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Repeated evolution of self-compatibility for reproductive assurance
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Ludwig Maximilians Univ Munchen, Div Evolutionary Biol, Fac Biol, Grosshaderner Str 2, D-82152 Planegg Martinsried, Germany.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Ludwig Maximilians Univ Munchen, Div Evolutionary Biol, Fac Biol, Grosshaderner Str 2, D-82152 Planegg Martinsried, Germany.ORCID iD: 0000-0002-0612-9230
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-8412-7919
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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.

Place, publisher, year, edition, pages
2018. Vol. 9, article id 1639
National Category
Genetics
Identifiers
URN: urn:nbn:se:uu:diva-354954DOI: 10.1038/s41467-018-04054-6ISI: 000430674000028PubMedID: 29691402OAI: oai:DiVA.org:uu-354954DiVA, id: diva2:1223564
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
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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Supervisors
Available from: 2019-10-02 Created: 2019-09-03 Last updated: 2019-10-15

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Nieuwenhuis, Bart P. S.Tusso Gomez, SergioBjerling, PernillaStångberg, JosefineWolf, Jochen B. W.

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