A yeast living ancestor reveals the origin of genomic introgressions

Melania D’Angiolo, Matteo De Chiara, Jia-Xing Yue, Agurtzane Irizar, Simon Stenberg, Karl Persson, Agnès Llored, Benjamin Barré, Joseph Schacherer, Roberto Marangoni, Eric Gilson, Jonas Warringer and Gianni Liti ()
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Melania D’Angiolo: Université Côte d’Azur, CNRS, INSERM, IRCAN
Matteo De Chiara: Université Côte d’Azur, CNRS, INSERM, IRCAN
Jia-Xing Yue: Université Côte d’Azur, CNRS, INSERM, IRCAN
Agurtzane Irizar: Université Côte d’Azur, CNRS, INSERM, IRCAN
Simon Stenberg: Norwegian University of Life Sciences (UMB)
Karl Persson: University of Gothenburg
Agnès Llored: Université Côte d’Azur, CNRS, INSERM, IRCAN
Benjamin Barré: Université Côte d’Azur, CNRS, INSERM, IRCAN
Joseph Schacherer: Université de Strasbourg, CNRS, GMGM UMR 7156
Roberto Marangoni: University of Pisa
Eric Gilson: Université Côte d’Azur, CNRS, INSERM, IRCAN
Jonas Warringer: University of Gothenburg
Gianni Liti: Université Côte d’Azur, CNRS, INSERM, IRCAN

Nature, 2020, vol. 587, issue 7834, 420-425

Abstract: Abstract Genome introgressions drive evolution across the animal1, plant2 and fungal3 kingdoms. Introgressions initiate from archaic admixtures followed by repeated backcrossing to one parental species. However, how introgressions arise in reproductively isolated species, such as yeast4, has remained unclear. Here we identify a clonal descendant of the ancestral yeast hybrid that founded the extant Saccharomyces cerevisiae Alpechin lineage5, which carries abundant Saccharomyces paradoxus introgressions. We show that this clonal descendant, hereafter defined as a ‘living ancestor’, retained the ancestral genome structure of the first-generation hybrid with contiguous S. cerevisiae and S. paradoxus subgenomes. The ancestral first-generation hybrid underwent catastrophic genomic instability through more than a hundred mitotic recombination events, mainly manifesting as homozygous genome blocks generated by loss of heterozygosity. These homozygous sequence blocks rescue hybrid fertility by restoring meiotic recombination and are the direct origins of the introgressions present in the Alpechin lineage. We suggest a plausible route for introgression evolution through the reconstruction of extinct stages and propose that genome instability allows hybrids to overcome reproductive isolation and enables introgressions to emerge.

Date: 2020
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DOI: 10.1038/s41586-020-2889-1

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