A yeast living ancestor reveals the origin of genomic introgressions

Melania D'Angiolo1, Matteo De Chiara1, Jia-Xing Yue1, Agurtzane Irizar1, Simon Stenberg2,3, Karl Persson3, Agnès Llored1, Benjamin Barré1, Joseph Schacherer4, Roberto Marangoni5,6, Eric Gilson1,7, Jonas Warringer3, Gianni Liti8

  1. Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France.
  2. Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), Ås, Norway.
  3. Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
  4. Université de Strasbourg, CNRS, GMGM UMR 7156, Strasbourg, France.
  5. Department of Biology, University of Pisa, Pisa, Italy.
  6. Institute of Biophysics, CNR, Pisa, Italy.
  7. Department of Genetics, CHU, Nice, France.
  8. Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France. gianni.liti@unice.fr.

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.

Presented By Melania D'Angiolo