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On the origin of an insular hybrid butterfly species
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0537-8219
Department of Biology, Lund University, Lund, Sweden.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0961-8427
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Most species arise from the divergence of two populations within a species, but this is not only way speciation can occur. A new species can also evolve when diverging lineages hybridize and give rise to a persistent and ecologically differentiated species. Hybrid speciation in animals has been intensely debated, partly because hard evidence for the process have been difficult to gain. Recent access to large-scale, whole-genome sequencing data and development of novel analytical methods have made it more feasible to statistically test for hybrid origin of lineages. Here we report the discovery of a hybrid butterfly lineage. This lineage is mainly inhabiting an island in the Baltic Sea in Northern Europe and was previously described as a subspecies (horkei) of one of the parental species (Aricia artaxerxes). By analyzing whole-genome resequencing data, we conclude that horkei originated as a consequence of hybridization between A. artaxerxes and A. agestis. We show that this hybridization event occurred approximately 54,000 years ago, predating the last glaciation of the current distribution range. Horkei must therefore have persisted long enough to be able to colonize its current distribution range, despite that this range lies between the current ranges of the parental species. The hybrid origin, the maintenance of genomic integrity through time periods with dramatic climatic changes and the expression of a combination of parental traits - such as voltinism and host plant use - suggest that horkei can be considered a distinct species (Aricia horkei stat. nov.). Thus, we add to a growing list of hybrid speciation cases in animals.

Keywords [en]
Biodiversity, Evolutionary Genetics, Speciation, Hybridization, Hybrid species
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-532922OAI: oai:DiVA.org:uu-532922DiVA, id: diva2:1875571
Available from: 2024-06-23 Created: 2024-06-23 Last updated: 2024-06-24Bibliographically 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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