Action, Nottingham, England, April 10-15, 1988, pp. 269-288.
Dong, K., 2007. Insect sodium channels and insecticide resistance. Invertebrate Neuroscience, 7(1), 17-30, https://doi.org/10.1007/s10158-006-0036-9.
Rinkevich, F.D., Du, Y. and Dong, K., 2013. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pesticide Biochemistry and Physiology, 106(3), 93-100, https://doi.org/10.1016/j.pestbp.2013.02.007.
Soderlund, D., 2005. Sodium channels. In: G.I. Lawrence, ed. Comprehensive Molecular Insect Science. Amsterdam: Elsevier, pp. 1-24.
Oliveira, E.E., Du, Y., Nomura, Y. and Dong, K., 2013. A residue in the transmembrane segment 6 of domain I in insect and mammalian sodium channels regulate differential sensitivities to pyrethroid insecticides. NeuroToxicology, 38, 42-50, https://doi.org/10.1016/j.neuro.2013.06.001.
Du, W., Awolola, T.S., Howell, P., Koekemoer, L.L., Brooke, B.D., Benedict, M.Q., Coetzee, M. and Zheng, L., 2005. Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Molecular Biology, 14(2), 179-183, https://doi.org/10.1111/j.1365-2583.2005.00544.x.
Knipple, D.C., Doyle, K.E., Marsella-Herrick, P.A. and Soderlund, D.M., 1994. Tight genetic linkage between the kdr insecticide resistance trait and a voltage-sensitive sodium channel gene in the house fly. Proceedings of the National Academy of Sciences, 91(7), 2483-2487, https://doi.org/10.1073/pnas.91.7.2483.
Li, T., Zhang, L., Reid, W.R., Xu, Q., Dong, K. and Liu, N., 2012. Multiple mutations and mutation combinations in the sodium channel of permethrin resistant mosquitoes, Culex quinquefasciatus. Scientific Reports, 2, https://doi.org/10.1038/srep00781.
Martinez‐Torres, D., Chandre, F., Williamson, M., Darriet, F., Berge, J.B., Devonshire, A. L., Guillet, P., Pasteur, N. and Pauron, D., 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae ss. Insect Molecular Biology, 7(2), 179-184, https://doi.org/10.1046/j.1365-2583.1998.72062.x
Davies, T.G., Field, L.M., Usherwood, P.N. and Williamson, M.S., 2007. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life, 59(3), 151-162, https://doi.org/10.1080/15216540701352042.
Du, Y., Nomura, Y., Satar, G., Hu, Z., Nauen, R., He, S.Y., Zhorov, B.S. and Dong, K., 2013. Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel. Proceedings of the National Academy of Sciences, 110(29), 11785-11790, https://doi.org/10.1073/pnas.1305118110.
Srisawat, R., Komalamisra, N., Eshita, Y., Zheng, M., Ono, K., Itoh, T.Q., Matsumoto, A., Petmitr, S. and Rongsriyam, Y., 2010. Point mutations in domain II of the voltage-gated sodium channel gene in deltamethrin-resistant Aedes aegypti (Diptera: Culicidae). Applied Entomology and Zoology, 45(2), 275-282, https://doi.org/10.1303/aez.2010.275.
Singh, O.P., Dykes, C.L., Das, M.K., Pradhan, S., Bhatt, R.M., Agrawal, O.P. and Adak, T., 2010. Presence of two alternative kdr-like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel of Anopheles culicifacies from Orissa, India. Malaria Journal, 9(1), https://doi.org/10.1186/1475-2875-9-146.
Jones, C.M., Liyanapathirana, M., Agossa, F.R., Weetman, D., Ranson, H., Donnelly, M. J. and Wilding, C.S., 2012. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proceedings of the National Academy of Sciences, 109(17), 6614-6619, https://doi.org/10.1073/pnas.1201475109.
Chang, C., Shen, W.-K., Wang, T.-T., Lin, Y.-H., Hsu, E.-L. and Dai, S.-M., 2009. A novel amino acid substitution in a voltage-gated sodium channel is associated with knockdown resistance to permethrin in Aedes aegypti. Insect Biochemistry and Molecular Biology, 39(4), 272-278, https://doi.org/10.1016/j.ibmb.2009.01.001.
SupYoon, K., Symington, S.B., Hyeock Lee, S., Soderlund, D.M. and Marshall Clark, J., 2008. Three mutations identified in the voltage-sensitive sodium channel alpha-subunit gene of permethrin-resistant human head lice reduce the permethrin sensitivity of house fly Vssc1 sodium channels expressed in Xenopus oocytes. Insect Biochemistry and Molecular Biology, 38(3), 296-306, https://doi.org/10.1016/j.ibmb.2007.11.011.
Petersen, R.A., Niamsup, H., Berenbaum, M.R. and Schuler, M.A., 2003. Transcriptional response elements in the promoter of CYP6B1, an insect P450 gene regulated by plant chemicals. Biochimica et Biophysica Acta (BBA) - General Subjects, 1619(3), 269-282, https://doi.org/10.1016/S0304-4165(02)00486-5.
Wang, D., Johnson, A.D., Papp, A.C., Kroetz, D.L. and Sadee, W., 2005. Multidrug resistance polypeptide 1 (MDR1, ABCB1) variant 3435C>T affects mRNA stability. Pharmacogenetics and Genomics, 15(10), 693-704, https://doi.org/10.1097/01.fpc.0000178311.02878.83.
Gupta, S., Majumdar, S., Bhattacharya, T. and Ghosh, T., 2000. Studies on the relationships between the synonymous codon usage and protein secondary structural units. Biochemical and Biophysical Research Communications, 269(3), 692-696, https://doi.org/10.1006/bbrc.2000.2351.
Kimchi-Sarfaty, C., Oh, J. M., Kim, I.-W., Sauna, Z.E., Calcagno, A.M., Ambudkar, S.V., and Gottesman, M.M., 2007. A silent polymorphism in the MDR1 gene changes substrate specificity. Science, 315(5811), 525-528, https://doi.org/10.1126/science.1135308.
Alout, H. and Weill, M., 2008. Amino-acid substitutions in acetylcholinesterase 1 involved in insecticide resistance in mosquitoes. Chemico-Biological Interactions, 175(1-3), 138-141, https://doi.org/10.1016/j.cbi.2008.03.018.
Weill, M., Fort, P., Berthomieu, A., Dubois, M.P., Pasteur, N. and Raymond, M., 2002. A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene Drosophila. Proceedings of the Royal Society of London B: Biological Sciences, 269(1504), 2007-2016, https://doi.org/10.1098/rspb.2002.2122.
Weill, M., Lutfalla, G., Mogensen, K., Chandre, F., Berthomieu, A., Berticat, C., Pasteur, N., Philips, A., Fort, P. and Raymond, M., 2003. Comparative genomics: Insecticide resistance in mosquito vectors. Nature, 423, 136-137, https://doi.org/10.1038/423136b.
Xu, Q., Wang, H., Zhang, L. and Liu, N., 2006. Sodium channel gene expression associated with pyrethroid resistant house flies and German cockroaches. Gene, 379, 62-67, https://doi.org/10.1016/j.gene.2006.04.013.
Anazawa, Y., Tomita, T., Aiki, Y., Kozaki, T. and Kono, Y., 2003. Sequence of a cDNA encoding acetylcholinesterase from susceptible and resistant two-spotted spider mite, Tetranychus urticae. Insect Biochemistry and Molecular Biology, 33(5), 509-514, https://doi.org/10.1016/S0965-1748(03)00025-0.
Alon, M., Alon, F., Nauen, R. and Morin, S., 2008. Organophosphates' resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochemistry and Molecular Biology, 38(10), 940-949, https://doi.org/10.1016/j.ibmb.2008.07.007.
Bloomquist, J.R., 2003. Chloride channels as tools for developing selective insecticides. Archives of Insect Biochemistry and Physiology, 54, 145-156, https://doi.org/10.1002/arch.10112.
Rocheleau, T.A., Steichen, J.C. and Chalmers, A.E., 1993. A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature, 363, 449-451, https://doi.org/10.1038/363449a0.
Wondji, C.S., Dabire, R.K., Tukur, Z., Irving, H., Djouaka, R. and Morgan, J.C., 2011. Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochemistry and Molecular Biology, 41(7), 484-491, https://doi.org/10.1016/j.ibmb.2011.03.012.
Davari, B., Vatandoost, H., Oshaghi, M., Ladonni, H., Enayati, A., Shaeghi, M., Basseri, H., Rassi, Y. and Hanafi-Bojd, A., 2007. Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spectrum to pyrethroids and fipronil. Pesticide Biochemistry and Physiology, 89(2), 97-103, https://doi.org/10.1016/j.pestbp.2007.04.003.
Liu, H., Cupp, E.W., Micher, K.M., Guo, A. and Liu, N., 2004. Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefaciatus. Journal of Medical Entomology, 41(3), 408-413, https://doi.org/10.1603/0022-2585-41.3.408.
Feyereisen, R., 2005. Insect Cytochrome P450. In: L.I. Gilbert, ed. Comprehensive Molecular Insect Science. Amsterdam: Elsevier, pp. 1-77.
Ketterman, A.J., Saisawang, C. and Wongsantichon, J., 2011. Insect glutathione transferases. Drug Metabolism Reviews, 43(2), 253-265, https://doi.org/10.3109/03602532.2011.552911.
Ranson, H. and Hemingway, J., 2005. Mosquito glutathione transferases. Methods in Enzymology, 401, 226-241, https://doi.org/10.1016/S0076-6879(05)01014-1.
Ranson, H., Rossiter, L., Ortelli, F., Jensen, B., Wang, X., Roth, C. W., Collins, F. H. and Hemingway, J., 2001. Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochemical Journal, 359(2), 295-304, https://doi.org/10.1042/0264-6021:3590295.
Itokawa, K., Komagata, O., Kasai, S., Okamura, Y., Masada, M. and Tomita, T., 2010. Genomic structures of Cyp9m10 in pyrethroid resistant and susceptible strains of Culex quinquefasciatus. Insect Biochemistry and Molecular Biology, 40(9), 631-640, https://doi.org/10.1016/j.ibmb.2010.06.001.
Riveron, J.M., Irving, H., Ndula, M., Barnes, K.G., Ibrahim, S.S., Paine, M.J. and Wondji, C.S., 2013. Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proceedings of the National Academy of Sciences, 110(1), 252-257, https://doi.org/10.1073/pnas.1216705110.
Wondji, C.S., Irving, H., Morgan, J., Lobo, N.F., Collins, F.H., Hunt, R.H., Coetzee, M., Hemingway, J. and Ranson, H., 2009. Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Research, 19(3), 452-459, https://doi.org/10.1101/gr.087916.108.
Pasteur, N. and Raymond, M., 1996. Insecticide resistance genes in mosquitoes: their mutations, migration, and selection in field populations. Journal of Heredity, 87(6), 444-449, https://doi.org/10.1093/oxfordjournals.jhered.a023035.
Vaughan, A. and Hemingway, J., 1995. Mosquito carboxylesterase Estα21 (A2). Cloning and sequence of the full-length cDNA for a major insecticide resistance gene worldwide in the mosquito Culex quinquefasciatus. Journal of Biological Chemistry, 270(28), 17044-17049, https://doi.org/10.1074/jbc.270.28.17044.
Chiu, T.L., Wen, Z., Rupasinghe, S.G. and Schuler, M.A., 2008. Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proceedings of the National Academy of Sciences, 105(26), 8855-8860, https://doi.org/10.1073/pnas.0709249105.
Daborn, P.J., Lumb, C., Harrop, T.W., Blasetti, A., Pasricha, S., Morin, S., Mitchell, S.N., Donnelly, M. J., Muller, P. and Batterham, P., 2012. Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests. Insect Biochemistry and Molecular Biology, 42(12), 918-924, https://doi.org/10.1016/j.ibmb.2012.09.003.
Li, T., Liu, L., Zhang, L. and Liu, N., 2014. Role of G-protein-coupled receptor-related genes in insecticide resistance of the mosquito, Culex quinquefasciatus. Scientific Reports, 4, https://doi.org/10.1038/srep06474.
Kleinschmidt, I., Bradley, J., Knox, T.B., Mnzava, A.P., Kafy, H.T., Mbogo, C., Ismail, B.A., Bigoga, J.D., Adechoubou, A., Raghavendra, K., Cook, J., Malik, E.M., Nkuni, Z.J., Macdonald, M., Bayoh, N., Ochomo, E., Fondjo, E., Awono-Ambene, H.P., Etang, J., Akogbeto, M., Bhatt, R.M., Chourasia, M.K., Swain, D.K., Kinyari, T., Subramaniam, K., Massougbodji, A., Oke-Sopoh, M., Ogouyemi-Hounto, A., Kouambeng, C., Abdin, M.S., West, P., Elmardi, K., Cornelie, S., Corbel, V., Valecha, N., Mathenge, E., Kamau, L., Lines, J. and Donnelly, M.J., 2018. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infectious Diseases, 18(6), 640-649, https://doi.org/10.1016/S1473-3099(18)30172-5.
N’Guessan, R., Corbel, V., Akogbeto, M. and Rowland, M., 2007. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerging Infectious Diseases, 13(2), 199-206, https://doi.org/10.3201/eid1302.060631.
Rivero, A., Vezilier, J., Weill, M., Read, A.F. and Gandon, S., 2010. Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PloS pathogens, 6(8), https://doi.org/10.1371/journal.ppat.1001000.
Alout, H., Roche, B., Dabire, R.K. and Cohuet, A., 2017. Consequences of insecticide resistance on malaria transmission. PLOS Pathogens, 13(9), https://doi.org/10.1371/journal.ppat.1006499.
Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. and Reich, D., 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38(8), 904-909, https://doi.org/10.1038/ng1847.
Pritchard, J.K., Stephens, M. and Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959, https://doi.org/10.1093/genetics/155.2.945.
Armitage, P., 1955. Tests for linear trends in proportions and frequencies. Biometrics, 11(3), 375-386, https://doi.org/10.2307/3001775.
Storey, J.D and Tibshirani, R., 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, 100(16), 9440-9445, https://doi.org/10.1073/pnas.1530509100.
Smith, J.M. and Haigh, J., 1974. The hitch-hiking effect of a favourable gene. Genetics Research, 23(1), 23-35, https://doi.org/10.1017/S0016672300014634.
Ronald, J. and Akey, J.M., 2005. Genome-wide scans for loci under selection in humans. Human Genomics, 2(2), 113-25, https://doi.org/10.1186/1479-7364-2-2-113.
Akey, J.M., Eberle, M.A., Rieder, M.J., Carlson, C.S., Shriver, M.D., Nickerson, D.A. and Kruglyak, L., 2004. Population history and natural selection shape patterns of genetic variation in 132 genes. PLOS Biology, 2(10), https://doi.org/10.1371/journal.pbio.0020286.
Vieira, M.L.C., Santini, L., Diniz, A.L. and Munhoz, C.D.F., 2016. Microsatellite markers: what they mean and why they are so useful. Genetics and Molecular Biology, 39(3), 312-328, https://doi.org/10.1590/1678-4685-GMB-2016-0027.
Barton, N.H. and Keightley, P.D., 2002. Understanding quantitative genetic variation. Nature Reviews Genetics, 3(1), 11-21, https://doi.org/10.1038/nrg700.
Fisher, R., 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press.
Daborn, P., Boundy, S., Yen, J., Pittendrigh, B. and ffrench-Constant, R., 2001. DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Molecular Genetics and Genomics, 266(4), 556-563, https://doi.org/10.1007/s004380100531.
Kaplan, N.L., Hudson, R. and Langley, C., 1989. The hitchhiking effect revisited. Genetics, 123(4), 887-899, https://doi.org/10.1093/genetics/123.4.887.
Hermisson, J. and Pennings, P.S., 2005. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics, 169(4), 2335-2352, https://doi.org/10.1534/genetics.104.036947.
Pennings, P.S. and Hermisson, J., 2006. Soft sweeps II--molecular population genetics of adaptation from recurrent mutation or migration. Molecular Biology and Evolution, 23(5), 1076-1084, https://doi.org/10.1093/molbev/msj117.
Orr, H.A. and Betancourt, A.J., 2001. Haldane9s sieve and adaptation from the standing genetic variation. Genetics, 157(2), 875-884, https://doi.org/10.1093/genetics/157.2.875.
Innan, H. and Kim, Y., 2004. Pattern of polymorphism after strong artificial selection in a domestication event. Proceedings of the National Academy of Sciences, 101(29), 10667-10672, https://doi.org/10.1073/pnas.0401720101.
Arendt, J. and Reznick, D., 2008. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology and Evolution, 23(1), 26-32, https://doi.org/10.1016/j.tree.2007.09.011.
Coop, G., Pickrell, J.K., Novembre, J., Kudaravalli, S., Li, J., Absher, D., Myers, R.M., Cavalli-Sforza, L.L., Feldman, M.W. and Pritchard, J.K., 2009. The role of geography in human adaptation. PLOS Genetics, 5(6), https://doi.org/10.1371/journal.pgen.1000500.
Ralph, P. and Coop, G., 2010. Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics, 186(2), 647-68, https://doi.org/10.1534/genetics.110.119594.
Novembre, J. and Han, E., 2012. Human population structure and the adaptive response to pathogen-induced selection pressures. Philosophical Transactions of the Royal Society B, 367(1590), 878-886, https://doi.org/10.1098/rstb.2011.0305.
Kim, Y. and Stephan, W., 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics, 160(2), 765-777, https://doi.org/10.1093/genetics/160.2.765.
Fay, J.C. and Wu, C.I., 2000. Hitchhiking under positive Darwinian selection. Genetics, 155(3), 1405-1413, https://doi.org/10.1093/genetics/155.3.1405.
Slatkin, M. and Hudson, R.R., 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129(2), 555-562, https://doi.org/10.1093/genetics/129.2.555.
Barton, N.H., 1998. The effect of hitch-hiking on neutral genealogies. Genetics Research, 72(2), 123-133, https://doi.org/10.1017/S0016672398003462.
Durrett, R. and Schweinsberg, J., 2004. Approximating selective sweeps. Theoretical Population Biology, 66(2), 129-138, https://doi.org/10.1016/j.tpb.2004.04.002.
Hudson, R.R., Bailey, K., Skarecky, D., Kwiatowski, J. and Ayala, F.J., 1994. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics, 136(4), 1329-1340, https://doi.org/10.1093/genetics/136.4.1329.
Hudson, R.R., Kreitman, M. and Aguade, M., 1987. A test of neutral molecular evolution based on nucleotide data. Genetics, 116(1), 153-159, https://doi.org/10.1093/genetics/116.1.153.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3), 585-595, https://doi.org/10.1093/genetics/123.3.585.
Przeworski, M., Coop, G. and Wall, J.D., 2005. The signature of positive selection on standing genetic variation. Evolution, 59(11), 2312-2323, https://doi.org/10.1111/j.0014-3820.2005.tb00941.x.
Pennings, P.S. and Hermisson, J., 2006. Soft sweeps III: the signature of positive selection from recurrent mutation. PLOS Genetics, 2(12), https://doi.org/10.1371/journal.pgen.0020186.
Cutter, A.D. and Payseur, B.A., 2013. Genomic signatures of selection at linked sites: unifying the disparity among species. Nature Reviews Genetics, 14(4), 262-274, https://doi.org/10.1038/nrg3425.
Williamson, S.H., Hubisz, M.J., Clark, A.G., Payseur, B.A., Bustamante, C.D. and Nielsen, R., 2007. Localizing recent adaptive evolution in the human genome. PLOS Genetics, 3(6), https://doi.org/10.1371/journal.pgen.0030090.
Hey, J., 2004. What's so hot about recombination hotspots? PLOS Biology, 2(6), https://doi.org/10.1371/journal.pbio.0020190.
Jiang, H., Li, N., Gopalan, V., Zilversmit, M.M., Varma, S., Nagarajan, V., Li, J., Mu, J., Hayton, K., Henschen, B., Yi, M., Stephens, R., McVean, G., Awadalla, P., Wellems, T.E. and Su, X.Z., 2011. High recombination rates and hotspots in a Plasmodium falciparum genetic cross. Genome Biology, 12(4), https://doi.org/10.1186/gb-2011-12-4-r33.
Mu, J., Awadalla, P., Duan, J., McGee, K.M., Joy, D.A., McVean, G.A. and Su, X.Z., 2005. Recombination hotspots and population structure in Plasmodium falciparum. PLOS Biology, 3(10), https://doi.org/10.1371/journal.pbio.0030335.