Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes
Abstract Background East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known a...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-01-01
|
| Series: | Genome Biology |
| Online Access: | https://doi.org/10.1186/s13059-025-03475-z |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832585710359543808 |
|---|---|
| author | Miguel Vasconcelos Almeida Moritz Blumer Chengwei Ulrika Yuan Pío Sierra Jonathan L. Price Fu Xiang Quah Aleksandr Friman Alexandra Dallaire Grégoire Vernaz Audrey L. K. Putman Alan M. Smith Domino A. Joyce Falk Butter Astrid D. Haase Richard Durbin M. Emília Santos Eric A. Miska |
| author_facet | Miguel Vasconcelos Almeida Moritz Blumer Chengwei Ulrika Yuan Pío Sierra Jonathan L. Price Fu Xiang Quah Aleksandr Friman Alexandra Dallaire Grégoire Vernaz Audrey L. K. Putman Alan M. Smith Domino A. Joyce Falk Butter Astrid D. Haase Richard Durbin M. Emília Santos Eric A. Miska |
| author_sort | Miguel Vasconcelos Almeida |
| collection | DOAJ |
| description | Abstract Background East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcriptional activity and epigenetic silencing. We set out to bridge this gap and to understand the interactions between TEs and their cichlid hosts. Results Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci. Conclusions Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity. |
| format | Article |
| id | doaj-art-619c228c37c745e89f58b86a6e969fba |
| institution | Kabale University |
| issn | 1474-760X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj-art-619c228c37c745e89f58b86a6e969fba2025-01-26T12:36:09ZengBMCGenome Biology1474-760X2025-01-0126113710.1186/s13059-025-03475-zDynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishesMiguel Vasconcelos Almeida0Moritz Blumer1Chengwei Ulrika Yuan2Pío Sierra3Jonathan L. Price4Fu Xiang Quah5Aleksandr Friman6Alexandra Dallaire7Grégoire Vernaz8Audrey L. K. Putman9Alan M. Smith10Domino A. Joyce11Falk Butter12Astrid D. Haase13Richard Durbin14M. Emília Santos15Eric A. Miska16Department of Biochemistry, University of CambridgeDepartment of Genetics, University of CambridgeDepartment of Biochemistry, University of CambridgeDepartment of Genetics, University of CambridgeDepartment of Biochemistry, University of CambridgeDepartment of Biochemistry, University of CambridgeNational Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthDepartment of Biochemistry, University of CambridgeWellcome/CRUK Gurdon Institute, University of CambridgeDepartment of Biochemistry, University of CambridgeSchool of Natural Sciences, University of HullSchool of Natural Sciences, University of HullInstitute of Molecular Biology (IMB)National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthDepartment of Genetics, University of CambridgeDepartment of Zoology, University of CambridgeDepartment of Biochemistry, University of CambridgeAbstract Background East African cichlid fishes have diversified in an explosive fashion, but the (epi)genetic basis of the phenotypic diversity of these fishes remains largely unknown. Although transposable elements (TEs) have been associated with phenotypic variation in cichlids, little is known about their transcriptional activity and epigenetic silencing. We set out to bridge this gap and to understand the interactions between TEs and their cichlid hosts. Results Here, we describe dynamic patterns of TE expression in African cichlid gonads and during early development. Orthology inference revealed strong conservation of TE silencing factors in cichlids, and an expansion of piwil1 genes in Lake Malawi cichlids, likely driven by PiggyBac TEs. The expanded piwil1 copies have signatures of positive selection and retain amino acid residues essential for catalytic activity. Furthermore, the gonads of African cichlids express a Piwi-interacting RNA (piRNA) pathway that targets TEs. We define the genomic sites of piRNA production in African cichlids and find divergence in closely related species, in line with fast evolution of piRNA-producing loci. Conclusions Our findings suggest dynamic co-evolution of TEs and host silencing pathways in the African cichlid radiations. We propose that this co-evolution has contributed to cichlid genomic diversity.https://doi.org/10.1186/s13059-025-03475-z |
| spellingShingle | Miguel Vasconcelos Almeida Moritz Blumer Chengwei Ulrika Yuan Pío Sierra Jonathan L. Price Fu Xiang Quah Aleksandr Friman Alexandra Dallaire Grégoire Vernaz Audrey L. K. Putman Alan M. Smith Domino A. Joyce Falk Butter Astrid D. Haase Richard Durbin M. Emília Santos Eric A. Miska Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes Genome Biology |
| title | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
| title_full | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
| title_fullStr | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
| title_full_unstemmed | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
| title_short | Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes |
| title_sort | dynamic co evolution of transposable elements and the pirna pathway in african cichlid fishes |
| url | https://doi.org/10.1186/s13059-025-03475-z |
| work_keys_str_mv | AT miguelvasconcelosalmeida dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT moritzblumer dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT chengweiulrikayuan dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT piosierra dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT jonathanlprice dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT fuxiangquah dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT aleksandrfriman dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT alexandradallaire dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT gregoirevernaz dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT audreylkputman dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT alanmsmith dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT dominoajoyce dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT falkbutter dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT astriddhaase dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT richarddurbin dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT memiliasantos dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes AT ericamiska dynamiccoevolutionoftransposableelementsandthepirnapathwayinafricancichlidfishes |