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Nature. 2018 Jan 18;553(7688):337-341. doi: 10.1038/nature25188. Epub 2018 Jan 10.

Paternal chromosome loss and metabolic crisis contribute to hybrid inviability in Xenopus.

Author information

1
Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.
2
Radboud University, Department of Molecular Developmental Biology, Faculty of Science, Radboud Institute for Molecular Life Sciences, 6500 HB Nijmegen, The Netherlands.
3
Departments of Chemistry and Nutritional Sciences and Toxicology, University of California, Berkeley, California 94720, USA.
4
Department of Molecular Bioscience, Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas 78712, USA.
5
Department of Biomedical Engineering, Ulsan National Institute of Science and Technology, Ulsan 44919, South Korea.

Abstract

Hybridization of eggs and sperm from closely related species can give rise to genetic diversity, or can lead to embryo inviability owing to incompatibility. Although central to evolution, the cellular and molecular mechanisms underlying post-zygotic barriers that drive reproductive isolation and speciation remain largely unknown. Species of the African clawed frog Xenopus provide an ideal system to study hybridization and genome evolution. Xenopus laevis is an allotetraploid with 36 chromosomes that arose through interspecific hybridization of diploid progenitors, whereas Xenopus tropicalis is a diploid with 20 chromosomes that diverged from a common ancestor approximately 48 million years ago. Differences in genome size between the two species are accompanied by organism size differences, and size scaling of the egg and subcellular structures such as nuclei and spindles formed in egg extracts. Nevertheless, early development transcriptional programs, gene expression patterns, and protein sequences are generally conserved. Whereas the hybrid produced when X. laevis eggs are fertilized by X. tropicalis sperm is viable, the reverse hybrid dies before gastrulation. Here we apply cell biological tools and high-throughput methods to study the mechanisms underlying hybrid inviability. We reveal that two specific X. laevis chromosomes are incompatible with the X. tropicalis cytoplasm and are mis-segregated during mitosis, leading to unbalanced gene expression at the maternal to zygotic transition, followed by cell-autonomous catastrophic embryo death. These results reveal a cellular mechanism underlying hybrid incompatibility that is driven by genome evolution and contributes to the process by which biological populations become distinct species.

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PMID:
29320479
PMCID:
PMC5988642
DOI:
10.1038/nature25188
[Indexed for MEDLINE]
Free PMC Article

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