Abstract
The Drosophila genus is one of the main model organisms in evolutionary studies, including those investigating the role of transposable elements (TE) in genomic evolution both at the nucleotide and chromosome levels. D. incompta is a species with restricted ecology, using Cestrum (Solanaceae) flowers as unique sources for oviposition, feeding and development. In the present study, we deeply characterise the D. incompta mobilome and generate a curated dataset. A total of 277 elements were identified, corresponding to approximately 14% of the genome, and 164 of these elements are new, of which 32.62% are putatively autonomous and 8.9% are transcriptionally active in adult flies. The restricted ecology does not seem to influence the dynamics of TE in this fly, since the proportion and diversity of TEs in its genome are similar to that of other Drosophila species. This result is reinforced by the absence of a clear pattern when comparing the TE landscape between generalist and specialist flies. Using 32 available Drosophila genomes—24 ecologically generalist species and 8 specialist species—no difference was found between their TE landscape patterns. However, differences were found between species of the Sophophora and Drosophila subgenus, indicating there are lineage-specific factors shaping TE landscapes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- TE:
-
Transposable elements
- bp:
-
Base pairs
- PA:
-
Putative autonomous
- PNA:
-
Putative non-autonomous
- DG:
-
Degenerated
- TIRs:
-
Terminal inverted repeats
- LTRs:
-
Long terminal repeats
- TSD:
-
Target site duplication
- ORF:
-
Open reading frame
- K2P:
-
Kimura two parameters
References
Afgan E, Baker D, van den Beek M, Blankenberg D, Bouvier D, Čech M, Chilton J, Clements D, Coraor N, Eberhard C, Grüning B, Guerler A, Hillman-Jackson J, von Kuster G, Rasche E, Soranzo N, Turaga N, Taylor J, Nekrutenko A, Goecks J (2016) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res 44:W3–W10. https://doi.org/10.1093/nar/gkw343
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Bächli G (2018) TaxoDros: the database on taxonomy of Drosophilidae. https://www.taxodros.uzh.ch/ Accessed 26 November 2018
Barrón MG, Fiston-Lavier AS, Petrov DA, González J (2014) Population genomics of transposable elements in Drosophila. Annu Rev Genet 48:561–581. https://doi.org/10.1146/annurev-genet-120213-092359
Bankevich A, Nurk S, Antipov D, Gurevich AA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Brouat C, Sennedot F, Audiot P, Leblois R, Rasplus JY (2003) Fine-scale genetic structure of two carabid species with contrasted levels of habitat specialization. Mol Ecol 12:1731–1745. https://doi.org/10.1046/j.1365-294X.2003.01861.x
Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509:7–15. https://doi.org/10.1016/j.gene.2012.07.042
Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2015) GenBank. Nucleic Acids Res 44:D67–D72. https://doi.org/10.1093/nar/gkv1276
Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman T, Kellis M, Gelbart W et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218. https://doi.org/10.1038/nature06341
da Silva AF, Dezordi FZ, Loreto ELS, Wallau GL (2018) Drosophila parasitoid wasps bears a distinct DNA transposon profile. Mob DNA 9:23. https://doi.org/10.1186/s13100-018-0127-2
de Ré FC, Wallau GL, Robe LJ, Loreto ELS (2014) Characterization of the complete mitochondrial genome of flower-breeding Drosophila incompta (Diptera, Drosophilidae). Genetica 142:525–535. https://doi.org/10.1007/s10709-014-9799-9
Dotto BR, Carvalho EL, Freitas A, et al (2018) HTT-DB: new features and updates. Database 2018:bax102. https://doi.org/10.1093/database/bax102, HTT-DB: new features and updates
Feschotte C, Wessler SR (2001) Treasures in the attic: rolling circle transposons discovered in eukaryotic genomes. PNAS 98:8923–8924. https://doi.org/10.1073/pnas.171326198
Flutre T, Permal E, Quesneville H (2012) Transposable element annotation in completely sequenced eukaryote genomes. In: Plant Ttranspos able Eelements (eds Grandbastien M-A & Casacuberta J). Topics in current genetics, vol. 24, Springer, Heidelberg, pp. 17–40
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. https://doi.org/10.1093/bioinformatics/bts565
Goubert C, Modolo L, Vieira C, ValienteMoro C, Mavingui P, Boulesteix M (2015) 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). Gen Biol and Evol 7:1192–1205. https://doi.org/10.1093/gbe/evv050
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652 https://www.nature.com/articles/nbt.1883
Guillín ER, Rafael V (2018) Two new species in the Drosophila flavopilosa and Drosophila morelia species groups (Diptera: Drosophilidae) in the eastern Andes of Ecuador. Rev Peru Biol 25:69–74. https://doi.org/10.15381/rpb.v25i2.14684
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Habel JC, Augenstein B, Meyer M, Nève G, Rödder D, Assmann T (2009) Population genetics and ecological niche modelling reveal high fragmentation and potential future extinction of the endangered relict butterfly Lycaena helle. In: Habel JC, Assmann T (eds) Relict species. Springer, Berlin, Heidelberg
Hartl DL (2001) Discovery of the transposable element mariner. Genetics 157:471–475
Heringer P, Dias GB, GCS K (2017) A horizontally transferred autonomous Helitron became a full polydnavirus segment in Cotesia vestalis. G3 7:3925–3935. https://doi.org/10.1534/g3.117.300280
Hoen DR, Hickey G, Bourque G, Casacuberta J, Cordaux R, Feschotte C, Fiston-Lavier AS, Hua-van A, Hubley R, Kapusta A, Lerat E, Maumus F, Pollock DD, Quesneville H, Smit A, Wheeler TJ, Bureau TE, Blanchette M (2015) A call for benchmarking transposable element annotation methods. Mob DNA 6:13. https://doi.org/10.1186/s13100-015-0044-6
Hua-Van A, Le Rouzic A, Boutin TS, Filée J, Capy P (2011) The struggle for life of the genome’s selfish architects. Biol Direct 6:19. https://doi.org/10.1186/1745-6150-6-19
Huang X, Madan A (1998) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467. https://doi.org/10.1159/000084979
Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SE (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3:research0084.1. https://doi.org/10.1186/gb-2002-3-12-research0084
Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. PNAS 98:8714–8719. https://doi.org/10.1073/pnas.151269298
Kapitonov VV, Jurka J (2005) Self-synthesizing DNA transposons in eukaryotes. PNAS 103:4540–4545. https://doi.org/10.1073/pnas.0600833103
Kapitonov VV, Jurka J (2007) Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet 23:521–529. https://doi.org/10.1016/j.tig.2007.08.004
Kelley ST, Farrell BD, Mitton JB (2000) Effects of specialization on genetic differentiation in sister species of bark beetles. Heredity 84:218–227. https://doi.org/10.1046/j.1365-2540.2000.00662.x
Kelley JL, Peyton JT, Fiston-Lavier AS, Teets NM, Yee MC, Johnston JS, Bustamante CD, Lee RE, Denlinger DL (2014) Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nat Commum 5:4611. https://doi.org/10.1038/ncomms5611
Krueger F (2015) Trim galore. A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files. [http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/]
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Le Rouzic A, Capy P (2005) The first steps of transposable elements invasion: parasitic strategy vs. genetic drift. Genetics 169:1033–1043. https://doi.org/10.1534/genetics.104.031211
Lerat E, Burlet N, Biémont C, Vieira C (2011) Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 473:100–109. https://doi.org/10.1016/j.gene.2010.11.009
Loreto ELS, Carareto CMA, Capy P (2008) Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 100:545–554. https://doi.org/10.1038/sj.hdy.6801094
Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404
Markow TA (2015) The secret lives of Drosophila flies. eLife 4. https://doi.org/10.7554/eLife.06793
McCullers TJ, Steiniger M (2017) Transposable elements in Drosophila. Mob Genet Elem 7:1–18. https://doi.org/10.1080/2159256X.2017.1318201
Napp M, Brncic D (1978) Eletrophoretic variability in two closely related Brazilian species of the flavopilosa species group of Drosophila. Braz J Genet 1:1–10
Nossil P (2002) Transition rates between specialization and generalization in phytophagous insects. Evolution 56:1701–1706. https://doi.org/10.1111/j.0014-3820.2002.tb01482.x
Novak P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next generation sequence reads. Bioinformatics. 29:792–793. https://doi.org/10.1093/bioinformatics/btt054
O’Grady PM, DeSalle R (2018) Phylogeny of the genus Drosophila. Genetics 209:1–25. https://doi.org/10.1534/genetics.117.300583
Okonechnikov K, Golosova O, Fursov M the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167. https://doi.org/10.1093/bioinformatics/bts091
Ortiz MF, Wallau GL, Graichen DÂS, Loreto ELS (2014) An evaluation of the ecological relationship between Drosophila species and their parasitoid wasps as an opportunity for horizontal transposon transfer. Mol Gen Genomics 290:67–78. https://doi.org/10.1007/s00438-014-0900-y
Packer L, Zayed A, Grixti JC et al (2005) Conservation genetics of potentially endangered mutualism: reduced levels of genetic variation in specialist vs. generalist bees. Conserv Biol 19:195–202. https://doi.org/10.1111/j.1523-1739.2005.00601.x
Peccoud J, Loiseau V, Cordaux R, Gilbert C (2017) Massive horizontal transfer of transposable elements in insects. PNAS 114:4721–4726. https://doi.org/10.1073/pnas.1621178114
Petersen M, Armisén D, Gibbs RA, Hering L, Khila A, Mayer G, Richards S, Niehuis O, Misof B (2019) Diversity and evolution of the transposable element repertoire in arthropods with particular reference to insects. BMC Evol Biol 19:11. https://doi.org/10.1186/s12862-018-1324-9
Picot S, Wallau GL, Loreto EL, Heredia FO, Hua-Van A, Capy P (2008) The mariner transposable element in natural populations of Drosophila simulans. Heredity (Edinb) 101(1):53–59. https://doi.org/10.1038/hdy.2008.27
Piégu B, Bire S, Arensburger P, Bigot Y (2015) A survey of transposable element classification systems–a call for a fundamental update to meet the challenge of their diversity and complexity. Mol Phylogenet Evol 86:90–109. https://doi.org/10.1016/j.ympev.2015.03.009
Platt RN, Blanco-Berdugo L, Ray DA (2016) Accurate transposable element annotation is vital when analyzing new genome assemblies. Genome Biol Evol 8:403–410. https://doi.org/10.1093/gbe/evw009
Rio DC, Ares M, Hannon GJ, Nilsen TW (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc 2010:pdb–prot5439
Rius N, Guillén Y, Delprat A, Kapusta A, Feschotte C, Ruiz A (2016) Exploration of the Drosophila buzzatii transposable element content suggests underestimation of repeats in Drosophila genomes. BMC Genomics 17:344. https://doi.org/10.1186/s12864-016-2648-8
Robe LJ, Loreto ELS, Valente VLS (2010) Radiation of the “Drosophila” subgenus (Drosophilidae, Diptera) in the Neotropics. J Zool Syst Evol Res 48:310–321. https://doi.org/10.1111/j.1439-0469.2009.00563.x
Robe LJ, De Ré FC, Ludwig A, Loreto ELS (2013) The Drosophila flavopilosa species group (Diptera, Drosophilidae): an array of exciting questions. Fly 7:59–69. https://doi.org/10.4161/fly.23923
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302
SanMiguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
Santos R, Vilela C (2005) Breeding sites of Neotropical Drosophilidae (Diptera): IV. Living and fallen flowers of Sessea brasiliensis and Cestrum spp. (Solanaceae). Revista Brasileira de Entomología 49:544–551
Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–547. https://doi.org/10.1016/j.tree.2010.06.001
Sepel LMN, Golombiesky RM, Napp M, Loresto ELS (2000) Seasonal fluctuation os Drosophila cestri and Drosophila incompta, two species of flavopilosa group. Drosophila Information Service 83:122–126
Sessegolo C, Burlet N, Haudry A (2016) Strong phylogenetic inertia on genome size and transposable element content among 26 species of flies. Biol Lett 12:20160407. https://doi.org/10.1098/rsbl.2016.0407
Siefert JL (2009) Defining the mobilome. Methods Mol Biol 532:13–27. https://doi.org/10.1007/978-1-60327-853-9_2
Smit AFA, Hubley R, Green P (2013-2016) RepeatMasker Open-4.0, http://www.repeatmasker.org. Accessed 18 December 2018
Venner S, Miele V, Terzian C, Biémont C, Daubin V, Feschotte C, Pontier D (2017) Ecological networks to unravel the routes to horizontal transposon transfers. PLoS Biol 15:e2001536. https://doi.org/10.1371/journal.pbio.2001536
Vieira C, Lepetit D, Dumont S, Biémont C (1999) Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol 16:1251–1255
Vieira C, Nardon C, Arpin C, Lepetit D, Biemont C (2002) Evolution of genome size in Drosophila. Is the invader’s genome being invaded by transposable elements? Mol Biol Evol 19:1154–1161
Wallau GL, Capy P, Loreto ELS, Le Rouzic A, Hua-Van A (2016a) VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the mariner family within Drosophila. Mol Biol Evol 33:1094–1109. https://doi.org/10.1093/molbev/msv3
Wallau GL, da Rosa MT, De Ré FC, Loreto ELS (2016b) Wolbachia from Drosophila incompta: just a hitchhiker shared by Drosophila in the New and Old World? Insect Mol Biol 25(4):487–499. https://doi.org/10.1111/imb.1223741
Wallau GL, Vieira C, Loreto ELS (2018) Genetic exchange in eukaryotes through horizontal transfer: connected by the mobilome. Mob DNA 9(6). https://doi.org/10.1186/s13100-018-0112-9
Weizhong L, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659
Wheeler M, Takada H, Brncic D (1962) The flavopilosa species group of Drosophila. The University of Texas Publication pp 395–413
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982. https://doi.org/10.1038/nrg2165
Zayed A, Packer L, Grixti JC, Ruz L, Owen RE, Toro H (2005) Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation. Conserv Genet 6:1017–1026. https://doi.org/10.1007/s10592-005-9094-5
Acknowledgements
We are grateful to Dr. Lizandra Robe and two anonymous reviewers for suggestions.
Funding
This study was supported by research grants and fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Pronex-Fapergs (16/2551—0000 499-4).
Author information
Authors and Affiliations
Contributions
PMF and EL conceived and designed research. PMF, RMD and GLW conducted experiments and analysed data. PMF, GLW and EL wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor:Rachel O'Neill
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Material 1:
A comparison of TE landscapes between specialist and generalist Drosophila. A table (Supplementary Table A) showing all the species used in the phylogenetic and landscape analyses with niche discrimination and group identification. (DOC 54 kb)
Supplementary Table S1:
Spreadsheet showing all the D. incompta annotated TEs. Each sheet corresponds to one superfamily. (XLSX 466 kb)
Supplementary Table S2:
Spreadsheet showing all the genes used in the phylogenetic and HTT (VHICA) analyses along with their accession codes and sequences. (XLSX 71 kb)
Supplementary Table S3:
Statistical data of both genome and transcriptome draft assemblies. (XLSX 5 kb)
Supplementary Table S4:
Spreadsheet containing the results of the homology search (BLASTn) of the all annotated D. incompta TEs against the D. incompta transcriptome draft. In this analysis the following threshold values were used: a) percentage of identity of query (annotated TEs) and subject (transcriptome draft scaffolds) = 84%; b) minimum alignment length = 100 bp; c) maximum number of base mismatches per alignment = 10; and d) maximum number of gaps per alignment = 5. (XLSX 12 kb)
Rights and permissions
About this article
Cite this article
Fonseca, P.M., Moura, R.D., Wallau, G.L. et al. The mobilome of Drosophila incompta, a flower-breeding species: comparison of transposable element landscapes among generalist and specialist flies. Chromosome Res 27, 203–219 (2019). https://doi.org/10.1007/s10577-019-09609-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-019-09609-x