Mosquito genomes are frequently invaded by transposable elements through horizontal transfer

Autoři: Elverson Soares de Melo aff001;  Gabriel Luz Wallau aff001
Působiště autorů: Department of Entomology, Aggeu Magalhães Institute–Oswaldo Cruz Foundation (Fiocruz), Recife, Pernambuco, Brazil aff001
Vyšlo v časopise: Mosquito genomes are frequently invaded by transposable elements through horizontal transfer. PLoS Genet 16(11): e1008946. doi:10.1371/journal.pgen.1008946
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008946


Transposable elements (TEs) are mobile genetic elements that parasitize basically all eukaryotic species genomes. Due to their complexity, an in-depth TE characterization is only available for a handful of model organisms. In the present study, we performed a de novo and homology-based characterization of TEs in the genomes of 24 mosquito species and investigated their mode of inheritance. More than 40% of the genome of Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus is composed of TEs, while it varied substantially among Anopheles species (0.13%–19.55%). Class I TEs are the most abundant among mosquitoes and at least 24 TE superfamilies were found. Interestingly, TEs have been extensively exchanged by horizontal transfer (172 TE families of 16 different superfamilies) among mosquitoes in the last 30 million years. Horizontally transferred TEs represents around 7% of the genome in Aedes species and a small fraction in Anopheles genomes. Most of these horizontally transferred TEs are from the three ubiquitous LTR superfamilies: Gypsy, Bel-Pao and Copia. Searching more than 32,000 genomes, we also uncovered transfers between mosquitoes and two different Phyla—Cnidaria and Nematoda—and two subphyla—Chelicerata and Crustacea, identifying a vector, the worm Wuchereria bancrofti, that enabled the horizontal spread of a Tc1-mariner element among various Anopheles species. These data also allowed us to reconstruct the horizontal transfer network of this TE involving more than 40 species. In summary, our results suggest that TEs are frequently exchanged by horizontal transfers among mosquitoes, influencing mosquito's genome size and variability.

Klíčová slova:

Anopheles gambiae – Bird genomics – Computer software – Genomics – Invertebrate genomics – Mosquitoes – Plant genomics – Transposable elements


1. McClintock B. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci. 1950;36: 344–355. doi: 10.1073/pnas.36.6.344 15430309

2. Ravindran S. Barbara McClintock and the discovery of jumping genes. Proc Natl Acad Sci. 2012;109: 20198–20199. doi: 10.1073/pnas.1219372109 23236127

3. Biémont C, Vieira C. Genetics: Junk DNA as an evolutionary force. Nature. 2006;443: 521–524. doi: 10.1038/443521a 17024082

4. Cowley M, Oakey RJ. Transposable Elements Re-Wire and Fine-Tune the Transcriptome. PLOS Genet. 2013;9: 1–7. doi: 10.1371/journal.pgen.1003234 23358118

5. Schrader L, Kim JW, Ence D, Zimin A, Klein A, Wyschetzki K, et al. Transposable element islands facilitate adaptation to novel environments in an invasive species. Nat Commun. 2014;5: 1–10. doi: 10.1038/ncomms6495 25510865

6. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet. 2017;18: 71–86. doi: 10.1038/nrg.2016.139 27867194

7. Jangam D, Feschotte C, Betrán E. Transposable Element Domestication As an Adaptation to Evolutionary Conflicts. Trends Genet. 2017;33: 817–831. doi: 10.1016/j.tig.2017.07.011 28844698

8. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8: 973–982. doi: 10.1038/nrg2165 17984973

9. Kapitonov V V, Jurka J. A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet. 2008;9: 411–412. doi: 10.1038/nrg2165-c1 18421312

10. Kojima KK. Structural and sequence diversity of eukaryotic transposable elements. Genes Genet Syst. 2019;94: 233–252. doi: 10.1266/ggs.18-00024 30416149

11. Haapa-Paananen S, Wahlberg N, Savilahti H. Phylogenetic analysis of Maverick/Polinton giant transposons across organisms. Mol Phylogenet Evol. 2014;78: 271–274. doi: 10.1016/j.ympev.2014.05.024 24882428

12. Kapitonov V V., Jurka J. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 2001;98: 8714–8719. doi: 10.1073/pnas.151269298 11447285

13. McDonald JF. Evolution and consequences of transposable elements. Curr Opin Genet Dev. 1993;3: 855–864. doi: 10.1016/0959-437x(93)90005-a 8118210

14. Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics. 1990;124: 339–55. 2155157

15. Peccoud J, Loiseau V, Cordaux R, Gilbert C. Massive horizontal transfer of transposable elements in insects. Proc Natl Acad Sci. 2017;114: 4721–4726. doi: 10.1073/pnas.1621178114 28416702

16. Wallau GL, Vieira C, Loreto ÉLS. Genetic exchange in eukaryotes through horizontal transfer: Connected by the mobilome. Mob DNA. 2018;9: 1–16. doi: 10.1186/s13100-017-0106-z 29308092

17. Cummings MP. Transmission patterns of eukaryotic transposable elements: arguments for and against horizontal transfer. Trends Ecol Evol. 1994;9: 141–145. doi: 10.1016/0169-5347(94)90179-1 21236798

18. Wallau GL, Ortiz MF, Loreto ELS. Horizontal transposon transfer in eukarya: Detection, bias, and perspectives. Genome Biol Evol. 2012;4: 689–699. doi: 10.1093/gbe/evs055 22798449

19. Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol. 2010;25: 537–546. doi: 10.1016/j.tree.2010.06.001 20591532

20. Peccoud J, Cordaux R, Gilbert C. Analyzing Horizontal Transfer of Transposable Elements on a Large Scale: Challenges and Prospects. BioEssays. 2018;40: 1–8. doi: 10.1002/bies.201700177 29283188

21. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 Maize Genome: Complexity, Diversity, and Dynamics. Science (80-). 2009;326: 1112–1115. doi: 10.1126/science.1178534 19965430

22. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu Z, et al. Genome Sequence of Aedes aegypti, a Major Arbovirus Vector. Science (80-). 2007;316: 1718–1723. doi: 10.1126/science.1138878 17510324

23. Foster WA, Walker ED. Mosquitoes (Culicidae). Medical and Veterinary Entomology. Elsevier; 2019. pp. 261–325. doi: 10.1016/B978-0-12-814043-7.00015–7

24. Benelli G, Mehlhorn H. Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitol Res. 2016;115: 1747–1754. doi: 10.1007/s00436-016-4971-z 26932263

25. Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA, Allen JE, et al. Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes. Science (80-). 2015;347: 1258522. doi: 10.1126/science.1258522 25554792

26. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, Antelo B, et al. Sequencing of Culex quinquefasciatus Establishes a Platform for Mosquito Comparative Genomics. Science (80-). 2010;330: 86–88. doi: 10.1126/science.1191864 20929810

27. Chen X-G, Jiang X, Gu J, Xu M, Wu Y, Deng Y, et al. Genome sequence of the Asian Tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution. Proc Natl Acad Sci. 2015;112: E5907–E5915. doi: 10.1073/pnas.1516410112 26483478

28. Logue K, Small ST, Chan ER, Reimer L, Siba PM, Zimmerman PA, et al. Whole-genome sequencing reveals absence of recent gene flow and separate demographic histories for Anopheles punctulatus mosquitoes in Papua New Guinea. Mol Ecol. 2015;24: 1263–1274. doi: 10.1111/mec.13107 25677924

29. Marinotti O, Cerqueira GC, de Almeida LGP, Ferro MIT, Loreto EL da S, Zaha A, et al. The Genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res. 2013;41: 7387–7400. doi: 10.1093/nar/gkt484 23761445

30. Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 2015;6: 11. doi: 10.1186/s13100-015-0041-9 26045719

31. Dotto BR, Carvalho EL, da Silva AF, Dezordi FZ, Pinto PM, Campos TDL, et al. HTT-DB: new features and updates. Database. 2018;2018: 1–5. doi: 10.1093/database/bax102 29315358

32. Barrón MG, Paupy C, Rahola N, Akone-Ella O, Ngangue MF, Wilson-Bahun TA, et al. A new species in the major malaria vector complex sheds light on reticulated species evolution. Sci Rep. 2019;9: 1–13. doi: 10.1038/s41598-018-37186-2 30626917

33. Wallau GL, Capy P, Loreto E, Le Rouzic A, Hua-Van A. VHICA, a New Method to Discriminate between Vertical and Horizontal Transposon Transfer: Application to the Mariner Family within Drosophila. Mol Biol Evol. 2016;33: 1094–1109. doi: 10.1093/molbev/msv341 26685176

34. Biedler JK, Chen X, Tu Z. Horizontal transmission of an R4 clade non-long terminal repeat retrotransposon between the divergent Aedes and Anopheles mosquito genera. Insect Mol Biol. 2015;24: 331–337. doi: 10.1111/imb.12160 25615532

35. Tang C, Davis KE, Delmer C, Yang D, Wills MA. Elevated atmospheric CO2 promoted speciation in mosquitoes (Diptera, Culicidae). Commun Biol. 2018;1: 1–8. doi: 10.1038/s42003-017-0002-6 29809203

36. Gilbert C, Feschotte C. Horizontal acquisition of transposable elements and viral sequences: patterns and consequences. Curr Opin Genet Dev. 2018;49: 15–24. doi: 10.1016/j.gde.2018.02.007 29505963

37. Bennetzen JL, Wang H. The Contributions of Transposable Elements to the Structure, Function, and Evolution of Plant Genomes. Annu Rev Plant Biol. 2014;65: 505–530. doi: 10.1146/annurev-arplant-050213-035811 24579996

38. Ito H, Kakutani T. Control of transposable elements in Arabidopsis thaliana. Chromosom Res. 2014;22: 217–223. doi: 10.1007/s10577-014-9417-9 24801341

39. Hirano T, Siomi H. Small RNAs: Artificial piRNAs for Transcriptional Silencing. Curr Biol. 2015;25: R280–R283. doi: 10.1016/j.cub.2015.02.009 25829012

40. Saito K, Siomi MC. Small RNA-Mediated Quiescence of Transposable Elements in Animals. Dev Cell. 2010;19: 687–697. doi: 10.1016/j.devcel.2010.10.011 21074719

41. Platt RN, Vandewege MW, Ray DA. Mammalian transposable elements and their impacts on genome evolution. Chromosom Res. 2018;26: 25–43. doi: 10.1007/s10577-017-9570-z 29392473

42. Friedli M, Trono D. The Developmental Control of Transposable Elements and the Evolution of Higher Species. Annu Rev Cell Dev Biol. 2015;31: 429–451. doi: 10.1146/annurev-cellbio-100814-125514 26393776

43. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, et al. The Genome Sequence of the Malaria Mosquito Anopheles gambiae. Science (80-). 2002;298: 129–149. doi: 10.1126/science.1076181 12364791

44. Goerner-Potvin P, Bourque G. Computational tools to unmask transposable elements. Nat Rev Genet. 2018;19: 688–704. doi: 10.1038/s41576-018-0050-x 30232369

45. Berthelier J, Casse N, Daccord N, Jamilloux V, Saint-Jean B, Carrier G. A transposable element annotation pipeline and expression analysis reveal potentially active elements in the microalga Tisochrysis lutea. BMC Genomics. 2018;19: 1–14. doi: 10.1186/s12864-017-4368-0 29291715

46. Marsano RM, Leronni D, D’Addabbo P, Viggiano L, Tarasco E, Caizzi R. Mosquitoes LTR Retrotransposons: A Deeper View into the Genomic Sequence of Culex quinquefasciatus. PLoS One. 2012;7: e30770. doi: 10.1371/journal.pone.0030770 22383973

47. Petersen M, Armisén D, Gibbs RA, Hering L, Khila A, Mayer G, et al. Diversity and evolution of the transposable element repertoire in arthropods with particular reference to insects. BMC Evol Biol. 2019;19: 11. doi: 10.1186/s12862-018-1324-9 30626321

48. Chalopin D, Naville M, Plard F, Galiana D, Volff JN. Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol. 2015;7: 567–580. doi: 10.1093/gbe/evv005 25577199

49. Lu J, Peatman E, Tang H, Lewis J, Liu Z. Profiling of gene duplication patterns of sequenced teleost genomes: evidence for rapid lineage-specific genome expansion mediated by recent tandem duplications. BMC Genomics. 2012;13: 246. doi: 10.1186/1471-2164-13-246 22702965

50. Wang N, Xiang Y, Fang L, Wang Y, Xin H, Li S. Patterns of Gene Duplication and Their Contribution to Expansion of Gene Families in Grapevine. Plant Mol Biol Report. 2013;31: 852–861. doi: 10.1007/s11105-013-0556-5

51. Silva JC, Loreto EL, Clark JB. Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol. 2004;6: 57–71. 14632259

52. Baidouri M El, Carpentier MC, Cooke R, Gao D, Lasserre E, Llauro C, et al. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res. 2014;24: 831–838. doi: 10.1101/gr.164400.113 24518071

53. Metzger MJ, Paynter AN, Siddall ME, Goff SP. Horizontal transfer of retrotransposons between bivalves and other aquatic species of multiple phyla. Proc Natl Acad Sci. 2018;115: E4227–E4235. doi: 10.1073/pnas.1717227115 29669918

54. Gao D, Chu Y, Xia H, Xu C, Heyduk K, Abernathy B, et al. Horizontal transfer of Non-LTR retrotransposons from arthropods to flowering plants. Mol Biol Evol. 2018;35: 354–364. doi: 10.1093/molbev/msx275 29069493

55. Oliveira SG, Bao W, Martins C, Jurka J. Horizontal transfers of Mariner transposons between mammals and insects. Mob DNA. 2012;3: 1–6. doi: 10.1186/1759-8753-3-1 22277150

56. Gilbert C, Schaack S, Pace II JK, Brindley PJ, Feschotte C. A role for host–parasite interactions in the horizontal transfer of transposons across phyla. Nature. 2010;464: 1347–1350. doi: 10.1038/nature08939 20428170

57. Palazzo A, Lorusso P, Miskey C, Walisko O, Gerbino A, Marobbio CMT, et al. Transcriptionally promiscuous “blurry” promoters in Tc1/mariner transposons allow transcription in distantly related genomes. Mob DNA. 2019;10: 1–11. doi: 10.1186/s13100-018-0144-1 30622655

58. Reiss D, Mialdea G, Miele V, de Vienne DM, Peccoud J, Gilbert C, et al. Global survey of mobile DNA horizontal transfer in arthropods reveals Lepidoptera as a prime hotspot. Buerkle A, editor. PLOS Genet. 2019;15: e1007965. doi: 10.1371/journal.pgen.1007965 30707693

59. Manguin S, Bangs MJ, Pothikasikorn J, Chareonviriyaphap T. Review on global co-transmission of human Plasmodium species and Wuchereria bancrofti by Anopheles mosquitoes. Infect Genet Evol. 2010;10: 159–177. doi: 10.1016/j.meegid.2009.11.014 19941975

60. Suh A, Witt CC, Menger J, Sadanandan KR, Podsiadlowski L, Gerth M, et al. Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes. Nat Commun. 2016;7: 11396. doi: 10.1038/ncomms11396 27097561

61. Van den Berg H, Kelly-Hope LA, Lindsay SW. Malaria and lymphatic filariasis: The case for integrated vector management. Lancet Infect Dis. 2013;13: 89–94. doi: 10.1016/S1473-3099(12)70148-2 23084831

62. Thurmond J, Goodman JL, Strelets VB, Attrill H, Gramates LS, Marygold SJ, et al. FlyBase 2.0: the next generation. Nucleic Acids Res. 2019;47: D759–D765. doi: 10.1093/nar/gky1003 30364959

63. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479: 487–492. doi: 10.1038/nature10640 22113690

64. Giraldo-Calderón GI, Emrich SJ, MacCallum RM, Maslen G, Dialynas E, Topalis P, et al. VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Res. 2015;43: D707–D713. doi: 10.1093/nar/gku1117 25510499

65. Kitts PA, Church DM, Thibaud-Nissen F, Choi J, Hem V, Sapojnikov V, et al. Assembly: a resource for assembled genomes at NCBI. Nucleic Acids Res. 2016;44: D73–D80. doi: 10.1093/nar/gkv1226 26578580

66. Sharakhova M V., Hammond MP, Lobo NF, Krzywinski J, Unger MF, Hillenmeyer ME, et al. Update of the Anopheles gambiae PEST genome assembly. Genome Biol. 2007;8: R5. doi: 10.1186/gb-2007-8-1-r5 17210077

67. Lawniczak MKN, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, et al. Widespread Divergence Between Incipient Anopheles gambiae Species Revealed by Whole Genome Sequences. Science (80-). 2010;330: 512–514. doi: 10.1126/science.1195755 20966253

68. Ghurye J, Koren S, Small ST, Redmond S, Howell P, Phillippy AM, et al. A chromosome-scale assembly of the major African malaria vector Anopheles funestus. Gigascience. 2019;8: 1–8. doi: 10.1093/gigascience/giz063 31157884

69. Chida AR, Ravi S, Jayaprasad S, Paul K, Saha J, Suresh C, et al. A near-chromosome level genome assembly of Anopheles stephensi. bioRxiv:063040 [preprint]. 2020. doi: 10.1101/2020.04.27.063040

70. Matthews BJ, Dudchenko O, Kingan SB, Koren S, Antoshechkin I, Crawford JE, et al. Improved reference genome of Aedes aegypti informs arbovirus vector control. Nature. 2018;563: 501–507. doi: 10.1038/s41586-018-0692-z 30429615

71. Kingan SB, Heaton H, Cudini J, Lambert CC, Baybayan P, Galvin BD, et al. A high-quality de novo genome assembly from a single mosquito using pacbio sequencing. Genes (Basel). 2019;10. doi: 10.3390/genes10010062 30669388

72. Palatini U, Masri RA, Cosme L V., Koren S, Thibaud-Nissen F, Biedler JK, et al. Improved reference genome of the arboviral vector Aedes albopictus. Genome Biol. 2020;21: 215. doi: 10.1186/s13059-020-02141-w 32847630

73. Hahn C, Bachmann L, Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res. 2013;41: e129–e129. doi: 10.1093/nar/gkt371 23661685

74. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol. 2010;59: 307–321. doi: 10.1093/sysbio/syq010 20525638

75. Lefort V, Longueville J-E, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol. 2017;34: 2422–2424. doi: 10.1093/molbev/msx149 28472384

76. Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2015. Available:

77. Zytnicki M, Akhunov E, Quesneville H. Tedna: A transposable element de novo assembler. Bioinformatics. 2014;30: 2656–2658. doi: 10.1093/bioinformatics/btu365 24894500

78. Goubert C, Modolo L, Vieira C, ValienteMoro C, Mavingui P, Boulesteix M. De Novo Assembly and Annotation of the Asian Tiger Mosquito (Aedes albopictus) Repeatome with dnaPipeTE from Raw Genomic Reads and Comparative Analysis with the Yellow Fever Mosquito (Aedes aegypti). Genome Biol Evol. 2015;7: 1192–1205. doi: 10.1093/gbe/evv050 25767248

79. Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35: W265–W268. doi: 10.1093/nar/gkm286 17485477

80. Bao Z, Eddy SR. Automated De Novo Identification of Repeat Sequence Families in Sequenced Genomes. Genome Res. 2002;12: 1269–1276. doi: 10.1101/gr.88502 12176934

81. Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics. 2005;21: 351–358. doi: 10.1093/bioinformatics/bti1018 15961478

82. Edgar RC, Myers EW. PILER: Identification and classification of genomic repeats. Bioinformatics. 2005;21: 152–158. doi: 10.1093/bioinformatics/bth487 15377504

83. Novák P, Neumann P, Pech J, Steinhaisl J, MacAs J. RepeatExplorer: A Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29: 792–793. doi: 10.1093/bioinformatics/btt054 23376349

84. Flutre T, Duprat E, Feuillet C, Quesneville H. Considering transposable element diversification in de novo annotation approaches. PLoS One. 2011;6: 1–15. doi: 10.1371/journal.pone.0016526 21304975

85. Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22: 1658–1659. doi: 10.1093/bioinformatics/btl158 16731699

86. Hoede C, Arnoux S, Moisset M, Chaumier T, Inizan O, Jamilloux V, et al. PASTEC: An automatic transposable element classification tool. PLoS One. 2014;9. doi: 10.1371/journal.pone.0091929 24786468

87. Zhang R-G, Wang Z-X, Ou S, Li G-Y. TEsorter: lineage-level classification of transposable elements using conserved protein domains. bioRxiv. 2019; 800177. doi: 10.1101/800177

88. Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci. 2020;117: 9451–9457. doi: 10.1073/pnas.1921046117 32300014

89. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16: 111–120. doi: 10.1007/BF01731581 7463489

90. Kassambara A. ggpubr: “ggplot2” Based Publication Ready Plots. 2018. Available:

91. Kriventseva E V., Rahman N, Espinosa O, Zdobnov EM. OrthoDB: the hierarchical catalog of eukaryotic orthologs. Nucleic Acids Res. 2007;36: D271–5. doi: 10.1093/nar/gkm845 17947323

92. Ranwez V, Harispe S, Delsuc F, Douzery EJP. MACSE: Multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS One. 2011;6. doi: 10.1371/journal.pone.0022594 21949676

93. Slotman M, della Torre A, Powell JR. The Genetics of Inviability and Male Sterility in Hybrids Between Anopheles gambiae and An. arabiensis. Genetics. 2004;167: 275–287. doi: 10.1534/genetics.167.1.275 15166154

94. Davidson G, Paterson HE, Coluzzi M, Mason GF, Micks DW. The Anopheles gambiae complex. In: Wright JW, Pal R, editors. Genetics of Insect Vector of Disease. Amsterdam: Elsevier Publishers; 1967. pp. 211–250.

95. Fortune PM, Roulin A, Panaud O. Horizontal transfer of transposable elements in plants. Commun Integr Biol. 2008;1: 74–77. doi: 10.4161/cib.1.1.6328 19513203

96. Graur D, Li W-H. Fundamentals of Molecular Evolution. 2nd ed. Sunderland: Sinauer Associates; 2000.

97. Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, et al. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010;3: 117. doi: 10.1186/1756-3305-3-117 21129198

98. Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011;4: 89. doi: 10.1186/1756-3305-4-89 21612587

99. Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010;3: 72. doi: 10.1186/1756-3305-3-72 20712879

100. Sinka ME. Global Distribution of the Dominant Vector Species of Malaria. Anopheles mosquitoes—New insights into malaria vectors. InTech; 2013. pp. 109–143. doi: 10.5772/54163

101. Hay SI, Snow RW. The Malaria Atlas Project: Developing global maps of malaria risk. PLoS Med. 2006;3: 2204–2208. doi: 10.1371/journal.pmed.0030473 17147467

102. Soghigian J, Gloria-Soria A, Robert V, Le Goff G, Failloux A, Powell JR. Genetic evidence for the origin of Aedes aegypti, the yellow fever mosquito, in the southwestern Indian Ocean. Mol Ecol. 2020; mec.15590. doi: 10.1111/mec.15590

103. Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species Aedes albopictus: Current knowledge and future perspectives. Trends Parasitol. 2013;29: 460–468. doi: 10.1016/ 23916878

104. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: A Resource for Timelines, Timetrees, and Divergence Times. Mol Biol Evol. 2017;34: 1812–1819. doi: 10.1093/molbev/msx116 28387841

105. Rivera-Vega L, Mittapalli O. Molecular characterization of mariner-like elements in emerald ash borer, agrilus planipennis (Coleoptera, Polyphaga). Arch Insect Biochem Physiol. 2010;74: 205–216. doi: 10.1002/arch.20357 20602451

106. Robertson HM, Lampe DJ. Distribution of transposable elements in arthropods. Annu Rev Entomol. 1995;40: 333–357. doi: 10.1146/annurev.en.40.010195.002001 7529010

107. Green CL, Frommer M. The genome of the Queensland fruit fly Bactrocera tryoni contains multiple representatives of the mariner family of transposable elements. Insect Mol Biol. 2001;10: 371–386. doi: 10.1046/j.0962-1075.2001.00275.x 11520360

108. Yoshiyama M, Tu Z, Kainoh Y, Honda H, Shono T, Kimura K. Possible horizontal transfer of a transposable element from host to parasitoid. Mol Biol Evol. 2001;18: 1952–1958. doi: 10.1093/oxfordjournals.molbev.a003735 11557800

109. Biedler JK, Shao H, Tu Z. Evolution and horizontal transfer of a DD37E DNA transposon in mosquitoes. Genetics. 2007;177: 2553–2558. doi: 10.1534/genetics.107.081109 17947403

110. Diao Y, Qi Y, Ma Y, Xia A, Sharakhov I, Chen X, et al. Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes. PLoS One. 2011;6. doi: 10.1371/journal.pone.0016743 21379317

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