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The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
Uppsala universitet, Science for Life Laboratory, SciLifeLab. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för cell- och molekylärbiologi, Molekylär evolution. Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi.
Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi. Uppsala universitet, Science for Life Laboratory, SciLifeLab.ORCID-id: 0000-0003-4826-0349
State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of Macau, Macau, China; BGI-Shenzhen, Shenzen, China; 5 College of Physics, Qingdao University, Qingdao, China .
Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi. Uppsala universitet, Science for Life Laboratory, SciLifeLab.
Visa övriga samt affilieringar
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.

Ort, förlag, år, upplaga, sidor
2016. Vol. 5, artikel-id e12081
Nationell ämneskategori
Genetik och förädling Evolutionsbiologi Genetik Fisk- och akvakulturforskning
Identifikatorer
URN: urn:nbn:se:uu:diva-279967DOI: 10.7554/eLife.12081ISI: 000387459700001PubMedID: 27138043OAI: oai:DiVA.org:uu-279967DiVA, id: diva2:1070840
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
Ingår i avhandling
1. The genetic basis for adaptation in natural populations
Öppna denna publikation i ny flik eller fönster >>The genetic basis for adaptation in natural populations
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
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:nbn:se:uu:diva-279969 (URN)978-91-554-9502-2 (ISBN)
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
2. Exploring genetic diversity in natural and domestic populations through next generation sequencing
Öppna denna publikation i ny flik eller fönster >>Exploring genetic diversity in natural and domestic populations through next generation sequencing
2017 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
Abstract [en]

Studying genetic diversity in natural and domestic populations is of major importance in evolutionary biology. The recent advent of next generation sequencing (NGS) technologies has dramatically changed the scope of these studies, enabling researchers to study genetic diversity in a whole-genome context. This thesis details examples of studies using NGS data to: (i) characterize evolutionary forces shaping the genome of the Atlantic herring, (ii) detect the genetic basis of speciation and domestication in the rabbit, and, (iii) identify mutations associated with skeletal atavism in Shetland ponies.

The Atlantic herring (Clupea harengus) is the most abundant teleost species inhabiting the North Atlantic. Herring has seasonal reproduction and is adapted to a wide range of salinity (3-35‰) throughout the Baltic Sea and Atlantic Ocean. By using NGS data and whole-genome screening of 20 populations, we revealed the underlying genetic architecture for both adaptive features. Our results demonstrated that differentiated genomic regions have evolved by natural selection and genetic drift has played a subordinate role.

The European rabbit (Oryctolagus cuniculus) is native to the Iberian Peninsula, where two rabbit subspecies with partial reproductive isolation have evolved. We performed whole genome sequencing to characterize regions of reduced introgression. Our results suggest key role of gene regulation in triggering genetic incompatibilities in the early stages of reproductive isolation. Moreover, we studied gene expression in testis and found misregulation of many genes in backcross progenies that often show impaired male fertility. We also scanned whole genome of wild and domestic populations and identified differentiated regions that were enriched for non-coding conserved elements. Our results indicated that selection has acted on standing genetic variation, particularly targeting genes expressed in the central nervous system. This finding is consistent with the tame behavior present in domestic rabbits, which allows them to survive and reproduce under the stressful non-natural rearing conditions provided by humans.

In Shetland ponies, abnormally developed ulnae and fibulae characterize a skeletal deformity known as skeletal atavism. To explore the genetic basis of this disease, we scanned the genome using whole genome resequencing data. We identified two partially overlapping large deletions in the pseudoautosomal region (PAR) of the sex chromosomes that remove the entire coding sequence of the SHOX gene and part of CRLF2 gene. Based on this finding, we developed a diagnostic test that can be used as a tool to eradicate this inherited disease in horses.

Ort, förlag, år, upplaga, sidor
Uppsala: Acta Universitatis Upsaliensis, 2017. s. 62
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1301
Nyckelord
Ecological adaptation, seasonal reproduction, Atlantic herring, domestication, speciation, rabbit, skeletal atavism, Shetland ponies, NGS, SMRT sequencing, genome, transcriptome, assembly, structural variation, genetic diversity, HCE, TSHR, SHOX, CRLF2
Nationell ämneskategori
Genetik
Identifikatorer
urn:nbn:se:uu:diva-315032 (URN)978-91-554-9821-4 (ISBN)
Disputation
2017-03-30, B42, BMC, Husarg. 3, Uppsala, 13:15 (Engelska)
Opponent
Handledare
Forskningsfinansiär
EU, Europeiska forskningsrådet
Tillgänglig från: 2017-03-09 Skapad: 2017-02-08 Senast uppdaterad: 2017-04-03

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Martínez Barrio, ÁlvaroLamichhaney, SangeetRafati, NimaPettersson, MatsDainat, JacquesHöppner, Marc P.Jern, PatricNystedt, BjörnFeng, ChungangRubin, Carl-JohanSällman Almén, MarkusAndersson, Leif
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Science for Life Laboratory, SciLifeLabMolekylär evolutionInstitutionen för medicinsk biokemi och mikrobiologi
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