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Differential gene expression in semispecies and hybrids of Drosophila paulistorum
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Department of epidemiology of microbial diseases, Yale University.
Department of cell and developmental biology, Medical university of Vienna.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.ORCID iD: 0000-0002-5874-7153
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Gene expression divergence is correlated with and can be either a cause or a consequence of species divergence. Studying gene expression differences between closely related species, and their hybrid offspring, can thus give us clues about genes and mechanisms associated with reproductive isolation (RI) between them and allow us to better understand early stages of speciation. In this study, we use RNA-Seq to investigate gene expression divergence between the Amazonian, Centro-American and Orinocan semispecies of Drosophila paulistorum, a species cluster in statu nascendi, and between inter-semispecies hybrids and their parents. We uncover a large number of genes with varying expression between semispecies, with the highest numbers in male abdomens. The differentially expressed genes are associated with a range of biological functions, but especially with broad, regulatory functions, that are governed by transcription, translation, post-translational modifications and induced by signal transduction. We found that the expression pattern of hybrids was much more similar to the maternal line and that very few genes have a different expression than both of their parents. When comparing the differentially expressed genes in semispecies and hybrids to gene affected by Wolbachia in D. paulistorum, we see a small overlap. However, especially in hybrids, some of the overlapping genes appear to be highly relevant. Our study provides insights about expression differences associated with RI in D. paulistorum, and the impact of Wolbachia on the divergence of semispecies and hybrid sterility.

National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-406757OAI: oai:DiVA.org:uu-406757DiVA, id: diva2:1414022
Available from: 2020-03-11 Created: 2020-03-11 Last updated: 2020-03-12
In thesis
1. Genomic and transcriptomic investigation of reproductive incompatibility in Drosophila
Open this publication in new window or tab >>Genomic and transcriptomic investigation of reproductive incompatibility in Drosophila
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Both nuclear and cytoplasmic elements can contribute to the emergence of reproductive incompatibilities that influence evolution and speciation. In the projects that compose this thesis, we use genomics and transcriptomics to study some of those elements in Drosophila.

In the first study, we show that Wolbachia, an endosymbiotic bacterium known to cause reproductive alterations in its hosts, influences gene expression in D. paulistorum. Affected genes were associated with biological functions such as metabolism, immunity, reproduction, and chemical communication. Our results indicate that Wolbachia accentuates the differences in expression profiles between semispecies and suggest that the symbiont influences host pre-and postmating isolation.

In the second paper, we uncover widespread persistent heteroplasmy in D. paulistorum. We reveal that D. paulistorum mitochondria are polyphyletic, with two divergent mitotypes, and that the heteroplasmy likely originated through introgression. One of the mitotypes shows biparental inheritance, non-responsiveness to host energy demands and rapid titer increase in the early embryo. We hypothesize that such selfish traits evolved in response to competition between mitotypes.

In the third project, we show that differentially expressed genes between D. paulistorum semispecies are associated with a variety of biological processes, especially broad regulatory functions that occur via variability in transcription, translation and ubiquitination of post-translational modification. We reveal that the expression profile of F1 inter-semispecies hybrids is markedly similar to that of the maternal line, and that Wolbachia has a small but potentially significant interaction with genes that are differentially expressed in semispecies and F1 hybrids.

Finally, we use comparative genomics to study the evolution of closely related Wolbachia strains with known reproductive phenotypes. We confirm previous observations that Wolbachia genomes are very dynamic and that phage-associated regions are particularly variable and likely involved in horizontal transfer of genes linked to reproductive phenotypes. An in-depth screen for genetic elements potentially involved in Wolbachia-induced cytoplasmic incompatibility recovers genes previously known to be involved in the phenotype and novel candidates.

In conclusion, this thesis contributes to our understanding of genetic factors that affect Drosophila evolution, particularly those leading to reproductive incompatibility in D. paulistorum and associated with Wolbachia.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2020. p. 69
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1914
Keywords
Wolbachia, Drosophila, Drosophila paulistorum, Differential Gene Expression, Reproductive Incompatibility, Reproductive Isolation, Comparative Genomics, Transcriptomics, RNA-Seq, Heteroplasmy, Mitochondria, Genomic conflict
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-406758 (URN)978-91-513-0897-5 (ISBN)
Public defence
2020-04-24, Room A1:111a, BMC, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2020-04-02 Created: 2020-03-12 Last updated: 2020-04-02

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Baiao, Guilherme CostaKlasson, Lisa

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