Disentangling the determinants of transposable elements dynamics in vertebrate genomes using empirical evidences and simulations

Autoři: Yann Bourgeois aff001;  Robert Ruggiero aff002;  Imtiyaz Hariyani aff001;  Stéphane Boissinot aff001;  Robert P. Ruggiero aff002;  Imtiyaz Hariyani aff002;  Stéphane Boissinot aff002
Působiště autorů: School of Biological Sciences, University of Portsmouth, Portsmouth, United Kingdom aff001;  New York University Abu Dhabi, Saadiyat Island Campus, Abu Dhabi, United Arab Emirates aff002;  Department of Biology, Southeast Missouri State University, Cape Girardeau, MO, United States of America aff003
Vyšlo v časopise: Disentangling the determinants of transposable elements dynamics in vertebrate genomes using empirical evidences and simulations. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009082
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009082


The interactions between transposable elements (TEs) and their hosts constitute one of the most profound co-evolutionary processes found in nature. The population dynamics of TEs depends on factors specific to each TE families, such as the rate of transposition and insertional preference, the demographic history of the host and the genomic landscape. How these factors interact has yet to be investigated holistically. Here we are addressing this question in the green anole (Anolis carolinensis) whose genome contains an extraordinary diversity of TEs (including non-LTR retrotransposons, SINEs, LTR-retrotransposons and DNA transposons). We observed a positive correlation between recombination rate and frequency of TEs and densities for LINEs, SINEs and DNA transposons. For these elements, there was a clear impact of demography on TE frequency and abundance, with a loss of polymorphic elements and skewed frequency spectra in recently expanded populations. On the other hand, some LTR-retrotransposons displayed patterns consistent with a very recent phase of intense amplification. To determine how demography, genomic features and intrinsic properties of TEs interact we ran simulations using SLiM3. We determined that i) short TE insertions are not strongly counter-selected, but long ones are, ii) neutral demographic processes, linked selection and preferential insertion may explain positive correlations between average TE frequency and recombination, iii) TE insertions are unlikely to have been massively recruited in recent adaptation. We demonstrate that deterministic and stochastic processes have different effects on categories of TEs and that a combination of empirical analyses and simulations can disentangle these mechanisms.

Klíčová slova:

DNA recombination – Effective population size – Florida – Genomics – Heterozygosity – Population genetics – Transposable elements – DNA transposons


1. Sotero-Caio CG, Platt RN, Suh A, Ray DA. Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol Evol. 2017;9: 161–177. doi: 10.1093/gbe/evw264 28158585

2. 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

3. Song MJ, Schaack S. Evolutionary Conflict between Mobile DNA and Host Genomes. Am Nat. 2018;192: 263–273. doi: 10.1086/698482 30016164

4. Venner S, Feschotte C, Biémont C. Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet. 2009;25: 317–323. doi: 10.1016/j.tig.2009.05.003 19540613

5. Brookfield JFY. The ecology of the genome—Mobile DNA elements and their hosts. Nat Rev Genet. 2005;6: 128–136. doi: 10.1038/nrg1524 15640810

6. Arkhipova IR. Neutral Theory, Transposable Elements, and Eukaryotic Genome Evolution. Mol Biol Evol. 2018;35: 1332–1337. doi: 10.1093/molbev/msy083 29688526

7. Boissinot S, Davis J, Entezam A, Petrov D, Furano A V. Fitness cost of LINE-1 (L1) activity in humans. Proc Natl Acad Sci. 2006;103: 9590–9594. doi: 10.1073/pnas.0603334103 16766655

8. Kawakami T, Mugal CF, Suh A, Nater A, Burri R, Smeds L, et al. Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds. Mol Ecol. 2017;26: 4158–4172. doi: 10.1111/mec.14197 28597534

9. Liu S, Yeh CT, Ji T, Ying K, Wu H, Tang HM, et al. Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet. 2009;5. doi: 10.1371/journal.pgen.1000733 19936291

10. González J, Karasov TL, Messer PW, Petrov DA. Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet. 2010;6: 33–35. doi: 10.1371/journal.pgen.1000905 20386746

11. Lockton S, Ross-Ibarra J, Gaut BS. Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci U S A. 2008;105: 13965–13970. doi: 10.1073/pnas.0804671105 18772373

12. Ruggiero RP, Bourgeois Y, Boissinot S. LINE Insertion Polymorphisms Are Abundant but at Low Frequencies across Populations of Anolis carolinensis. Front Genet. 2017;8: 1–14. doi: 10.3389/fgene.2017.00001 28179914

13. Xue AT, Ruggiero RP, Hickerson MJ, Boissinot S. Differential effect of selection against LINE retrotransposons among vertebrates inferred from whole-genome data and demographic modeling. Genome Biol Evol. 2018;10: 1265–1281. doi: 10.1093/gbe/evy083 29688421

14. Burri R. Interpreting differentiation landscapes in the light of long-term linked selection. Evol Lett. 2017;1: 118–131. doi: 10.1002/evl3.14

15. Barron MG, Fiston-Lavier A-S, Petrov DA, Gonzalez J. Population Genomics of Transposable Elements in Drosophila. Annu Rev Genet. 2014;48: 561–81. doi: 10.1146/annurev-genet-120213-092359 25292358

16. Dolgin ES, Charlesworth B. The effects of recombination rate on the distribution and abundance of transposable elements. Genetics. 2008;178: 2169–2177. doi: 10.1534/genetics.107.082743 18430942

17. Hill WG, Robertson A. Local effects of limited recombination. Genet Res. 1966;8: 269–294. 5980116

18. Charlesworth B, Charlesworth D. Elements of evolutionary genetics. Roberts and Company Publishers. 2010. doi: 10.1525/bio.2011.61.5.12

19. Boissinot S, Entezam A, Furano A V. Selection Against Deleterious LINE-1-Containing Loci in the Human Lineage. Mol Biol. 2001;18: 926–935.

20. Villanueva-Cañas JL, Rech GE, de Cara MAR, González J. Beyond SNPs: how to detect selection on transposable element insertions. Methods Ecol Evol. 2017;8: 728–737. doi: 10.1111/2041-210X.12781

21. Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, et al. Finding the Genomic Basis of Local Adaptation: Pitfalls, Practical Solutions, and Future Directions. Am Nat. 2016;188: 379–397. doi: 10.1086/688018 27622873

22. 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

23. van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, et al. The industrial melanism mutation in British peppered moths is a transposable element. Nature. 2016;534: 102–105. doi: 10.1038/nature17951 27251284

24. González J, Petrov DA. The adaptive role of transposable elements in the Drosophila genome. Gene. 2009;448: 124–133. doi: 10.1016/j.gene.2009.06.008 19555747

25. Bourgeois Y, Boissinot S. On the Population Dynamics of Junk: A Review on the Population Genomics of Transposable Elements. Genes (Basel). 2019;10: 419. doi: 10.3390/genes10060419 31151307

26. Feiner N. Accumulation of transposable elements in Hox gene clusters during adaptive radiation of Anolis lizards. Proceedings Biol Sci. 2016;283. doi: 10.1098/rspb.2016.1555 27733546

27. Glor RE, Losos JB, Larson A. Out of Cuba: Overwater dispersal and speciation among lizards in the Anolis carolinensis subgroup. Mol Ecol. 2005;14: 2419–2432. doi: 10.1111/j.1365-294X.2005.02550.x 15969724

28. Tollis M, Boissinot S. Genetic Variation in the Green Anole Lizard (Anolis carolinensis) Reveals Island Refugia and a Fragmented Florida During the Quaternary. Genetica. 2014;1: 59–72. doi: 10.1038/nbt.3121.ChIP-nexus

29. Manthey JD, Tollis M, Lemmon AR, Moriarty Lemmon E, Boissinot S. Diversification in wild populations of the model organism Anolis carolinensis: A genome-wide phylogeographic investigation. Ecol Evol. 2016;6: 8115–8125. doi: 10.1002/ece3.2547 27891220

30. Bourgeois Y, Ruggiero RP, Manthey JD, Boissinot S. Recent Secondary Contacts, Linked Selection, and Variable Recombination Rates Shape Genomic Diversity in the Model Species Anolis carolinensis. Genome Biol Evol. 2019;11: 2009–2022. doi: 10.1093/gbe/evz110 31134281

31. Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477: 587–91. doi: 10.1038/nature10390 21881562

32. Ray DA, Xing J, Salem AH, Batzer MA. SINEs of a nearly perfect character. Syst Biol. 2006;55: 928–935. doi: 10.1080/10635150600865419 17345674

33. Han KL, Braun EL, Kimball RT, Reddy S, Bowie RCK, Braun MJ, et al. Are transposable element insertions homoplasy free?: An examination using the avian tree of life. Syst Biol. 2011;60: 375–386. doi: 10.1093/sysbio/syq100 21303823

34. Burri R, Nater A, Kawakami T, Mugal CF, Olason PI, Smeds L, et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 2015;25: 1656–1665. doi: 10.1101/gr.196485.115 26355005

35. Cruickshank TE, Hahn MW. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol. 2014;23: 3133–3157. doi: 10.1111/mec.12796 24845075

36. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE. Size matters: Non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol. 2003;20: 880–892. doi: 10.1093/molbev/msg102 12716993

37. Boissinot S, Sookdeo A. The Evolution of Line-1 in Vertebrates. Genome Biol Evol. 2016; evw247. doi: 10.1093/gbe/evw247 28175298

38. Cooper DM, Schimenti KJ, Schimenti JC. Factors affecting ectopic gene conversion in mice. Mamm Genome. 1998;9: 355–360. doi: 10.1007/s003359900769 9545491

39. Nam K, Ellegren H. Recombination drives vertebrate genome contraction. PLoS Genet. 2012;8. doi: 10.1371/journal.pgen.1002680 22570634

40. Haller BC, Messer PW. SLiM 3: Forward Genetic Simulations Beyond the Wright-Fisher Model. Mol Biol Evol. 2019;36: 632–637. doi: 10.1093/molbev/msy228 30517680

41. Gautier M. Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates. Genetics. 2015;201: 1555–1579. doi: 10.1534/genetics.115.181453 26482796

42. Kern AD, Schrider DR. diploS/HIC: An Updated Approach to Classifying Selective Sweeps. G3; Genes|Genomes|Genetics. 2018; g3.200262.2018. doi: 10.1534/g3.118.200262 29626082

43. Librado P, Orlando L. Detecting signatures of positive selection along defined branches of a population tree using LSD. Mol Biol Evol. 2018;35: 1520–1535. doi: 10.1093/molbev/msy053 29617830

44. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123: 585–95. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1203831&tool=pmcentrez&rendertype=abstract 2513255

45. Hazzouri KM, Mohajer A, Dejak SI, Otto SP, Wright SI. Contrasting patterns of transposable-element insertion polymorphism and nucleotide diversity in autotetraploid and allotetraploid Arabidopsis species. Genetics. 2008;179: 581–592. doi: 10.1534/genetics.107.085761 18493073

46. García Guerreiro MP, Chávez-Sandoval BE, Balanyà J, Serra L, Fontdevila A. Distribution of the transposable elements bilbo and gypsy in original and colonizing populations of Drosophila subobscura. BMC Evol Biol. 2008;8: doi: 10.1186/1471-2148-8-234 18702820

47. Petrov DA, Fiston-Lavier A-S, Lipatov M, Lenkov K, Gonzalez J. Population Genomics of Transposable Elements in Drosophila melanogaster. Mol Biol Evol. 2011;28: 1633–1644. doi: 10.1093/molbev/msq337 21172826

48. Kofler R, Betancourt AJ, Schlötterer C. Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet. 2012;8. doi: 10.1371/journal.pgen.1002487 22291611

49. Kapun M, Barrón M, Staubach F, Obbard DJ, Wiberg RAW, Vieira J, et al. Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses. Mol Biol Evol. 2020. doi: 10.1093/molbev/msaa120 32413142

50. Baller JA, Gao J, Voytas DF. Access to DNA establishes a secondary target site bias for the yeast retrotransposon Ty5. Proc Natl Acad Sci U S A. 2011;108: 20351–20356. doi: 10.1073/pnas.1103665108 21788500

51. Yoshida J, Akagi K, Misawa R, Kokubu C, Takeda J, Horie K. Chromatin states shape insertion profiles of the piggyBac, Tol2 and Sleeping Beauty transposons and murine leukemia virus. Sci Rep. 2017;7: 1–18. doi: 10.1038/s41598-016-0028-x 28127051

52. Flasch DA, Macia Á, Sánchez L, Ljungman M, Heras SR, García-Pérez JL, et al. Genome-wide de novo L1 Retrotransposition Connects Endonuclease Activity with Replication. Cell. 2019;177: 837–851.e28. doi: 10.1016/j.cell.2019.02.050 30955886

53. Sultana T, van Essen D, Siol O, Bailly-Bechet M, Philippe C, Zine El Aabidine A, et al. The Landscape of L1 Retrotransposons in the Human Genome Is Shaped by Pre-insertion Sequence Biases and Post-insertion Selection. Mol Cell. 2019;74: 555–570.e7. doi: 10.1016/j.molcel.2019.02.036 30956044

54. Suh A, Smeds L, Ellegren H. Abundant recent activity of retrovirus-like retrotransposons within and among flycatcher species implies a rich source of structural variation in songbird genomes. Mol Ecol. 2018;27: 99–111. doi: 10.1111/mec.14439 29171119

55. Hudson RR. Properties of a neutral allele model with intragenic recombination. Theor Popul Biol. 1983;23: 183–201. doi: 10.1016/0040-5809(83)90013-8 6612631

56. de Boer JG, Yazawa R, Davidson WS, Koop BF. Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids. BMC Genomics. 2007;8: 1–10. doi: 10.1186/1471-2164-8-1 17199895

57. Hellen EHB, Brookfield JFY. Transposable element invasions. Mob Genet Elements. 2013;3: e23920. doi: 10.4161/mge.23920 23734297

58. Vieira C, Lepetit D, Dumont S, Biémont C. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol. 1999;16: 1251–1255. doi: 10.1093/oxfordjournals.molbev.a026215 10486980

59. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, et al. Doubling genome size without polyploidization: Dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 2006;16: 1262–1269. doi: 10.1101/gr.5290206 16963705

60. Manthey JD, Moyle RG, Boissinot S. Multiple and independent phases of transposable element amplification in the genomes of piciformes (woodpeckers and allies). Genome Biol Evol. 2018;10: 1445–1456. doi: 10.1093/gbe/evy105 29850797

61. Blumenstiel JP, Chen X, He M, Bergman CM. An age-of-allele test of neutrality for transposable element insertions. Genetics. 2014;196: 523–538. doi: 10.1534/genetics.113.158147 24336751

62. Bourgeois Y, Boissinot S. Selection at behavioural, developmental and metabolic genes is associated with the northward expansion of a successful tropical colonizer. Mol Ecol. 2019;28: 3523–3543. doi: 10.1111/mec.15162 31233650

63. Sadvakassova G, Dobocan MC, Difalco MR, Congote LF. Regulator of Differentiation 1 (ROD1) Binds to the Amphipathic C-terminal Peptide of Thrombospondin-4 and Is Involved in Its Mitogenic Activity. J Cell Physiol. 2009;1: 672–679. doi: 10.1002/jcp.21817 19441079

64. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, et al. α-neurexins couple Ca 2+ channels to synaptic vesicle exocytosis. Nature. 2003;423: 939–948. doi: 10.1038/nature01755 12827191

65. Vetrini F, McKee S, Rosenfeld JA, Suri M, Lewis AM, Nugent KM, et al. De novo and inherited TCF20 pathogenic variants are associated with intellectual disability, dysmorphic features, hypotonia, and neurological impairments with similarities to Smith-Magenis syndrome. Genome Med. 2019;11: 1–17. doi: 10.1186/s13073-018-0611-9 30609936

66. Schäfgen J, Cremer K, Becker J, Wieland T, Zink AM, Kim S, et al. De novo nonsense and frameshift variants of TCF20 in individuals with intellectual disability and postnatal overgrowth. Eur J Hum Genet. 2016;24: 1739–1745. doi: 10.1038/ejhg.2016.90 27436265

67. González J, Lenkov K, Lipatov M, Macpherson JM, Petrov DA. High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol. 2008;6: 2109–2129. doi: 10.1371/journal.pbio.0060251 18942889

68. Rech GE, Bogaerts-Marquez M, Barron MG, Merenciano M, Villanueva-Canas JL, Horvath V, et al. Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila. PloS Genet. 2018;15: e1007900. doi: 10.1101/380618

69. Schrider DR, Kern AD. Supervised Machine Learning for Population Genetics: A New Paradigm. Trends Genet. 2018;34: 301–312. doi: 10.1016/j.tig.2017.12.005 29331490

70. Gardner EJ, Lam VK, Harris DN, Chuang NT, Scott EC, Pittard WS, et al. The Mobile Element Locator Tool (MELT): Population-scale mobile element discovery and biology. Genome Res. 2017; gr.218032.116. doi: 10.1101/gr.218032.116 28855259

71. 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

72. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

73. R Development Core Team R. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2011. doi: 10.1007/978-3-540-74686-7

74. McVean G, Awadalla P, Fearnhead P. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics. 2002;160: 1231–1241. 11901136

75. Pfeifer B, Wittelsburger U, Ramos-Onsins SE, Lercher MJ. PopGenome: An efficient swiss army knife for population genomic analyses in R. Mol Biol Evol. 2014;31: 1929–1936. doi: 10.1093/molbev/msu136 24739305

76. Ginestet C. ggplot2: Elegant Graphics for Data Analysis. J R Stat Soc Ser A (Statistics Soc. 2011. doi: 10.1111/j.1467-985x.2010.00676_9.x

77. Tollis M, Hutchins ED, Stapley J, Rupp SM, Eckalbar WL, Maayan I, et al. Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards. Genome Biol Evol. 2018;10: 489–506. doi: 10.1093/gbe/evy013 29360978

78. Eyre-Walker A, Keightley PD. The distribution of fitness effects of new mutations. Nat Rev Genet. 2007;8: 610–618. doi: 10.1038/nrg2146 17637733

79. Kryukov G V., Schmidt S, Sunyaev S. Small fitness effect of mutations in highly conserved non-coding regions. Hum Mol Genet. 2005;14: 2221–2229. doi: 10.1093/hmg/ddi226 15994173

80. Myers S, Freeman C, Auton A, Donnelly P, McVean G. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet. 2008;40: 1124–1129. doi: 10.1038/ng.213 19165926

81. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

82. Terhorst J, Kamm JA, Song YS. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat Genet. 2016;49: 303–309. doi: 10.1038/ng.3748 28024154

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle

Zvyšte si kvalifikaci online z pohodlí domova

Třikrát z interní medicíny
nový kurz
Autoři: MUDr. Jana Kubátová

Pokročilá Parkinsonova nemoc − úskalí a možnosti léčby
Autoři: doc. MUDr. Marek Baláž, Ph.D.

Léčba diabetes mellitus 2. typu pomocí GLP- 1 RA

Depresivní porucha a zánětlivé procesy
Autoři: MUDr. Juraj Tkáč

Methotrexát a jeho formy podávání v revmatologii
Autoři: MUDr. Liliana Šedová

Všechny kurzy
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se