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Regulatory and evolutionary impact of DNA methylation in two songbird species and their naturally occurring F1 hybrids
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0537-8219
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-1178-4053
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Lyon 1, CNRS, Lab Biometry & Evolutionary Biol, UMR 5558, Villeurbanne, France..
2024 (English)In: BMC Biology, E-ISSN 1741-7007, Vol. 22, no 1, article id 124Article in journal (Refereed) Published
Abstract [en]

Background:  Regulation of transcription by DNA methylation in 5'-CpG-3' context is a widespread mechanism allowing differential expression of genetically identical cells to persist throughout development. Consequently, differences in DNA methylation can reinforce variation in gene expression among cells, tissues, populations, and species. Despite a surge in studies on DNA methylation, we know little about the importance of DNA methylation in population differentiation and speciation. Here we investigate the regulatory and evolutionary impact of DNA methylation in five tissues of two Ficedula flycatcher species and their naturally occurring F-1 hybrids.

Results: We show that the density of CpG in the promoters of genes determines the strength of the association between DNA methylation and gene expression. The impact of DNA methylation on gene expression varies among tissues with the brain showing unique patterns. Differentially expressed genes between parental species are predicted by genetic and methylation differentiation in CpG-rich promoters. However, both these factors fail to predict hybrid misexpression suggesting that promoter mismethylation is not a main determinant of hybrid misexpression in Ficedula flycatchers. Using allele-specific methylation estimates in hybrids, we also determine the genome-wide contribution of cis- and trans effects in DNA methylation differentiation. These distinct mechanisms are roughly balanced in all tissues except the brain, where trans differences predominate.

Conclusions:  Overall, this study provides insight on the regulatory and evolutionary impact of DNA methylation in songbirds.

Place, publisher, year, edition, pages
BioMed Central (BMC), 2024. Vol. 22, no 1, article id 124
Keywords [en]
DNA methylation, Speciation, Transcriptomics, Epigenomics
National Category
Genetics Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-531095DOI: 10.1186/s12915-024-01920-2ISI: 001234529800003PubMedID: 38807214OAI: oai:DiVA.org:uu-531095DiVA, id: diva2:1868826
Funder
Swedish Research Council, 2013- 8271Swedish Research Council, 2012-3722Swedish Research Council, 2022-06725Knut and Alice Wallenberg Foundation, 2014/0044Available from: 2024-06-12 Created: 2024-06-12 Last updated: 2024-06-23Bibliographically approved
In thesis
1. Genetic architecture of speciation
Open this publication in new window or tab >>Genetic architecture of speciation
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

New species are formed either by the splitting of a lineage in two or through hybridization of divergent lineages. Using genetics to understand the origin and persistence of species is a central theme in evolutionary biology. The genetic architecture of speciation refers to the number, types and effect sizes of different genetic loci underlying the process of speciation. Insightful models and painstaking laboratory and field work have provided the first sketches of the genetic architecture of speciation in a handful of model organisms. In this thesis, I explore different aspects of speciation genetics in several less studied model systems: from birds to butterflies. In Paper I, I investigate the genetic architecture of hybrid inviability between chromosomal races of the wood white butterfly (Leptidea sinapis) and find an association between chromosome fusions and the evolution of hybrid inviability. In Paper II, I study whether the many chromosomal differences separating the L. sinapis races show evidence of non-Mendelian inheritance. We observe the preferential inheritance of the ancestral state at chromosome fusions in line with the meiotic drive model. Thus, meiotic drive acts against karyotype change and thus potentially opposes the evolution of reproductive isolation. Recent work has highlighted that epigenetic mechanisms, such as DNA methylation, could be important for the dysfunction of hybrids. In Paper III, we test this prediction in naturally occurring hybrids between the collared flycatcher (F. albicollis) and the pied flycatcher (F. hypoleuca). I show that DNA methylation differences in promoter regions are often correlated with signatures of differential gene expression between species, but does not predict misexpression in hybrids. Hybridization between species is expected to reduce the genetic differentiation and erode species differences. However, hybridization can also be the trigger of speciation if the combination of alleles and traits allow the hybrid species to persist. In Paper IV, I discover a hybrid Aricia butterfly species on the island of Öland in the Baltic Sea. Using whole-genome resequencing data and species models I infer that the main hybridization event occurred approximately 54,000 years ago, long before Öland arose from the sea after the last ice age. To conclude, this thesis highlights different aspects of speciation genetics: from the genetic underpinnings of viability of hybrids (Paper I and III) to causes of speciation (Paper II and IV). Hopefully this work will provide a few more lines to the blueprint that is our understanding of the genetic architecture of speciation

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2024. p. 63
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2418
Keywords
Speciation, Evolutionary genetics, Speciation genetics, Hybrid incompatibilities
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-532935 (URN)978-91-513-2170-7 (ISBN)
Public defence
2024-09-06, Ekmansalen, Evolutionsbiolgiskt Centrum, Norbyvägen 14, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2024-08-16 Created: 2024-06-23 Last updated: 2024-08-16

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Boman, JesperQvarnström, AnnaMugal, Carina

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