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Genome size evolution in the diverse insect order Trichoptera

BACKGROUND: Genome size is implicated in the form, function, and ecological success of a species. Two principally different mechanisms are proposed as major drivers of eukaryotic genome evolution and diversity: polyploidy (i.e., whole-genome duplication) or smaller duplication events and bursts in t...

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Autores principales: Heckenhauer, Jacqueline, Frandsen, Paul B, Sproul, John S, Li, Zheng, Paule, Juraj, Larracuente, Amanda M, Maughan, Peter J, Barker, Michael S, Schneider, Julio V, Stewart, Russell J, Pauls, Steffen U
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8881205/
https://www.ncbi.nlm.nih.gov/pubmed/35217860
http://dx.doi.org/10.1093/gigascience/giac011
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author Heckenhauer, Jacqueline
Frandsen, Paul B
Sproul, John S
Li, Zheng
Paule, Juraj
Larracuente, Amanda M
Maughan, Peter J
Barker, Michael S
Schneider, Julio V
Stewart, Russell J
Pauls, Steffen U
author_facet Heckenhauer, Jacqueline
Frandsen, Paul B
Sproul, John S
Li, Zheng
Paule, Juraj
Larracuente, Amanda M
Maughan, Peter J
Barker, Michael S
Schneider, Julio V
Stewart, Russell J
Pauls, Steffen U
author_sort Heckenhauer, Jacqueline
collection PubMed
description BACKGROUND: Genome size is implicated in the form, function, and ecological success of a species. Two principally different mechanisms are proposed as major drivers of eukaryotic genome evolution and diversity: polyploidy (i.e., whole-genome duplication) or smaller duplication events and bursts in the activity of repetitive elements. Here, we generated de novo genome assemblies of 17 caddisflies covering all major lineages of Trichoptera. Using these and previously sequenced genomes, we use caddisflies as a model for understanding genome size evolution in diverse insect lineages. RESULTS: We detect a ∼14-fold variation in genome size across the order Trichoptera. We find strong evidence that repetitive element expansions, particularly those of transposable elements (TEs), are important drivers of large caddisfly genome sizes. Using an innovative method to examine TEs associated with universal single-copy orthologs (i.e., BUSCO genes), we find that TE expansions have a major impact on protein-coding gene regions, with TE-gene associations showing a linear relationship with increasing genome size. Intriguingly, we find that expanded genomes preferentially evolved in caddisfly clades with a higher ecological diversity (i.e., various feeding modes, diversification in variable, less stable environments). CONCLUSION: Our findings provide a platform to test hypotheses about the potential evolutionary roles of TE activity and TE-gene associations, particularly in groups with high species, ecological, and functional diversities.
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spelling pubmed-88812052022-02-28 Genome size evolution in the diverse insect order Trichoptera Heckenhauer, Jacqueline Frandsen, Paul B Sproul, John S Li, Zheng Paule, Juraj Larracuente, Amanda M Maughan, Peter J Barker, Michael S Schneider, Julio V Stewart, Russell J Pauls, Steffen U Gigascience Research BACKGROUND: Genome size is implicated in the form, function, and ecological success of a species. Two principally different mechanisms are proposed as major drivers of eukaryotic genome evolution and diversity: polyploidy (i.e., whole-genome duplication) or smaller duplication events and bursts in the activity of repetitive elements. Here, we generated de novo genome assemblies of 17 caddisflies covering all major lineages of Trichoptera. Using these and previously sequenced genomes, we use caddisflies as a model for understanding genome size evolution in diverse insect lineages. RESULTS: We detect a ∼14-fold variation in genome size across the order Trichoptera. We find strong evidence that repetitive element expansions, particularly those of transposable elements (TEs), are important drivers of large caddisfly genome sizes. Using an innovative method to examine TEs associated with universal single-copy orthologs (i.e., BUSCO genes), we find that TE expansions have a major impact on protein-coding gene regions, with TE-gene associations showing a linear relationship with increasing genome size. Intriguingly, we find that expanded genomes preferentially evolved in caddisfly clades with a higher ecological diversity (i.e., various feeding modes, diversification in variable, less stable environments). CONCLUSION: Our findings provide a platform to test hypotheses about the potential evolutionary roles of TE activity and TE-gene associations, particularly in groups with high species, ecological, and functional diversities. Oxford University Press 2022-02-25 /pmc/articles/PMC8881205/ /pubmed/35217860 http://dx.doi.org/10.1093/gigascience/giac011 Text en © The Author(s) 2022. Published by Oxford University Press GigaScience. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Heckenhauer, Jacqueline
Frandsen, Paul B
Sproul, John S
Li, Zheng
Paule, Juraj
Larracuente, Amanda M
Maughan, Peter J
Barker, Michael S
Schneider, Julio V
Stewart, Russell J
Pauls, Steffen U
Genome size evolution in the diverse insect order Trichoptera
title Genome size evolution in the diverse insect order Trichoptera
title_full Genome size evolution in the diverse insect order Trichoptera
title_fullStr Genome size evolution in the diverse insect order Trichoptera
title_full_unstemmed Genome size evolution in the diverse insect order Trichoptera
title_short Genome size evolution in the diverse insect order Trichoptera
title_sort genome size evolution in the diverse insect order trichoptera
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8881205/
https://www.ncbi.nlm.nih.gov/pubmed/35217860
http://dx.doi.org/10.1093/gigascience/giac011
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