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The genetic basis for adaptation in natural populations
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.ORCID iD: 0000-0003-4826-0349
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Many previous studies in evolutionary genetics have been based on few model organisms that can be reared at ease in the laboratory. In contrast, genetic studies of non-model, natural populations are desirable as they provide a wider range of adaptive phenotypes throughout evolutionary timescales and allow a more realistic understanding of how natural selection drives adaptive evolution. This thesis represents an example of how modern genomic tools can be effectively used to study adaptation in natural populations.

Atlantic herring is one of the world’s most numerous fish having multiple populations with phenotypic differences adapted to strikingly different environments. Our study demonstrated insignificant level of genetic drift in herring that resulted in minute genetic differences in the majority of the genome among these populations. In contrast, a small percentage of the loci showed striking genetic differentiation that were potentially under natural selection. We identified loci associated with adaptation to the Baltic Sea and with seasonal reproduction (spring- and autumn-spawning) and demonstrated that ecological adaptation in Atlantic herring is highly polygenic but controlled by a finite number of loci.

The study of Darwin’s finches constitutes a breakthrough in characterizing their evolution. We identified two loci, ALX1 and HMGA2, which most likely are the two most prominent loci that contributed to beak diversification and thereby to expanded food utilization. These loci have played a key role in adaptive evolution of Darwin’s finches. Our study also demonstrated that interspecies gene flow played a significant role in the radiation of Darwin’s finches and some species have a mixed ancestry.

This thesis also explored the genetic basis for the remarkable phenotypic differences between three male morphs in the ruff. Identification of two different versions of a 4.5 MB inversion in Satellites and Faeders that occurred about 4 million years ago revealed clues about the genetic foundation of male mating strategies in ruff. We highlighted two genes in the inverted region; HSD17B2 that affects metabolism of testosterone and MC1R that has a key role in regulating pigmentation, as the major loci associated with this adaptation.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 60 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1192
Keyword [en]
Adaptive evolution, Atlantic herring, ecological adaptation, seasonal reproduction, TSHR, Darwin’s finches, natural selection, beak, ALX1, HMGA2, ruff, lek, inversion, HSD17B2, MC1R
National Category
Genetics and Breeding
Identifiers
URN: urn:nbn:se:uu:diva-279969ISBN: 978-91-554-9502-2 (print)OAI: oai:DiVA.org:uu-279969DiVA: diva2:909306
Public defence
2016-04-29, B41, BMC, Husargätan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2016-04-06 Created: 2016-03-06 Last updated: 2017-04-03
List of papers
1. Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring
Open this publication in new window or tab >>Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring
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2012 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 109, no 47, 19345-19350 p.Article in journal (Refereed) Published
Abstract [en]

The Atlantic herring (Clupea harengus), one of the most abundant marine fishes in the world, has historically been a critical food source in Northern Europe. It is one of the few marine species that can reproduce throughout the brackish salinity gradient of the Baltic Sea. Previous studies based on few genetic markers have revealed a conspicuous lack of genetic differentiation between geographic regions, consistent with huge population sizes and minute genetic drift. Here, we present a cost-effective genome-wide study in a species that lacks a genome sequence. We first assembled amuscle transcriptome and then aligned genomic reads to the transcripts, creating an "exome assembly," capturing both exons and flanking sequences. We then resequenced pools of fish from a wide geographic range, including the Northeast Atlantic, as well as different regions in the Baltic Sea, aligned the reads to the exome assembly, and identified 440,817 SNPs. The great majority of SNPs showed no appreciable differences in allele frequency among populations; however, several thousand SNPs showed striking differences, some approaching fixation for different alleles. The contrast between low genetic differentiation at most loci and striking differences at others implies that the latter category primarily reflects natural selection. A simulation study confirmed that the distribution of the fixation index F-ST deviated significantly from expectation for selectively neutral loci. This study provides insights concerning the population structure of an important marine fish and establishes the Atlantic herring as a model for population genetic studies of adaptation and natural selection.

Keyword
Baltic herring, genetics, population biology
National Category
Natural Sciences Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-191049 (URN)10.1073/pnas.1216128109 (DOI)000311997200067 ()
Available from: 2013-01-09 Created: 2013-01-09 Last updated: 2017-12-06Bibliographically approved
2. The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
Open this publication in new window or tab >>The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
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2016 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 5, e12081Article in journal (Refereed) Published
Abstract [en]

Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.

National Category
Genetics and Breeding Evolutionary Biology Genetics Fish and Aquacultural Science
Identifiers
urn:nbn:se:uu:diva-279967 (URN)10.7554/eLife.12081 (DOI)000387459700001 ()27138043 (PubMedID)
Funder
EU, European Research CouncilSwedish Research Council FormasKnut and Alice Wallenberg Foundation
Note

Alvaro Martinez Barrio, Sangeet Lamichhaney, Guangyi Fan and Nima Rafati contributed equally to this work.

Available from: 2016-03-06 Created: 2016-03-06 Last updated: 2017-11-29Bibliographically approved
3. Evolution of Darwin's finches and their beaks revealed by genome sequencing
Open this publication in new window or tab >>Evolution of Darwin's finches and their beaks revealed by genome sequencing
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2015 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 518, no 7539Article in journal (Refereed) Published
Abstract [en]

Darwin's finches, inhabiting the Galapagos archipelago and Cocos Island, constitute an iconic model for studies of speciation and adaptive evolution. Here we report the results of whole-genome re-sequencing of 120 individuals representing all of the Darwin's finch species and two close relatives' Phylogenetic analysis reveals important discrepancies with the phenotype-based taxonomy. We find extensive evidence for interspecific gene flow throughout the radiation. Hybridization has given rise to species of mixed ancestry. A 240 kilobase haplotype encompassing the ALX1 gene that encodes a transcription factor affecting craniofacial. development is strongly associated with beak shape diversity across Darwin's finch species as well as within the medium ground finch (Geospiza fortis) a species that has undergone rapid evolution of beak shape in response to environmental changes. The ALX1 haplotype has contributed to diversification of beak shapes among the Darwin's finches and thereby, to an expanded utilization of food resources.

National Category
Medical Genetics Microbiology in the medical area
Identifiers
urn:nbn:se:uu:diva-247384 (URN)10.1038/nature14181 (DOI)000349547400036 ()25686609 (PubMedID)
Available from: 2015-03-20 Created: 2015-03-18 Last updated: 2017-12-04Bibliographically approved
4. A beak size locus in Darwin’s finches facilitated character displacement during a drought
Open this publication in new window or tab >>A beak size locus in Darwin’s finches facilitated character displacement during a drought
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2016 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 352, no 6284, 470-474 p.Article in journal (Refereed) Published
Abstract [en]

Ecological character displacement is a process of morphological divergence that reducescompetition for limited resources. We used genomic analysis to investigate the geneticbasis of a documented character displacement event in Darwin’s finches on Daphne Majorin the Galápagos Islands: The medium ground finch diverged from its competitor, the largeground finch, during a severe drought. We discovered a genomic region containing theHMGA2gene that varies systematically among Darwin’s finch species with different beaksizes. Two haplotypes that diverged early in the radiation were involved in the characterdisplacement event: Genotypes associated with large beak size were at a strong selectivedisadvantage in medium ground finches (selection coefficients= 0.59). Thus, a majorlocus has apparently facilitated a rapid ecological diversification in the adaptive radiationof Darwin’s finches.

National Category
Genetics and Breeding
Identifiers
urn:nbn:se:uu:diva-279968 (URN)10.1126/science.aad8786 (DOI)000374479700050 ()27102486 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council, 80576801Swedish Research Council, 70374401
Available from: 2016-03-06 Created: 2016-03-06 Last updated: 2017-11-30Bibliographically approved
5. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)
Open this publication in new window or tab >>Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)
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2016 (English)In: Nature Genetics, ISSN 1061-4036, E-ISSN 1546-1718, Vol. 48, no 1, 84-+ p.Article in journal (Refereed) Published
Abstract [en]

The ruff is a Palearctic wader with a spectacular lekking behavior where highly ornamented males compete for females(1-4). This bird has one of the most remarkable mating systems in the animal kingdom, comprising three different male morphs (independents, satellites and faeders) that differ in behavior, plumage color and body size. Remarkably, the satellite and faeder morphs are controlled by dominant alleles(5,6). Here we have used whole-genome sequencing and resolved the enigma of how such complex phenotypic differences can have a simple genetic basis. The Satellite and Faeder alleles are both associated with a 4.5-Mb inversion that occurred about 3.8 million years ago. We propose an evolutionary scenario where the Satellite chromosome arose by a rare recombination event about 500,000 years ago. The ruff mating system is the result of an evolutionary process in which multiple genetic changes contributing to phenotypic differences between morphs have accumulated within the inverted region.

National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-274919 (URN)10.1038/ng.3430 (DOI)000367255300018 ()26569123 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council, 1989-2546Swedish Research Council, 1992-2685Swedish Research Council, 2013-5418Swedish Research Council, 2001-6005Swedish Research Council, 80576801Swedish Research Council, 70374401
Available from: 2016-01-27 Created: 2016-01-26 Last updated: 2017-11-30Bibliographically approved

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