Transposable element islands facilitate adaptation to novel environments in an invasive species

Lukas Schrader; Jay W. Kim; Daniel Ence; Aleksey Zimin; Antonia Klein; Katharina Wyschetzki; Tobias Weichselgartner; Carsten Kemena; Johannes Stökl; Eva Schultner; Yannick Wurm; Christopher D. Smith; Mark Yandell; Jürgen Heinze; Juergen Gadau; Jan Oettler

doi:10.1038/ncomms6495

Transposable element islands facilitate adaptation to novel environments in an invasive species

Lukas Schrader, Jay W. Kim, Daniel Ence, Aleksey Zimin, Antonia Klein, Katharina Wyschetzki, Tobias Weichselgartner, Carsten Kemena, Johannes Stökl, Eva Schultner, Yannick Wurm, Christopher D. Smith, Mark Yandell, Jürgen Heinze, Juergen Gadau, Jan Oettler

Life Sciences, School of (SOLS)

Research output: Contribution to journal › Article › peer-review

129 Scopus citations

Abstract

Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.

Original language	English (US)
Article number	5495
Journal	Nature communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms6495
State	Published - Dec 2014

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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Schrader, L., Kim, J. W., Ence, D., Zimin, A., Klein, A., Wyschetzki, K., Weichselgartner, T., Kemena, C., Stökl, J., Schultner, E., Wurm, Y., Smith, C. D., Yandell, M., Heinze, J., Gadau, J., & Oettler, J. (2014). Transposable element islands facilitate adaptation to novel environments in an invasive species. Nature communications, 5, Article 5495. https://doi.org/10.1038/ncomms6495

@article{9e9c99d93f4e4954bafa2c4ca772bcdf,

title = "Transposable element islands facilitate adaptation to novel environments in an invasive species",

abstract = "Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.",

author = "Lukas Schrader and Kim, {Jay W.} and Daniel Ence and Aleksey Zimin and Antonia Klein and Katharina Wyschetzki and Tobias Weichselgartner and Carsten Kemena and Johannes St{\"o}kl and Eva Schultner and Yannick Wurm and Smith, {Christopher D.} and Mark Yandell and J{\"u}rgen Heinze and Juergen Gadau and Jan Oettler",

note = "Funding Information: We would like to thank John Wang for helpful discussions during the initial phase of the project and Andr{\'e}s Moya for encouraging comments at an earlier stage of writing. We are most grateful to Masaki Suefuji and Jacques H.C. Delabie for collecting the colonies. We thank Christine Elsik, Deepak Unni and Chris Childers, who provide great support in hosting Cobs1.4 on hymenopteragenome.org. We thank Axel Strittmatter (MWG) and Thomas Stempfl (KFB) for advising on sequencing and Nicole Lehmann for advice on RNA amplification. We thank Helena Lowack for PCR validation of small-scale structural variants, Erich Bornberg-Bauer who assisted with CpG o/e calculation, Anurag Priyam for help with BLAST analyses and Robert Waterhouse for comparing the gene sets with OrthoDB. Y.W. is supported by BBSRC (BB/K004204/1) and NERC (NE/ L00626X/1), A.Z. by NIH (R01 HG002945) and C.K. by DFG (BO2544/4-1). This study was funded by a DFG grant He1623/31 to J.O., J.G. and J.H. Publisher Copyright: {\textcopyright} 2014 Macmillan Publishers Limited. All rights reserved.",

year = "2014",

month = dec,

doi = "10.1038/ncomms6495",

language = "English (US)",

volume = "5",

journal = "Nature communications",

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T1 - Transposable element islands facilitate adaptation to novel environments in an invasive species

AU - Schrader, Lukas

AU - Kim, Jay W.

AU - Ence, Daniel

AU - Zimin, Aleksey

AU - Klein, Antonia

AU - Wyschetzki, Katharina

AU - Weichselgartner, Tobias

AU - Kemena, Carsten

AU - Stökl, Johannes

AU - Schultner, Eva

AU - Wurm, Yannick

AU - Smith, Christopher D.

AU - Yandell, Mark

AU - Heinze, Jürgen

AU - Gadau, Juergen

AU - Oettler, Jan

N1 - Funding Information: We would like to thank John Wang for helpful discussions during the initial phase of the project and Andrés Moya for encouraging comments at an earlier stage of writing. We are most grateful to Masaki Suefuji and Jacques H.C. Delabie for collecting the colonies. We thank Christine Elsik, Deepak Unni and Chris Childers, who provide great support in hosting Cobs1.4 on hymenopteragenome.org. We thank Axel Strittmatter (MWG) and Thomas Stempfl (KFB) for advising on sequencing and Nicole Lehmann for advice on RNA amplification. We thank Helena Lowack for PCR validation of small-scale structural variants, Erich Bornberg-Bauer who assisted with CpG o/e calculation, Anurag Priyam for help with BLAST analyses and Robert Waterhouse for comparing the gene sets with OrthoDB. Y.W. is supported by BBSRC (BB/K004204/1) and NERC (NE/ L00626X/1), A.Z. by NIH (R01 HG002945) and C.K. by DFG (BO2544/4-1). This study was funded by a DFG grant He1623/31 to J.O., J.G. and J.H. Publisher Copyright: © 2014 Macmillan Publishers Limited. All rights reserved.

PY - 2014/12

Y1 - 2014/12

N2 - Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.

AB - Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.

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JO - Nature communications

JF - Nature communications

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Transposable element islands facilitate adaptation to novel environments in an invasive species

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