Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths

David A. Ray; Jenna R. Grimshaw; Michaela K. Halsey; Jennifer M. Korstian; Austin B. Osmanski; Kevin A.M. Sullivan; Kristen A. Wolf; Harsith Reddy; Nicole Foley; Richard D. Stevens; Binyamin A. Knisbacher; Orr Levy; Brian Counterman; Nathaniel B. Edelman; James Mallet; Sarah Schaack

doi:10.1093/gbe/evz125

Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths

David A. Ray, Jenna R. Grimshaw, Michaela K. Halsey, Jennifer M. Korstian, Austin B. Osmanski, Kevin A.M. Sullivan, Kristen A. Wolf, Harsith Reddy, Nicole Foley, Richard D. Stevens, Binyamin A. Knisbacher, Orr Levy, Brian Counterman, Nathaniel B. Edelman, James Mallet, Sarah Schaack

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16 Scopus citations

Abstract

Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.

Original language	English
Pages (from-to)	2162-2177
Number of pages	16
Journal	Genome Biology and Evolution
Volume	11
Issue number	8
DOIs	https://doi.org/10.1093/gbe/evz125
State	Published - 1 Aug 2019

Bibliographical note

Publisher Copyright:
© 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Funding

The authors wish to thank the College of Arts and Sciences at Texas Tech University for funding related to this work. In addition, we would like to thank the Texas Tech HPCC (http:// www.depts.ttu.edu/hpcc/) for providing computational resources necessary to complete this project. Angela Peace provided assistance with early conceptual analyses. The 20-genome Heliconius project was funded by a SPARC Grant from the Broad Institute of Harvard and MIT as well as startup and studentship funds from Harvard University. Fernando Seixas provided valuable assistance with the PSMC analysis. Support for DAR was provided by the National Science Foundation (DEB1838283).

Funders	Funder number
Broad Institute of Harvard
College of Arts and Sciences at Texas Tech University
SPARC
National Science Foundation	1838273, DEB1838283
Directorate for Biological Sciences	1838283
Massachusetts Institute of Technology
Harvard University

Keywords

butterflies
evolution
transposable elements

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10.1093/gbe/evz125

Cite this

Ray, D. A., Grimshaw, J. R., Halsey, M. K., Korstian, J. M., Osmanski, A. B., Sullivan, K. A. M., Wolf, K. A., Reddy, H., Foley, N., Stevens, R. D., Knisbacher, B. A., Levy, O., Counterman, B., Edelman, N. B., Mallet, J., & Schaack, S. (2019). Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths. Genome Biology and Evolution, 11(8), 2162-2177. https://doi.org/10.1093/gbe/evz125

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title = "Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths",

abstract = "Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.",

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note = "Publisher Copyright: {\textcopyright} 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",

year = "2019",

month = aug,

day = "1",

doi = "10.1093/gbe/evz125",

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Ray, DA, Grimshaw, JR, Halsey, MK, Korstian, JM, Osmanski, AB, Sullivan, KAM, Wolf, KA, Reddy, H, Foley, N, Stevens, RD, Knisbacher, BA, Levy, O, Counterman, B, Edelman, NB, Mallet, J & Schaack, S 2019, 'Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths', Genome Biology and Evolution, vol. 11, no. 8, pp. 2162-2177. https://doi.org/10.1093/gbe/evz125

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AU - Wolf, Kristen A.

AU - Reddy, Harsith

AU - Foley, Nicole

AU - Stevens, Richard D.

AU - Knisbacher, Binyamin A.

AU - Levy, Orr

AU - Counterman, Brian

AU - Edelman, Nathaniel B.

AU - Mallet, James

AU - Schaack, Sarah

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N2 - Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.

AB - Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.

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Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths

Abstract

Bibliographical note

Funding

Keywords

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