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

• Published in: Nature (London) Vol. 553; no. 7688; pp. 337 - 341
• Main Authors: Gibeaux, Romain, Acker, Rachael, Kitaoka, Maiko, Georgiou, Georgios, van Kruijsbergen, Ila, Ford, Breanna, Marcotte, Edward M., Nomura, Daniel K., Kwon, Taejoon, Veenstra, Gert Jan C., Heald, Rebecca
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 18.01.2018; Nature Publishing Group
• Subjects: 13; 13/1; 13/51; 14; 14/1; 14/19; 14/35; 14/63; 38; 38/22; 42; 45; 45/91; 49/23; 49/39; 631/181; 631/80; 64/114; Animals; Biodiversity; Biological activity; Biological evolution; Cell cycle; Cell death; Chromosome abnormalities; Chromosome Segregation; Chromosomes; Chromosomes - genetics; Chromosomes - metabolism; Cytoplasm; Cytoplasm - genetics; Cytoplasm - metabolism; Deoxyribonucleic acid; DNA; Eggs; Embryo Loss - veterinary; Embryos; Evolution; Evolution, Molecular; Female; Frogs; Gastrulation; Gene expression; Gene sequencing; Genetic aspects; Genetic diversity; Genetic Speciation; Genomes; Growth; Humanities and Social Sciences; Hybridization; Hybridization, Genetic; Interspecific; Interspecific hybridization; letter; Life Sciences; Male; Mitosis; Molecular modelling; Morphology; multidisciplinary; Nuclei; Paternal Inheritance - genetics; Physiological aspects; Reproductive isolation; Science; Speciation; Sperm; Spindles; Transcription; Xenopus; Xenopus - genetics; Xenopus - metabolism; Xenopus laevis; Xenopus laevis - genetics; Xenopus tropicalis; Zoological research; United States
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature25188

In hybrid inviability between Xenopus laevis and Xenopus tropicalis , genomic regions on two 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. Incompatibility issues Interbreeding between some closely related species can result in inviable embryos. However, the molecular mechanisms behind these evolutionary barriers are not well characterized. Rebecca Heald and colleagues examine the mechanisms involved in hybrid inviability between two closely related species of clawed frog, Xenopus laevis and Xenopus tropicalis . They find that genomic regions on two X. laevis chromosomes are lost prior to embryonic cell death and show mis-segration during mitosis. This leads to unbalanced gene expression at the maternal to zygotic transition, followed by cell-autonomous catastrophic embryo death. 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 1 , 2 . 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 3 . 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 4 . Nevertheless, early development transcriptional programs, gene expression patterns, and protein sequences are generally conserved 5 , 6 . Whereas the hybrid produced when X. laevis eggs are fertilized by X. tropicalis sperm is viable, the reverse hybrid dies before gastrulation 7 , 8 . 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.