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Ancestral admixture is the main determinant of global biodiversity in fission yeast
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab. Division of Evolutionary Biology, Faculty of Biology, LMU Munich, Planegg-Martinsried, Germany.ORCID iD: 0000-0002-0612-9230
Division of Evolutionary Biology, Faculty of Biology, LMU Munich, Planegg-Martinsried, Germany.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX.
Bioscience Technology Facility, Department of Biology, University of York, York, United Kingdom.
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2019 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 9, p. 1975-1989Article in journal (Refereed) Published
Abstract [en]

Mutation and recombination are key evolutionary processes governing phenotypic variation and reproductive isolation. We here demonstrate that biodiversity within all globally known strains of Schizosaccharomyces pombe arose through admixture between two divergent ancestral lineages. Initial hybridization was inferred to have occurred similar to 20-60 sexual outcrossing generations ago consistent with recent, human-induced migration at the onset of intensified transcontinental trade. Species-wide heritable phenotypic variation was explained near-exclusively by strain-specific arrangements of alternating ancestry components with evidence for transgressive segregation. Reproductive compatibility between strains was likewise predicted by the degree of shared ancestry. To assess the genetic determinants of ancestry block distribution across the genome, we characterized the type, frequency, and position of structural genomic variation using nanopore and single-molecule real-time sequencing. Despite being associated with double-strand break initiation points, over 800 segregating structural variants exerted overall little influence on the introgression landscape or on reproductive compatibility between strains. In contrast, we found strong ancestry disequilibrium consistent with negative epistatic selection shaping genomic ancestry combinations during the course of hybridization. This study provides a detailed, experimentally tractable example that genomes of natural populations are mosaics reflecting different evolutionary histories. Exploiting genome-wide heterogeneity in the history of ancestral recombination and lineage-specific mutations sheds new light on the population history of S. pombe and highlights the importance of hybridization as a creative force in generating biodiversity.

Place, publisher, year, edition, pages
Oxford University Press, 2019. Vol. 36, no 9, p. 1975-1989
Keywords [en]
hybridization, structural variation, epistasis, reproductive isolation, transgression, Schizosaccharomyces pombe
National Category
Evolutionary Biology Biochemistry and Molecular Biology
Identifiers
URN: urn:nbn:se:uu:diva-390729DOI: 10.1093/molbev/msz126ISI: 000493043800011PubMedID: 31225876OAI: oai:DiVA.org:uu-390729DiVA, id: diva2:1342622
Funder
Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)NIH (National Institute of Health), UM1 HG008898Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-11-18Bibliographically approved
In thesis
1. Adaptive divergence in fission yeast: From experimental evolution to evolutionary genomics
Open this publication in new window or tab >>Adaptive divergence in fission yeast: From experimental evolution to evolutionary genomics
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

How adaptation and population differentiation occur is fundamental to understand the origin of biodiversity. Work in speciation alongside the increased ease of generating genomic data have allowed the exploration of genomic changes relevant to adaptation. However, it remains challenging to infer the underlying mechanisms from genomic patterns of divergence governed by both genomic properties and external selective pressures. The chronological order of genomic changes, evolutionary history and selective forces can rarely be inferred from natural populations.

Currently, I see two promising ways to tackle the problem of the genomic underpinnings of divergence: (1) evolution experiments simulating adaptation and population divergence and measuring genomic changes as they occur through time; (2) empirical studies of closely related populations in which the extent of divergence varies, allowing us to infer the chronology of the genomic changes. In my Ph.D. research I applied these two approaches, using the fungus Schizosaccharomyces pombe. First, I experimentally tested the potential for ecological divergence with gene flow, and investigated genomic and phenotypic changes associated with this process. Next, I studied genomic data obtained from natural populations sampled worldwide.  In both cases, the genetic inference relied on different sequencing technologies including the Illumina, Pacific Biosciences and Oxford Nanopore platforms.

The experiment explored the effect of gene flow on phenotype and fitness, and uncovered potential molecular mechanisms underlying adaptive divergence. In paper I we demonstrate the emergence of specialisation under low gene flow, but generalist strategies when gene flow was high. Evolved phenotypes were largely influenced by standing genetic variation subject to opposite antagonistic pleiotropy complemented by new mutations enriched in a subset of genes. In paper II, we show that the experimental selective regime also had an effect on mating strategies, result of temporal ecological heterogeneity and selection for mating efficiency. We found that the evolution of mating strategies was explained by a trade-off between mating efficiency and asexual growth rate dependent on environmental stability. Papers III and IV consider the role of gene flow in natural populations. In paper III, we provide evidence that gene flow also played a predominant role in adaptive divergence in nature. All strains resulted from recent hybridization between two ancestral groups manifested in large phenotypic variation and reproductive isolation.This demographic history of hybridization was confirmed in paper IV focusing on patterns of mitochondrial diversity, adding evidence for the geographic distribution of the ancestral populations and potential for horizontal gene transfer from a distant yeast clade. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 68
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1851
Keywords
adaptation, divergence, selection, experimental evolution, genomics, genome evolution, population genetics, fission yeast, phenotypic variation
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-392422 (URN)978-91-513-0743-5 (ISBN)
Public defence
2019-10-25, Lindahlsalen, Evolutionsbiologiskt centrum, Norbyvägen 18A , Uppsala, 13:00 (English)
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Available from: 2019-10-02 Created: 2019-09-03 Last updated: 2019-10-15

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