Published July 11, 2024
| Published
Journal Article
Open
The genomic and cellular basis of biosynthetic innovation in rove beetles
- Creators
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Kitchen, Sheila A.
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Naragon, Thomas H.
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Brückner, Adrian
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Ladinsky, Mark S.
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Quinodoz, Sofia A.
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Badroos, Jean M.
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Viliunas, Joani W.
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Kishi, Yuriko
- Wagner, Julian M.
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Miller, David R.
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Yousefelahiyeh, Mina
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Antoshechkin, Igor A.
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Eldredge, K. Taro
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Pirro, Stacy
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Guttman, Mitchell1
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Davis, Steven R.
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Aardema, Matthew L.
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Parker, Joseph1
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1.
California Institute of Technology
Abstract
How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.
Copyright and License
© 2024 Elsevier.
Acknowledgement
We thank Charlie Barnes, Mike Caterino, Munetoshi Maruyama, Thomas Schmitt, and Christoph von Beeren for beetle specimens; Taku Shimada and Udo Schmidt for Dalotia photography and specimen images; Nathan Dalleska (Water and Environment lab, Caltech) for HPLC assistance, and Elizabeth Soehalim for help with SPRITE. We acknowledge support from Caltech's Center for Evolutionary Science. A.B. was a Simons Fellow of the Life Sciences Research Foundation. J.M.W. and J.W.V. are NSF GRFP recipients. This work was funded by grants to J.P. from the NIH (1R34NS118470-01), NSF (2047472 CAREER), along with a Shurl and Kay Curci Foundation grant, Rita Allen Foundation Scholarship, Pew Biomedical Scholarship, and an Alfred P. Sloan Foundation fellowship. Additional funding was provided by Iridian Genomes (IRGEN_RG_2021-1345 Genomic Studies of Eukaryotic Taxa), Caltech’s Millard and Muriel Jacobs Genetics and Genomics Laboratory, and an American Museum of Natural History Gerstner Fellowship in Bioinformatics and Computational Biology to M.L.A.
Contributions
Conceptualization, J.P., M.L.A., and S.A.K.; methodology, J.P., M.L.A., and S.A.K.; investigation, S.A.K., T.H.N., A.B., M.S.L., S.A.Q., J.M.B., J.W.V., Y.K., J.M.W., D.R.M., M.Y., I.A.A., K.T.E., S.P., M.G., S.R.D., M.L.A., and J.P.; formal analysis, S.A.K., T.H.N., A.B., J.M.B., and J.W.V.; data curation, S.A.K.; writing – original draft, J.P. and S.A.K.; writing – review & editing, J.P. and S.A.K.; supervision, J.P.; project administration, J.P.; funding acquisition, J.P.
Data Availability
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Sequence reads related to this manuscript have been deposited in the NCBI Sequence Read Archive (SRA) database under the accession numbers listed in the key resources table. New genome assemblies from this study have been deposited in the NCBI GenBank database, with accession numbers listed in the key resources table. Genome assemblies from other studies were downloaded from the NCBI Reference Sequence (RefSeq) database (accessions listed in key resources table). All other data were uploaded to CaltechData (see key resources table for listed DOIs) and are available as of the date of publication.
- Data S2. Analysis of variation in SMART-Seq and bulk RNAseq transcriptome data from aleocharine rove beetle tergal gland cell types, related to Figures 4, 6 and 7
- Data S3. Supplemental phylogenetic and gene family trees
- Data S4. Comparative transcriptomics of Dalotia and Aleochara tergal gland cell types, related to Figure 4
- Data S5. Synteny of CYP4G-encoding enzymes in Aleocharinae, and RELAX analysis of tergal gland expression programs, related to Figures 4, 6 and 7
Code Availability
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Code for the genome assembly, repeat and gene prediction, phylogenomic and phylogenetic tree construction, selection tests, inactivating mutation identification and other analyses has been deposited on GitHub (https://github.com/Parker-Lab-Caltech/Genomic_and_Cellular_Biosynthetic_Innovation_in_Rove_Beetles) and is publicly available as of the date of publication.
Conflict of Interest
The authors declare no competing interests.
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Additional details
- California Institute of Technology
- Caltech Center for Evolutionary Science
- Life Sciences Research Foundation
- National Science Foundation
- NSF Graduate Research Fellowship
- National Institutes of Health
- 1R34NS118470-01
- National Science Foundation
- IOS-2047472
- Shurl and Kay Curci Foundation
- Rita Allen Foundation
- Pew Charitable Trusts
- Alfred P. Sloan Foundation
- Iridian Genomes
- IRGEN_RG_2021-1345
- California Institute of Technology
- Millard and Muriel Jacobs Genetics and Genomics Laboratory
- American Museum of Natural History
- Caltech groups
- Division of Biology and Biological Engineering, Tianqiao and Chrissy Chen Institute for Neuroscience, Caltech Center for Evolutionary Science, Millard and Muriel Jacobs Genetics and Genomics Laboratory