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Divergence of mitochondrial aerobic metabolism and its molecular basis in two closely related birds adapted to different climates
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0001-7861-7359
Tree of Life, Wellcome Sanger Institute, Hinxton, United Kingdom.
Swiss Ornithological Institute, Sempach, Switzerland.ORCID iD: 0000-0002-7916-3560
Univ Lyon, Université Claude Bernard Lyon 1, Vaulx-en-Velin, France.
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-595681OAI: oai:DiVA.org:uu-595681DiVA, id: diva2:2094491
Available from: 2026-08-23 Created: 2026-08-23 Last updated: 2026-08-23
In thesis
1. Divergence in mitochondrial aerobic metabolism and ecological speciation
Open this publication in new window or tab >>Divergence in mitochondrial aerobic metabolism and ecological speciation
2026 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Genetic incompatibilities causing intrinsic post-zygotic isolation in terms of hybrid sterility and/or inviability ensure the long-term stability of reproductive isolation between diverging lineages. Despite a well-established theoretical foundation and empirical evidence from laboratory experiments, how genetic incompatibilities build up in nature remains poorly understood. Different ecological environments can invoke divergent natural selection on mitochondrial aerobic metabolism, a critical physiological trait controlled by co-evolving mitochondrial and nuclear genomes, and thereby cause mitonuclear incompatibilities between lineages. In this thesis, I investigate the arise of intrinsic postzygotic isolation from divergent ecological adaptation in naturally hybridising pied (Ficedula hypoleuca) and collared flycatchers (Ficedula albicollis), with mitochondrial aerobic metabolism as the crucial phenotypic link. Using long-term monitoring data, I first find viability reductions in hybrids throughout their lifespan, strong at the embryonic stage and subtler later in life, and different mortality trajectories between hybrid adults from reciprocal crosses (Paper I). The results indicate emerging genetic incompatibilities involving segregating or mild-effect alleles and possible mitonuclear incompatibilities. I then reveal ecologically based divergence of mitochondrial aerobic metabolism in Ficedula flycatchers and a complicated, multi-level molecular basis to the divergence (Paper II). Collared flycatchers have more efficient energy production due to high Complex I function in the oxidative phosphorylation (OXPHOS) pathway. This difference likely contributes to subtle differences in environmental sensitivity, competitive ability, incubation temperature and nestling growth potential between the two species. My results imply that natural selection has favoured new adaptive mutations in the mitochondrial genome as well as complementary changes based on standing variation in the nuclear genome. Next, I find that hybrid adults generally resemble the parental species in mitochondrial aerobic respiration (Paper III). Individuals carrying severe BDMIs may have died during earlier energy-demanding life stages such as growth and migration. However, I find evidence for transgressive gene expression in one of the body’s most metabolically demanding tissues, the liver. Finally, I discover that hybrid nestlings have more costly and less efficient metabolism accompanied by high mortality, slower growth and lower fledging mass (a fitness proxy) as compared to non-hybrid nestlings sharing the same rearing environment (Paper IV). I conclude that species divergence in Complex I may have impaired the coordination in the OXPHOS pathway but I have also revealed other candidate BDMI loci. This is the first study exploring the phenotypic consequences of mitonuclear incompatibilities in avian hybrids during the energetically costly nestling stage. Overall, my work demonstrates that divergent natural selection on mitochondrial aerobic metabolism can promote intrinsic postzygotic isolation, leading to ecological speciation.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2026. p. 53
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2709
Keywords
speciation, ecological speciation, mitochondrial aerobic metabolism, BDMI, mitonuclear incomaptibility, hybrid inviability
National Category
Evolutionary Biology Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-595687 (URN)978-91-513-2935-2 (ISBN)
Public defence
2026-10-09, Lindahlsalen, Norbyvägen 14, Uppsala, 10:00 (English)
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Available from: 2026-09-16 Created: 2026-08-23 Last updated: 2026-09-16

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Zhu, YishuChase, MadelineÅlund, MurielleMcFarlane, S. Erynvan der Valk, TomWheatcroft, DavidMugal, CarinaQvarnström, Anna

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