Genome size evolution in the diverse insect order Trichoptera

Author:

Heckenhauer Jacqueline12ORCID,Frandsen Paul B134ORCID,Sproul John S56ORCID,Li Zheng7ORCID,Paule Juraj8ORCID,Larracuente Amanda M5ORCID,Maughan Peter J3ORCID,Barker Michael S7ORCID,Schneider Julio V2ORCID,Stewart Russell J9ORCID,Pauls Steffen U1210ORCID

Affiliation:

1. LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Frankfurt 60325, Germany

2. Department of Terrestrial Zoology, Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt 60325, Germany

3. Department of Plant & Wildlife Sciences, Brigham Young University, Provo, UT 84602, USA

4. Data Science Lab, Smithsonian Institution, Washington, DC 20560, USA

5. Department of Biology, University of Rochester, Rochester, NY 14620, USA

6. Department of Biology, University of Nebraska Omaha, Omaha, NE 68182, USA

7. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA

8. Department of Botany and Molecular Evolution, Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt 60325, Germany

9. Department of Biomedical Engineering, University of Utah, Salt Lake City, UT 84112, USA

10. Institute for Insect Biotechnology, Justus-Liebig-University, Gießen 35390, Germany

Abstract

Abstract 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.

Funder

National Science Foundation

National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Computer Science Applications,Health Informatics

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