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A beak size locus in Darwin’s finches facilitated character displacement during a drought
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.ORCID iD: 0000-0003-4826-0349
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
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2016 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 352, no 6284, p. 470-474Article 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.

Place, publisher, year, edition, pages
2016. Vol. 352, no 6284, p. 470-474
National Category
Genetics and Breeding
Identifiers
URN: urn:nbn:se:uu:diva-279968DOI: 10.1126/science.aad8786ISI: 000374479700050PubMedID: 27102486OAI: oai:DiVA.org:uu-279968DiVA, id: diva2:909305
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council, 80576801Swedish Research Council, 70374401Available from: 2016-03-06 Created: 2016-03-06 Last updated: 2019-11-28Bibliographically approved
In thesis
1. The genetic basis for adaptation in natural populations
Open this publication in new window or tab >>The genetic basis for adaptation in natural populations
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. p. 60
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1192
Keywords
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:nbn:se:uu:diva-279969 (URN)978-91-554-9502-2 (ISBN)
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
2. Genetic Adaptation and Speciation in Darwin’s Finches and Atlantic Herring
Open this publication in new window or tab >>Genetic Adaptation and Speciation in Darwin’s Finches and Atlantic Herring
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Natural selection acts on existing genetic variation to drive genetic adaptation of organisms to various ecological niches. Interaction between closely related populations, through processes such as competition and hybridization, may either lead to their divergence or population fusion, which has consequences for adaptation and the formation of species. This thesis aims to use two natural populations, Darwin’s finches and Atlantic herring, as models to explore the genetic mechanisms underlying ecological adaptation and speciation.

The ecological adaptation of Darwin’s finches across the Galápagos Islands is primarily reflected by variation in beak morphology. Using whole-genome re-sequencing of all Darwin’s finch species, we discover that a locus, HMGA2, is highly associated with variation in beak size. Data collected before and after a severe drought show that this locus plays a critical role for ecological character displacement in large ground finches Geospiza magnirostris and medium ground finches G. fortis.

Genomic islands of divergence refer to genomic regions of elevated divergence when comparing the genomes of closely related taxa. Establishment of these genomic islands can reflect a role in reproductive isolation or be related to ecological adaptation or background selection. Investigating their properties can shed light on how new species evolve. We study the landscape of genomic islands in Darwin’s finches, and find that the most pronounced genomic islands are likely ancient balanced polymorphisms, which govern adaptive variation in beak morphology.

Hybridization is increasingly recognized as an important evolutionary process which may lead to speciation. We study two cases of hybridization in Darwin’s finches. In the first case, a new lineage of Darwin’s finches was founded through hybridization between a resident medium ground finch G. fortis and an immigrant Española cactus finch G. conirostris. In the second case, female-biased introgression occurred predominantly from medium ground finches G. fortis to common cactus finches G. scandens. Our genetic analysis on the mosaic genomes of hybrid finches show that non-random mating and natural selection primarily determine the outcome of hybridization.

We generate a chromosome-level assembly of the Atlantic herring with a total size of 726 Mb, which coincides with a high-resolution linkage map and an LD-based recombination map. This facilitates the identification of an ~8Mb inversion, which is likely to be associated with ecological adaptation in herring to differences in water temperature. The contiguity of the assembly sorts placement of loci under selection that were identified based on a previous, highly fragmented draft assembly of the herring genome.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2020. p. 49
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1620
Keywords
Darwin's finches, Atlantic herring, Population genetics, Evolution, Ecological adaptation, Speciation
National Category
Ecology Evolutionary Biology Genetics
Research subject
Biology with specialization in Animal Ecology; Bioinformatics
Identifiers
urn:nbn:se:uu:diva-397886 (URN)978-91-513-0826-5 (ISBN)
Public defence
2020-02-28, Room C8:305, BMC, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2020-01-13 Created: 2019-11-28 Last updated: 2020-01-13

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Lamichhaney, SangeetHan, FanBerglund, JonasWang, ChaoSällman Almen, MarkusT. Webster, MatthewAndersson, Leif

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