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Gene expression dynamics during rapid organismal diversification in African cichlid fishes

Nature Ecology & Evolution volume 5, pages 243–250 (2021)Cite this article

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Abstract

Changes in gene expression play a fundamental role in phenotypic evolution. Transcriptome evolutionary dynamics have so far mainly been compared among distantly related species and remain largely unexplored during rapid organismal diversification, in which gene regulatory changes have been suggested as particularly effective drivers of phenotypic divergence. Here we studied gene expression evolution in a model system of adaptive radiation, the cichlid fishes of African Lake Tanganyika. By comparing gene expression profiles of 6 different organs in 74 cichlid species representing all subclades of this radiation, we demonstrate that the rate of gene expression evolution varies among organs, transcriptome parts and the subclades of the radiation, indicating different strengths of selection. We found that the noncoding part of the transcriptome evolved more rapidly than the coding part, and that the gonadal transcriptomes evolved more rapidly than the somatic ones, with the exception of liver. We further show that the rate of gene expression change was not constant over the course of the radiation but accelerated at its later phase. Finally, we show that—at the per-gene level—the evolution of expression patterns is dominated by stabilizing selection.

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Fig. 1: Gene expression patterns across the adaptive radiation of cichlid fishes in African Lake Tanganyika.
Fig. 2: PCA of overall gene expression levels per organ.
Fig. 3: Gene expression similarities among species and transcriptome parts.
Fig. 4: Rate of gene expression evolution across organs for protein-coding genes and lncRNAs.
Fig. 5: Organ-specific expression and expression dynamics of protein-coding genes and lncRNAs.

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Data availability

The datasets generated during and/or analysed during the current study are available in the NCBI repository under the BioProject accession number PRJNA550295. All related metadata are available on Dryad under the project accession number fj6q573sj.

Code availability

All custom codes generated during and/or analysed in the current study are available on Dryad under the project accession number fj6q573sj.

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Acknowledgements

We thank the University of Burundi, the Ministère de l’Eau, de l’Environnement, de l’Aménagement du Territoire et de l’Urbanisme, Republic of Burundi, the Tanzania Commission for Science and Technology, the Tanzania Fisheries Research Institute, the Tanzania National Parks Authority, the Tanzania Wildlife Research Institute and the Lake Tanganyika Research Unit, Department of Fisheries, Republic of Zambia, for research permits; G. Banyankimbona (University of Burundi), I. Kimirei (TAFIRI, Kigoma, Tanzania) and T. Banda and L. Makasa (Department of Fisheries, Mpulungu, Zambia) for assistance with research permits; the boat crews of the Chomba (D. Mwanakulya, J. Sichilima and H. D. Sichilima Jr) and the Maji Makubwa II (G. Kazumbe and family) for help during field work; V. Huwiler (Kalambo Lodge, Zambia), ‘Charity’ (Nkupi Lodge, Zambia) and the Zytkow family (Ndole Bay Lodge, Zambia) for lodging; C. Zytkow (Conservation Lake Tanganyika, Zambia), and P. Lassen and V. Huwiler (Kalambo Lodge, Zambia) for logistic support; C. Beisel and E. Burcklen at the Genomics Facility Basel for library preparation and sequencing; and J. Himes for fish illustrations. We also thank A. Necsulea for discussions and advice on the project. Calculations were performed at sciCORE (http://scicore.unibas.ch/) scientific computing centre at University of Basel (with support by the SIB/Swiss Institute of Bioinformatics). This work was funded by the European Research Council (Consolidator Grant no. 617585 ‘CICHLID~X’) and the Swiss National Science Foundation to W.S.

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  1. Astrid Böhne

    Present address: Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Bonn, Germany

Authors and Affiliations

  1. Zoological Institute, Department of Environmental Sciences, University of Basel, Basel, Switzerland

    Athimed El Taher, Astrid Böhne, Nicolas Boileau, Fabrizia Ronco, Adrian Indermaur, Lukas Widmer & Walter Salzburger

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Contributions

A.E.T., F.R., A.I., N.B., L.W. and W.S. collected and/or dissected the specimens in the field. A.E.T. and N.B. organized the RNA-sequencing data production. A.E.T. processed and mapped the reads. A.E.T. performed all data analyses except for the temporal dynamics of transcriptome evolution that F.R. performed. A.B. contributed ideas and supervised data analyses. F.R. formatted the final figures. A.E.T. and W.S. wrote the manuscript with input from all authors. The project was originally designed by W.S., with input from A.E.T., F.R., A.B. and A.I.

Corresponding authors

Correspondence to Athimed El Taher or Walter Salzburger.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Emily Wong, Marie Sémon and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Gene expression patterns per organ and sex.

Principal component analyses of overall gene expression levels in brain, gill, lower pharyngeal jaw bone (LPJ), ovary, testis, and liver. Samples (brain: n = 428; gill: n = 434; LPJ: n = 425; ovary: n = 219; testis: n = 213; liver: n = 412) are coloured according to sex (red: female, blue: male). The proportion of variance explained by the first two principal components (PC1 and PC2) for each organ are indicated in parenthesis at x and y axes, respectively.

Extended Data Fig. 2 Expression variation through time within organs and transcriptome parts.

a, Pairwise Spearman’s rank correlation coefficient (ρ) of per species (brain, ovary, gill and testis: n = 74 taxa; LPJ and liver: n = 73 taxa) as a function of divergence time17 for protein-coding genes (left panel) and lncRNAs (right panel) in brain, gill, LPJ, ovary, testis, and liver. Samples are colour-coded according to tribe as defined in Fig. 1a; pairs of species belonging to two different tribes are indicated in grey. The regression line is represented with a dashed black line. b, Comparison of rate of expression change (measured as [1 – ρ] / divergence time17) between protein-coding genes (p-c) and lncRNAs (lnc) (two-sided t-test: ***P < 10-16). The box plot centre lines represent the median, box limits the upper and lower quartiles, and whiskers the 1.5x interquartile range. Outliers are not shown.

Extended Data Fig. 3 Protein-coding expression trajectories.

Neighbour-joining trees based on pairwise distance matrices of gene expression between pairs of species (n = 73 taxa) for protein-coding genes for brain, gill, LPJ, ovary, testis, and liver. All branches are coloured according to tribe as defined in Fig. 1a (see Extended Data Fig. 9 and Supplementary Table 2 for full species names).

Extended Data Fig. 4 lncRNAs expression trajectories.

Neighbour-joining trees based on pairwise distance matrices of gene expression between pairs of species (n = 73 taxa) for lncRNAs for brain, gill, LPJ, ovary, testis, and liver. All branches are colour-coded according to tribe as defined in Fig. 1a (see Extended Data Fig. 9 and Supplementary Table 2 for full species names).

Extended Data Fig. 5 Rate of protein-coding gene expression evolution along the species tree.

Species tree with branch lengths estimated along the fixed species tree topology35 (n = 73 taxa) based on pairwise correlations of gene expression of protein-coding genes in brain, gill, LPJ, ovary, testis, and liver. All branches are colour-coded according to tribe as defined in Fig. 1a (see Extended Data Fig. 9 and Supplementary Table 2 for full species names).

Extended Data Fig. 6 Rate of lncRNA gene expression evolution along the species tree.

Species tree with branch lengths estimated along the fixed species tree topology35 (n = 73 taxa) based on pairwise correlations of gene expression of lncRNAs in brain, gill, LPJ, ovary, testis, and liver. All branches are colour-coded according to tribe as defined in Fig. 1a (see Extended Data Fig. 9 and Supplementary Table 2 for full species names).

Extended Data Fig. 7 Rate of transcriptome evolution within organs for protein-coding genes (left panel) and lncRNAs (right panel).

Linear regression of the expression tree branch length (calculated along the fixed species tree (n = 73 taxa) topology, Extended Data Fig. 3c, d) as a function of species tree branch lengths (Fig. 1a) for brain, gill, LPJ, ovary, testis, and liver. Data points representing branches within tribes are colour-coded corresponding to the tribe as defined in Fig. 1a, and data points representing branches that link species from different tribes are coloured in grey. Dashed lines represent linear model fits. Next to each plot, a time-calibrated species tree is shown, with branches coloured according to the rate of transcriptome evolution (measured as expression tree branch length divided by species tree branch length).

Extended Data Fig. 8 Level of expression variation within organs.

a, Cumulative branch lengths (from root to tip of expression tree branch length calculated along the fixed species tree (n = 73 taxa) topology; Extended Data Fig. 3c, d) for protein-coding genes (left panel) and lncRNAs (right panel) in brain, gill, LPJ, ovary, testis, and liver calculated per species and summarised per tribe (n = 12 tribes). Boxplots are colour-coded according to tribe as defined in Fig. 1a; boxplot centre lines represent the median, box limits the upper and lower quartiles, and whiskers the 1.5x interquartile range. Differences among the tribes were assessed using an ANOVA (see Supplementary Table 5 for the P-values for all pairwise comparisons). b, Comparison of cumulative branch lengths between protein-coding genes (p-c) and lncRNAs (lnc) (two-sided t-test: ***P < 10-8). Boxplot centre lines represent the median, box limits the upper and lower quartiles, and whiskers the 1.5x interquartile range.

Extended Data Fig. 9 Species information.

List of species used in this experiment with abbreviation code, full species name and tribe information.

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El Taher, A., Böhne, A., Boileau, N. et al. Gene expression dynamics during rapid organismal diversification in African cichlid fishes. Nat Ecol Evol 5, 243–250 (2021). https://doi.org/10.1038/s41559-020-01354-3

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