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Peer-reviewedCC BY 4.0Science Advances

Independent origin of genomic imprinting in placental fish

  • Ying Zhang1
  • Polly Campbell2
  • Alec Kingsley3
  • Yuridia Reynoso2
  • Yuan Kang4
  • Chen-Che Jeff Huang4
  • John H. Werren3
  • David Reznick2
  • Xu Wang1,5,6
6 affiliations
  1. 1Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USA.
  2. 2Department of Evolution, Ecology and Organismal Biology, University of California, Riverside, Riverside, CA 92521, USA.
  3. 3Department of Biology, University of Rochester, Rochester, NY 14627, USA.
  4. 4Department of Anatomy, Physiology & Pharmacology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USA.
  5. 5Center for Advanced Science, Innovation and Commerce, Alabama Agricultural Experiment Station, Auburn, AL 36849, USA.
  6. 6HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, USA.
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Abstract

Genomic imprinting results in biased expression of one parental allele. Such non-Mendelian expression occurs in angiosperms and placental mammals, which share having an active paternal genome during maternal offspring provisioning. It is hypothesized that imprinting modulates conflict between maternal control of resource allocation and paternal control of resource acquisition. If true, then imprinting should evolve in any organism that evolves a placenta. Here, we demonstrate genomic imprinting in a placental poeciliid fish, Poeciliopsis prolifica. Using transcriptomes from reciprocal crosses between two inbred strains, we identified 84 protein-coding genes with robust evidence of imprinting in P. prolifica placenta. These include the teleost ortholog of mammalian imprinted gene, grb10, and a pair of adjacent genes, dpp4 and gcga, with opposing effects on glucose metabolism that are oppositely imprinted in a fashion that potentially resolves parental conflict. Significantly elevated allelic DNA methylation on the promoters of two focal imprinted genes suggests epigenetic mechanisms of imprinting similar to those in mammals. We also discovered the convergent recruitment of a gene network associated with nutrient transport in mammals. To our knowledge, this is the first demonstration of genomic imprinting in a non-mammalian vertebrate and supports the potential role of imprinting in resolving parental conflict.

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Cite

BibTeXRIS
BibTeX
@article{zhang2026independent,
  title = {{Independent origin of genomic imprinting in placental fish}},
  author = {Ying Zhang and Polly Campbell and Alec Kingsley and Yuridia Reynoso and Yuan Kang and Chen-Che Jeff Huang and John H. Werren and David Reznick and Xu Wang},
  journal = {Science Advances},
  year = {2026},
  month = nov,
  doi = {10.1126/sciadv.aeh5487},
  url = {https://www.science.org/doi/abs/10.1126/sciadv.aeh5487},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Independent origin of genomic imprinting in placental fish
AU  - Ying Zhang
AU  - Polly Campbell
AU  - Alec Kingsley
AU  - Yuridia Reynoso
AU  - Yuan Kang
AU  - Chen-Che Jeff Huang
AU  - John H. Werren
AU  - David Reznick
AU  - Xu Wang
PY  - 2026
DA  - 2026/11/04
JO  - Science Advances
DO  - 10.1126/sciadv.aeh5487
UR  - https://www.science.org/doi/abs/10.1126/sciadv.aeh5487
AB  - Genomic imprinting results in biased expression of one parental allele. Such non-Mendelian expression occurs in angiosperms and placental mammals, which share having an active paternal genome during maternal offspring provisioning. It is hypothesized that imprinting modulates conflict between maternal control of resource allocation and paternal control of resource acquisition. If true, then imprinting should evolve in any organism that evolves a placenta. Here, we demonstrate genomic imprinting in a placental poeciliid fish, Poeciliopsis prolifica. Using transcriptomes from reciprocal crosses between two inbred strains, we identified 84 protein-coding genes with robust evidence of imprinting in P. prolifica placenta. These include the teleost ortholog of mammalian imprinted gene, grb10, and a pair of adjacent genes, dpp4 and gcga, with opposing effects on glucose metabolism that are oppositely imprinted in a fashion that potentially resolves parental conflict. Significantly elevated allelic DNA methylation on the promoters of two focal imprinted genes suggests epigenetic mechanisms of imprinting similar to those in mammals. We also discovered the convergent recruitment of a gene network associated with nutrient transport in mammals. To our knowledge, this is the first demonstration of genomic imprinting in a non-mammalian vertebrate and supports the potential role of imprinting in resolving parental conflict.
SN  - 2375-2548
ER  -