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Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
2011 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 332, no 6031, 845-848 p.Article in journal (Refereed) Published
Abstract [en]

Mitochondria are maternally transmitted; hence, their genome can only make a direct and adaptive response to selection through females, whereas males represent an evolutionary dead end. In theory, this creates a sex-specific selective sieve, enabling deleterious mutations to accumulate in mitochondrial genomes if they exert male-specific effects. We tested this hypothesis, expressing five mitochondrial variants alongside a standard nuclear genome in Drosophila melanogaster, and found striking sexual asymmetry in patterns of nuclear gene expression. Mitochondrial polymorphism had few effects on nuclear gene expression in females but major effects in males, modifying nearly 10% of transcripts. These were mostly male-biased in expression, with enrichment hotspots in the testes and accessory glands. Our results suggest an evolutionary mechanism that results in mitochondrial genomes harboring male-specific mutation loads.

Place, publisher, year, edition, pages
2011. Vol. 332, no 6031, 845-848 p.
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-154276DOI: 10.1126/science.1201157ISI: 000290529900047PubMedID: 21566193OAI: oai:DiVA.org:uu-154276DiVA: diva2:420007
Available from: 2011-05-30 Created: 2011-05-30 Last updated: 2017-12-11Bibliographically approved
In thesis
1. Sexual Conflict and Gene Expression in Drosophila melanogaster
Open this publication in new window or tab >>Sexual Conflict and Gene Expression in Drosophila melanogaster
2011 (English)Doctoral thesis, comprehensive summary (Other academic) [Artistic work]
Abstract [en]

Sexual conflict is broadly defined as a conflict between the evolutionary interests of the two sexes. Depending on the genetic architecture of the traits involved, it can occur at the level of male-female interactions or take the form of selection acting to change the mean of a shared trait against the sign of its genetic correlation. The aim of my thesis was to use genome-wide expression profiles in the model organism Drosophila melanogaster to provide novel insights in the study of sexual conflict.

First, we studied the female post-mating response to partition transcriptional changes associated with reproduction from male-induced effects, which are known to be harmful to females. We found substantial changes in expression of metabolic pathways associated with the activation of reproduction, while male-specific effects were dominated by the onset of an immune response. Changes in female response under different mating strategies was studied using experimental evolution: we found that monogamous females suffered decreased fecundity and their gene expression profiles suggested an overall weaker response to mating. To identify sexually antagonistic genes, we used hemiclonal lines and associated their sex-specific fitness with genome-wide transcript abundance. We confirmed the presence of a negative covariance for fitness and identified a group of candidate genes experiencing sexually antagonistic selection. We then focused on mitochondria, which can enable the accumulation of deleterious mutations with sex-specific effects due to their maternal inheritance, and found few effects on nuclear gene expression in females but major effects in males, predominantly in male-specific tissues. Finally, we used published data to compare intraspecific and interspecific genetic variation for a set of transcripts, to test whether speciation occurs along lines of maximum genetic variance.

In conclusion, gene expression techniques can generate useful results in the study of sexual conflict, particularly in association with phenotypic data or when integrated with published datasets.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2011. 46 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 843
Keyword
Sexual conflict, sexual selection, male-female coevolution, gene expression, transcriptome, microarrays, sexual dimorphism, Drosophila
National Category
Biological Sciences
Research subject
Biology with specialization in Animal Ecology; Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-156567 (URN)978-91-554-8130-8 (ISBN)
Public defence
2011-10-01, Zootissalen, EBC, Villavägen 9, Uppsala, 09:30 (English)
Opponent
Supervisors
Available from: 2011-09-08 Created: 2011-08-03 Last updated: 2011-11-03

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