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The genetic basis for adaptation in natural populations
Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi.ORCID-id: 0000-0003-4826-0349
2016 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
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.

Ort, förlag, år, upplaga, sidor
Uppsala: Acta Universitatis Upsaliensis, 2016. , s. 60
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1192
Nyckelord [en]
Adaptive evolution, Atlantic herring, ecological adaptation, seasonal reproduction, TSHR, Darwin’s finches, natural selection, beak, ALX1, HMGA2, ruff, lek, inversion, HSD17B2, MC1R
Nationell ämneskategori
Genetik och förädling
Identifikatorer
URN: urn:nbn:se:uu:diva-279969ISBN: 978-91-554-9502-2 (tryckt)OAI: oai:DiVA.org:uu-279969DiVA, id: diva2:909306
Disputation
2016-04-29, B41, BMC, Husargätan 3, Uppsala, 13:15 (Engelska)
Opponent
Handledare
Tillgänglig från: 2016-04-06 Skapad: 2016-03-06 Senast uppdaterad: 2017-04-03
Delarbeten
1. Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring
Öppna denna publikation i ny flik eller fönster >>Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring
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2012 (Engelska)Ingår i: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 109, nr 47, s. 19345-19350Artikel i tidskrift (Refereegranskat) 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.

Nyckelord
Baltic herring, genetics, population biology
Nationell ämneskategori
Naturvetenskap Medicin och hälsovetenskap
Identifikatorer
urn:nbn:se:uu:diva-191049 (URN)10.1073/pnas.1216128109 (DOI)000311997200067 ()
Tillgänglig från: 2013-01-09 Skapad: 2013-01-09 Senast uppdaterad: 2017-12-06Bibliografiskt granskad
2. The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
Öppna denna publikation i ny flik eller fönster >>The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
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2016 (Engelska)Ingår i: eLIFE, E-ISSN 2050-084X, Vol. 5, artikel-id e12081Artikel i tidskrift (Refereegranskat) 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.

Nationell ämneskategori
Genetik och förädling Evolutionsbiologi Genetik Fisk- och akvakulturforskning
Identifikatorer
urn:nbn:se:uu:diva-279967 (URN)10.7554/eLife.12081 (DOI)000387459700001 ()27138043 (PubMedID)
Forskningsfinansiär
EU, Europeiska forskningsrådetForskningsrådet FormasKnut och Alice Wallenbergs Stiftelse
Anmärkning

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

Tillgänglig från: 2016-03-06 Skapad: 2016-03-06 Senast uppdaterad: 2017-11-29Bibliografiskt granskad
3. Evolution of Darwin's finches and their beaks revealed by genome sequencing
Öppna denna publikation i ny flik eller fönster >>Evolution of Darwin's finches and their beaks revealed by genome sequencing
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2015 (Engelska)Ingår i: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 518, nr 7539Artikel i tidskrift (Refereegranskat) 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.

Nationell ämneskategori
Medicinsk genetik Mikrobiologi inom det medicinska området
Identifikatorer
urn:nbn:se:uu:diva-247384 (URN)10.1038/nature14181 (DOI)000349547400036 ()25686609 (PubMedID)
Tillgänglig från: 2015-03-20 Skapad: 2015-03-18 Senast uppdaterad: 2018-01-11Bibliografiskt granskad
4. A beak size locus in Darwin’s finches facilitated character displacement during a drought
Öppna denna publikation i ny flik eller fönster >>A beak size locus in Darwin’s finches facilitated character displacement during a drought
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2016 (Engelska)Ingår i: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 352, nr 6284, s. 470-474Artikel i tidskrift (Refereegranskat) 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.

Nationell ämneskategori
Genetik och förädling
Identifikatorer
urn:nbn:se:uu:diva-279968 (URN)10.1126/science.aad8786 (DOI)000374479700050 ()27102486 (PubMedID)
Forskningsfinansiär
Knut och Alice Wallenbergs StiftelseVetenskapsrådet, 80576801Vetenskapsrådet, 70374401
Tillgänglig från: 2016-03-06 Skapad: 2016-03-06 Senast uppdaterad: 2017-11-30Bibliografiskt granskad
5. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)
Öppna denna publikation i ny flik eller fönster >>Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)
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2016 (Engelska)Ingår i: Nature Genetics, ISSN 1061-4036, E-ISSN 1546-1718, Vol. 48, nr 1, s. 84-+Artikel i tidskrift (Refereegranskat) 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.

Nationell ämneskategori
Genetik
Identifikatorer
urn:nbn:se:uu:diva-274919 (URN)10.1038/ng.3430 (DOI)000367255300018 ()26569123 (PubMedID)
Forskningsfinansiär
Knut och Alice Wallenbergs StiftelseVetenskapsrådet, 1989-2546Vetenskapsrådet, 1992-2685Vetenskapsrådet, 2013-5418Vetenskapsrådet, 2001-6005Vetenskapsrådet, 80576801Vetenskapsrådet, 70374401
Tillgänglig från: 2016-01-27 Skapad: 2016-01-26 Senast uppdaterad: 2017-11-30Bibliografiskt granskad

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