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Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes

View ORCID ProfileMadeleine Carruthers, View ORCID ProfileDuncan E. Edgley, View ORCID ProfileAndrew D. Saxon, Nestory P. Gabagambi, View ORCID ProfileAsilatu Shechonge, View ORCID ProfileEric A. Miska, View ORCID ProfileRichard Durbin, Jon R. Bridle, View ORCID ProfileGeorge F. Turner, View ORCID ProfileMartin J. Genner
doi: https://doi.org/10.1101/2022.01.07.475335
Madeleine Carruthers
1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK
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  • For correspondence: ph19872@bristol.ac.uk
Duncan E. Edgley
1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK
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Andrew D. Saxon
1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK
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Nestory P. Gabagambi
2Tanzanian Fisheries Research Institute, Kyela Research Centre, P.O. Box 98, Kyela, Mbeya, Tanzania
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Asilatu Shechonge
3Tanzanian Fisheries Research Institute, Dar es Salaam Research Centre, P.O. Box 9750, Dar es Salaam, Tanzania
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Eric A. Miska
4Wellcome/CRUK Gurdon Institute, University of Cambridge, Cambridge, CB2 1QN, UK
5Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK
6Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
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Richard Durbin
5Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK
6Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
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Jon R. Bridle
1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK
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George F. Turner
7School of Natural Sciences, Bangor University, Bangor, Wales, LL57 2UW, UK
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Martin J. Genner
1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK
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  • ORCID record for Martin J. Genner
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Abstract

Rapid ecological speciation along depth gradients has taken place independently and repeatedly in freshwater fishes. While the extent of genomic divergence between ecomorphs is often well understood, the molecular mechanisms facilitating such rapid diversification are typically unclear. In Lake Masoko, an East African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data from jaw tissue, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants and examine their contribution to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 4.2% were regulated by cis-regulatory expression QTLs, and 6.4% were regulated by cis-regulatory splicing QTLs. There were also strong signals of divergent selection of differentially expressed genes that showed divergent regulation from expression, splicing or both QTL variants, including genes associated with major jaw plasticity and adaptation networks, adaptive immune system response, and oxidoreductase processes. These results suggest that transcriptome plasticity and modification have important roles during early-stage ecological speciation and demonstrate the role of regulatory-variants as important targets of selection driving ecologically-relevant divergence in gene expression that is associated with adaptive diversification.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 08, 2022.
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Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes
Madeleine Carruthers, Duncan E. Edgley, Andrew D. Saxon, Nestory P. Gabagambi, Asilatu Shechonge, Eric A. Miska, Richard Durbin, Jon R. Bridle, George F. Turner, Martin J. Genner
bioRxiv 2022.01.07.475335; doi: https://doi.org/10.1101/2022.01.07.475335
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Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes
Madeleine Carruthers, Duncan E. Edgley, Andrew D. Saxon, Nestory P. Gabagambi, Asilatu Shechonge, Eric A. Miska, Richard Durbin, Jon R. Bridle, George F. Turner, Martin J. Genner
bioRxiv 2022.01.07.475335; doi: https://doi.org/10.1101/2022.01.07.475335

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