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Meiotic drive against chromosome fusions in butterfly hybrids
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0537-8219
Stockholm Univ, Dept Zool, Div Ecol, Stockholm, Sweden..
Univ Pompeu Fabra, Inst Biol Evolut, CSIC, Passeig Maritim Barceloneta 37-49, Barcelona 08003, Spain..
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0961-8427
2024 (English)In: Chromosome Research, ISSN 0967-3849, E-ISSN 1573-6849, Vol. 32, no 2, article id 7Article in journal (Refereed) Published
Abstract [en]

Species frequently differ in the number and structure of chromosomes they harbor, but individuals that are heterozygous for chromosomal rearrangements may suffer from reduced fitness. Chromosomal rearrangements like fissions and fusions can hence serve as a mechanism for speciation between incipient lineages, but their evolution poses a paradox. How can rearrangements get fixed between populations if heterozygotes have reduced fitness? One solution is that this process predominantly occurs in small and isolated populations, where genetic drift can override natural selection. However, fixation is also more likely if a novel rearrangement is favored by a transmission bias, such as meiotic drive. Here, we investigate chromosomal transmission distortion in hybrids between two wood white (Leptidea sinapis) butterfly populations with extensive karyotype differences. Using data from two different crossing experiments, we uncover that there is a transmission bias favoring the ancestral chromosomal state for derived fusions, a result that shows that chromosome fusions actually can fix in populations despite being counteracted by meiotic drive. This means that meiotic drive not only can promote runaway chromosome number evolution and speciation, but also that it can be a conservative force acting against karyotypic change and the evolution of reproductive isolation. Based on our results, we suggest a mechanistic model for why chromosome fusion mutations may be opposed by meiotic drive and discuss factors contributing to karyotype evolution in Lepidoptera.

Place, publisher, year, edition, pages
Springer, 2024. Vol. 32, no 2, article id 7
Keywords [en]
Chromosomal rearrangements, Meiotic drive, Lepidoptera, Speciation, Karyotype, Leptidea
National Category
Genetics Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-528711DOI: 10.1007/s10577-024-09752-0ISI: 001221286400001PubMedID: 38702576OAI: oai:DiVA.org:uu-528711DiVA, id: diva2:1860715
Part of project
Molecular mechanisms and evolutionary forces underlying recombination frequency in butterflies, Swedish Research Council
Funder
Swedish Research Council, 2019-04791Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)Stiftelsen Akademiens Nilsson-Ehle medalj, 42499Royal Physiographic Society in Lund, 42499Science for Life Laboratory, SciLifeLabEuropean Regional Development Fund (ERDF)UPPMAXUppsala UniversityAvailable from: 2024-05-24 Created: 2024-05-24 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, JesperBackström, Niclas

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