The mobilome of Drosophila incompta, a flower-breeding species: comparison of transposable element landscapes among generalist and specialist flies
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.
KeywordsTransposable Elements Niche Amplitude Horizontal Transfer transposons Genome
Terminal inverted repeats
Long terminal repeats
Target site duplication
Open reading frame
Kimura two parameters
We are grateful to Dr. Lizandra Robe and two anonymous reviewers for suggestions.
Author contribution statement
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.
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).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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
- 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
- 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. 17–40Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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, HeidelbergGoogle Scholar
- Hartl DL (2001) Discovery of the transposable element mariner. Genetics 157:471–475Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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/]
- Markow TA (2015) The secret lives of Drosophila flies. eLife 4. https://doi.org/10.7554/eLife.06793
- Napp M, Brncic D (1978) Eletrophoretic variability in two closely related Brazilian species of the flavopilosa species group of Drosophila. Braz J Genet 1:1–10Google Scholar
- 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 CrossRefGoogle Scholar
- 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
- Rio DC, Ares M, Hannon GJ, Nilsen TW (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc 2010:pdb–prot5439Google Scholar
- 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 83:122–126Google Scholar
- Smit AFA, Hubley R, Green P (2013-2016) RepeatMasker Open-4.0, http://www.repeatmasker.org. Accessed 18 December 2018
- 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
- Wheeler M, Takada H, Brncic D (1962) The flavopilosa species group of Drosophila. The University of Texas Publication pp 395–413Google Scholar