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Adaptive divergence in fission yeast: From experimental evolution to evolutionary genomics
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Division of Evolutionary Biology, Faculty of Biology, LMU Munich. (Jochen Wolf)ORCID iD: 0000-0002-0612-9230
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 [en]
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: urn:nbn:se:uu:diva-392422ISBN: 978-91-513-0743-5 (print)OAI: oai:DiVA.org:uu-392422DiVA, id: diva2:1348240
Public defence
2019-10-25, Lindahlsalen, Evolutionsbiologiskt centrum, Norbyvägen 18A , Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2019-10-02 Created: 2019-09-03 Last updated: 2019-10-15
List of papers
1. Parallelism in adaptive divergence and the modulating effect of gene flow
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(English)Manuscript (preprint) (Other academic)
Keywords
adaptive divergence, gene flow, experimental evolution
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-392416 (URN)
Available from: 2019-09-03 Created: 2019-09-03 Last updated: 2019-09-03
2. Repeated evolution of self-compatibility for reproductive assurance
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 1639Article in journal (Refereed) Published
Abstract [en]

Sexual reproduction in eukaryotes requires the fusion of two compatible gametes of opposite sexes or mating types. To meet the challenge of finding a mating partner with compatible gametes, evolutionary mechanisms such as hermaphroditism and self-fertilization have repeatedly evolved. Here, by combining the insights from comparative genomics, computer simulations and experimental evolution in fission yeast, we shed light on the conditions promoting separate mating types or self-compatibility by mating-type switching. Analogous to multiple independent transitions between switchers and non-switchers in natural populations mediated by structural genomic changes, novel switching genotypes readily evolved under selection in the experimental populations. Detailed fitness measurements accompanied by computer simulations show the benefits and costs of switching during sexual and asexual reproduction, governing the occurrence of both strategies in nature. Our findings illuminate the trade-off between the benefits of reproductive assurance and its fitness costs under benign conditions facilitating the evolution of self-compatibility.

National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-354954 (URN)10.1038/s41467-018-04054-6 (DOI)000430674000028 ()29691402 (PubMedID)
Funder
Swedish Research CouncilEU, European Research Council, HapSelA-336633Carl Tryggers foundation
Note

These authors jointly supervised this work: Jochen B.W. Wolf, Simone Immler.

Available from: 2018-06-25 Created: 2018-06-25 Last updated: 2019-09-03Bibliographically approved
3. Ancestral admixture is the main determinant of global biodiversity in fission yeast
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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
Keywords
hybridization, structural variation, epistasis, reproductive isolation, transgression, Schizosaccharomyces pombe
National Category
Evolutionary Biology Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-390729 (URN)10.1093/molbev/msz126 (DOI)000493043800011 ()31225876 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)NIH (National Institute of Health), UM1 HG008898
Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-11-18Bibliographically approved
4. Intraspecific diversity of fission yeast mitochondrial genomes
Open this publication in new window or tab >>Intraspecific diversity of fission yeast mitochondrial genomes
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2019 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 11, no 8, p. 2312-2329Article in journal (Refereed) Published
Abstract [en]

The fission yeast Schizosaccharomyces pombe is an important model organism, but its natural diversity and evolutionary history remain under-studied. In particular, the population genomics of the S. pombe mitochondrial genome (mitogenome) has not been thoroughly investigated. Here, we assembled the complete circular-mapping mitogenomes of 192 S. pombe isolates de novo, and found that these mitogenomes belong to 69 nonidentical sequence types ranging from 17,618 to 26,910 bp in length. Using the assembled mitogenomes, we identified 20 errors in the reference mitogenome and discovered two previously unknown mitochondrial introns. Analyzing sequence diversity of these 69 types of mitogenomes revealed two highly distinct clades, with only three mitogenomes exhibiting signs of inter-clade recombination. This diversity pattern suggests that currently available S. pombe isolates descend from two long-separated ancestral lineages. This conclusion is corroborated by the diversity pattern of the recombination-repressed K-region located between donor mating-type loci mat2 and mat3 in the nuclear genome. We estimated that the two ancestral S. pombe lineages diverged about 31 million generations ago. These findings shed new light on the evolution of S. pombe and the data sets generated in this study will facilitate future research on genome evolution.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-390730 (URN)10.1093/gbe/evz165 (DOI)000484266300022 ()31364709 (PubMedID)
Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-10-17Bibliographically approved

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