Brain microRNAs among social and solitary bees

Karen M. Kapheim; Beryl M. Jones; Eirik Søvik; Eckart Stolle; Robert M. Waterhouse; Guy Bloch; Yehuda Ben-Shahar

doi:10.1098/rsos.200517

Brain microRNAs among social and solitary bees

Karen M. Kapheim, Beryl M. Jones, Eirik Søvik, Eckart Stolle, Robert M. Waterhouse, Guy Bloch, Yehuda Ben-Shahar

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

16 Scopus citations

Abstract

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the brain, 24-72% of which did not have homologues in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.

Original language	English
Article number	200517
Journal	Royal Society Open Science
Volume	7
Issue number	7
DOIs	https://doi.org/10.1098/rsos.200517
State	Published - Jul 1 2020

Bibliographical note

Publisher Copyright:
© 2020 The Authors.

Funding

Data accessibility. Sequences are deposited at NCBI SRA as BioProject PRJNA559906. Other data supporting this article are available in electronic supplementary material, tables S1\u2013S8. Relevant code for this research is stored in GitHub: www. github.com/kapheimlab/bee_microRNA and have been archived within the Zenodo repository: https://zenodo.org/ badge/latestdoi/250347886. Authors\u2019 contribution. K.M.K. conceived of the study and designed the experiments. K.M.K., E.S., G.B. and Y.B.-S. collected the data. K.M.K., B.M.J., E.S. and R.M.W. analysed the data. K.M.K. wrote the initial draft of the manuscript. All authors edited and approved the final article for publication. All authors agree to be held accountable for the work performed therein. Competing interests. The authors declare no competing interests. Funding. Financial support came from the USDA National Institute of Food and Agriculture (2018-67014-27542 to K.M.K.); the Utah Agricultural Experiment Station, Utah State University (Project 1297, journal paper number 9239 to K.M.K.); the U.S.-Israel Binational Science Foundation (BSF 2012807 to G.B. and Y.B.-S.) and the Swiss National Science Foundation (PP00P3_170664 to R.M.W.). Acknowledgements. Sequencing was performed at the University of Illinois Roy J. Carver Biotechnology Center. We thank the University of Utah High Performance Computing Center for computational time and assistance. Illustrations were created by J. Johnson (LifeSciences Studios). G.B. thanks the Clark Way Harrison Visiting Professor in Arts and Sciences that supported his stay in Washington University in St Louis. We thank G. Robinson for helpful feedback on an earlier draft of this manuscript.

Funders	Funder number
United States-Israel Binational Science Foundation	BSF 2012807
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative	2018-67014-27542
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	PP00P3_170664, 170664
U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China	1707221
Utah Agricultural Experiment Station	9239

Keywords

eusociality
gene regulation
lineage-specific
microRNA targets
small non-coding RNA

ASJC Scopus subject areas

General

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10.1098/rsos.200517

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title = "Brain microRNAs among social and solitary bees",

abstract = "Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20-35\%) of detected miRNAs had lineage-specific expression in the brain, 24-72\% of which did not have homologues in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.",

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AU - Ben-Shahar, Yehuda

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Brain microRNAs among social and solitary bees

Abstract

Bibliographical note

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Keywords

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