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Recombining your way out of trouble: The genetic architecture of hybrid fitness under environmental stress

Zhang, Z; Bendixsen, DP; Janzen, T; Nolte, AW; Greig, D; Stelkens, R; (2019) Recombining your way out of trouble: The genetic architecture of hybrid fitness under environmental stress. Molecular Biology and Evolution 10.1093/molbev/msz211. (In press). Green open access

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Abstract

Hybridization between species can either promote or impede adaptation. But there is a deficit in our understanding of the genetic basis of hybrid fitness, especially in non-domesticated organisms, and when populations are facing environmental stress. We made genetically variable F2 hybrid populations from two divergent Saccharomyces yeast species. We exposed populations to ten toxins and sequenced the most resilient hybrids on low coverage using ddRADseq to investigate four aspects of their genomes: 1) hybridity, 2) interspecific heterozygosity, 3) epistasis (positive or negative associations between non-homologous chromosomes) and 4) ploidy. We used linear mixed effect models and simulations to measure to which extent hybrid genome composition was contingent on the environment. Genomes grown in different environments varied in every aspect of hybridness measured, revealing strong genotype-environment interactions. We also found selection against heterozygosity or directional selection for one of the parental alleles, with larger fitness of genomes carrying more homozygous allelic combinations in an otherwise hybrid genomic background. In addition, individual chromosomes and chromosomal interactions showed significant species biases and pervasive aneuploidies. Against our expectations, we observed multiple beneficial, opposite-species chromosome associations, confirmed by epistasis- and selection-free computer simulations, which is surprising given the large divergence of parental genomes (∼15%). Together, these results suggest that successful, stress-resilient hybrid genomes can be assembled from the best features of both parents without paying high costs of negative epistasis. This illustrates the importance of measuring genetic trait architecture in an environmental context when determining the evolutionary potential of genetically diverse hybrid populations.

Type: Article
Title: Recombining your way out of trouble: The genetic architecture of hybrid fitness under environmental stress
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1093/molbev/msz211
Publisher version: https://doi.org/10.1093/molbev/msz211
Language: English
Additional information: Copyright © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com.
Keywords: Saccharomyces, ddRADseq, environmental stress, epistasis, genome evolution, heterozygosity, hybridization
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10082511
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