Adaptive cellular evolution in the intestine of hyperdiverse cichlid fishes | Nature
Subjects
- Evolutionary genetics
- Molecular evolution
Abstract
The ability of animals to efficiently track down and digest food is crucial for their survival, and the specialization to different diets is a major driver of diversification in this group1,2,3. Although the evolution of feeding structures has been studied extensively in this context4,5,6, the nature and extent of adaptations in the digestive tract remain poorly understood. Here, we examine dietary adaptations in the intestines of one of the largest adaptive radiations in vertebrates, the cichlid fishes of Lake Tanganyika. By generating comprehensive single-cell transcriptomic data for 24 Tanganyikan cichlid species with divergent feeding habits, and integrating this with eco-morphological and genomic information, we uncover that, at the cellular level, dietary adaptations primarily involve anterior enterocytes. In particular, we show that the relative abundances of anterior enterocytes as well as the gene expression profiles in this cell population evolved in response to rapid trophic specializations, and that these diet-related adaptations are driven by fast-evolving, cell-population-specific genes. Overall, our findings show that alterations in intestinal epithelium cell composition and in the cell-type-specific molecular makeup provided the substrate for trophic specializations, demonstrating that ecological adaptations target multiple layers of biological organization.
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Fig. 1: Characterization of the intestines of cichlid fishes at single-cell resolution.The alternative text for this image may have been generated using AI.
Fig. 2: Cell-population-specific trajectories of transcriptome evolution in the cichlids’ intestines.The alternative text for this image may have been generated using AI.
Fig. 3: Associations between trophic specialization and epithelial cell population proportions.The alternative text for this image may have been generated using AI.
Fig. 4: Gene expression evolution of diet-related genes in anterior enterocytes.The alternative text for this image may have been generated using AI.
Data availability
All single-cell and bulk RNA-seq raw and processed data generated in this study have been deposited at GEO (https://www.ncbi.nlm.hiv.gov/geo/) under accession numbers GSE280410 and GSE280411. Protein–protein interactions were retrieved from the STRING v.11 database (https://string-db.org/).
Code availability
All original code is available from GitHub at https://github.com/AntoineFages/scRNA_paper.
References
- Darwin, C. On the Origin of Species (Cambridge Univ. Press, 1859).
- Simpson, G. G. The Major Features of Evolution (Columbia Univ. Press, 1953).
- Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233 (1988).
Article
Google Scholar
- Fryer, G. & Iles, T. D. The Cichlid Fishes of the Great Lakes of Africa (T.F.H. Publications, 1972).
- Ronco, F. et al. Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589, 76–81 (2021).
Article
ADS
CAS
PubMed
Google Scholar
- Grant, P. R. Ecology and Evolution of Darwin’s Finches (Princeton Univ. Press, 1986).
- Starck, J. M. & Wang, T. Physiological and Ecological Adaptations to Feeding in Vertebrates (Science Publishers, 2005).
- Pough, F. H., Janis, C. M. & Heiser, J. B. Vertebrate Life (Pearson Education, 2013).
- Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000).
- Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).
Article
ADS
CAS
PubMed
Google Scholar
- Hung, R.-J. et al. A cell atlas of the adult Drosophila midgut. Proc. Natl Acad. Sci. USA 117, 1514–1523 (2020).
Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
- Haber, A. L. et al. A single-cell survey of the small intestinal epithelium. Nature 551, 333–339 (2017).
Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
- Ronco, F., Büscher, H. H., Indermaur, A. & Salzburger, W. The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. J. Great Lakes Res. 46, 1067–1078 (2020).
Article
PubMed
PubMed Central
Google Scholar
- Muschick, M., Indermaur, A. & Salzburger, W. Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22, 2362–2368 (2012).