Adaptive cellular evolution in the intestine of hyperdiverse cichlid fishes

  • 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).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zwick, R. K. et al. Epithelial zonation along the mouse and human small intestine defines five discrete metabolic domains. Nat. Cell Biol. 26, 250–262 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Park, J. et al. Lysosome-rich enterocytes mediate protein absorption in the vertebrate gut. Dev. Cell 51, 7–20 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Harper, J., Mould, A., Andrews, R. M., Bikoff, E. K. & Robertson, E. J. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc. Natl Acad. Sci. USA 108, 10585–10590 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lickwar, C. R. et al. Genomic dissection of conserved transcriptional regulation in intestinal epithelial cells. PLoS Biol. 15, e2002054 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chu, T., Wang, Z., Pe’er, D. & Danko, C. G. Cell type and gene expression deconvolution with BayesPrism enables Bayesian integrative analysis across bulk and single-cell RNA sequencing in oncology. Nat. Cancer 3, 505–517 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hopperdietzel, C. et al. Gross morphology and histology of the alimentary tract of the convict cichlid Amatitlania nigrofasciata. J. Fish Biol. 85, 1707–1725 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • El Taher, A. et al. Gene expression dynamics during rapid organismal diversification in African cichlid fishes. Nat. Ecol. Evol. 5, 243–250 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Berthelot, C., Villar, D., Horvath, J. E., Odom, D. T. & Flicek, P. Complexity and conservation of regulatory landscapes underlie evolutionary resilience of mammalian gene expression. Nat. Ecol. Evol. 2, 152–163 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Hansen, T. F. Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341–1351 (1997).

    Article 
    PubMed 

    Google Scholar
     

  • Chen, J. et al. A quantitative framework for characterizing the evolutionary history of mammalian gene expression. Genome Res. 29, 53–63 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bedford, T. & Hartl, D. L. Optimization of gene expression by natural selection. Proc. Natl Acad. Sci. USA 106, 1133–1138 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hill, M. S., Vande Zande, P. & Wittkopp, P. J. Molecular and evolutionary processes generating variation in gene expression. Nat. Rev. Genet. 22, 203–215 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fay, J. C. & Wittkopp, P. J. Evaluating the role of natural selection in the evolution of gene regulation. Heredity 100, 191–199 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Skinnider, M. A. et al. Cell type prioritization in single-cell data. Nat. Biotechnol. 39, 30–34 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Domazet-Lošo, T. & Tautz, D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468, 815–818 (2010).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Murat, F. et al. The molecular evolution of spermatogenesis across mammals. Nature 613, 308–316 (2023).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun, Y. et al. Evolutionarily conserved transcriptional co-expression guiding embryonic stem cell differentiation. PLoS ONE 3, e3406 (2008).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fischer, M., Schade, A. E., Branigan, T. B., Müller, G. A. & DeCaprio, J. A. Coordinating gene expression during the cell cycle. Trends Biochem. Sci. 47, 1009–1022 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rombout, J. H. W. M., Abelli, L., Picchietti, S., Scapigliati, G. & Kiron, V. Teleost intestinal immunology. Fish Shellfish Immunol. 31, 616–626 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Szklarczyk, D. et al. The STRING database in 2023: protein–protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res. 51, D638–D646 (2022).

    Article 

    Google Scholar
     

  • Roux, J. & Robinson-Rechavi, M. Developmental constraints on vertebrate genome evolution. PLoS Genet. 4, e1000311 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Johnson, Z. V. et al. Cellular profiling of a recently-evolved social behavior in cichlid fishes. Nat. Commun. 14, 4891 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hunnicutt, K. E., Good, J. M. & Larson, E. L. Unraveling patterns of disrupted gene expression across a complex tissue. Evolution 76, 275–291 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Duque-Correa, M. J. et al. Diet and habitat as determinants of intestine length in fishes. Rev. Fish Biol. Fish. 34, 1017–1034 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clavel, J., Escarguel, G. & Merceron, G. Mvmorph: an R package for fitting multivariate evolutionary models to morphometric data. Methods Ecol. Evol. 6, 1311–1319 (2015).

    Article 

    Google Scholar
     

  • Feregrino, C. & Tschopp, P. Assessing evolutionary and developmental transcriptome dynamics in homologous cell types. Dev. Dyn. 251, 1472–1489 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Papakostas, S. et al. Gene pleiotropy constrains gene expression changes in fish adapted to different thermal conditions. Nat. Commun. 5, 4071 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, P. et al. Phylogenomics of trophically diverse cichlids disentangles processes driving adaptive radiation and repeated trophic transitions. Ecol. Evol. 12, e9077 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clara, R. et al. Metabolic adaptation of the small intestine to short- and medium-term high-fat diet exposure. J. Cell. Physiol. 232, 167–175 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Enriquez, J. R. et al. A dietary change to a high-fat diet initiates a rapid adaptation of the intestine. Cell Rep. 41, 111641 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sullivan, Z. A. et al. γδ T cells regulate the intestinal response to nutrient sensing. Science 371, eaba8310 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crosnier, C. et al. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132, 1093–1104 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tóth, B., Ben-Moshe, S., Gavish, A., Barkai, N. & Itzkovitz, S. Early commitment and robust differentiation in colonic crypts. Mol. Syst. Biol. 13, 902 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carroll, S. B. Evolution at two levels: on genes and form. PLoS Biol. 3, e245 (2005).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, J. Patterns and evolutionary consequences of pleiotropy. Annu. Rev. Ecol. Evol. Syst. 54, 1–19 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wagner, C. E., McIntyre, P. B., Buels, K. S., Gilbert, D. M. & Michel, E. Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct. Ecol. 23, 1122–1131 (2009).

    Article 

    Google Scholar
     

  • Conte, M. A., Gammerdinger, W. J., Bartie, K. L., Penman, D. J. & Kocher, T. D. A high quality assembly of the Nile Tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genomics 18, 341 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Young, M. D. & Behjati, S. SoupX removes ambient RNA contamination from droplet-based single-cell RNA sequencing data. Gigascience 9, giaa151 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Subramanian, A., Alperovich, M., Yang, Y. & Li, B. Biology-inspired data-driven quality control for scientific discovery in single-cell transcriptomics. Genome Biol. 23, 267 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, C. et al. SciBet as a portable and fast single cell type identifier. Nat. Commun. 11, 1818 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crow, M., Paul, A., Ballouz, S., Huang, Z. J. & Gillis, J. Characterizing the replicability of cell types defined by single cell RNA-sequencing data using MetaNeighbor. Nat. Commun. 9, 884 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Larsson, E. et al. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut 61, 1124–1131 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, Z. et al. Morphological and molecular evidence for functional organization along the rostrocaudal axis of the adult zebrafish intestine. BMC Genomics 11, 392 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Childers, L. et al. Protein absorption in the zebrafish gut is regulated by interactions between lysosome rich enterocytes and the microbiome. eLife 13, RP100611 (2025).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Putri, G. H., Anders, S., Pyl, P. T., Pimanda, J. E. & Zanini, F. Analysing high-throughput sequencing data in Python with HTSeq 2.0. Bioinformatics 38, 2943–2945 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gene Ontology Consortium et al. The Gene Ontology knowledgebase in 2023. Genetics 224, iyad031 (2023).

    Article 

    Google Scholar
     

  • Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McGlinn, E. & Mansfield, J. H. Detection of gene expression in mouse embryos and tissue sections. Methods Mol. Biol. 770, 259–292 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Grall, E. et al. Self-organized BMP signaling dynamics underlie the development and evolution of digit segmentation patterns in birds and mammals. Proc. Natl Acad. Sci. USA 121, e2304470121 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tosches, M. A. et al. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360, 881–888 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Ullrich, K. K. & Glytnasi, N. E. oggmap: a Python package to extract gene ages per orthogroup and link them with single-cell RNA data. Bioinformatics 39, btad657 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rajkov, J., El Taher, A., Böhne, A., Salzburger, W. & Egger, B. Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish. Mol. Ecol. 30, 274–296 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ricci, V., Ronco, F., Boileau, N. & Salzburger, W. Visual opsin gene expression evolution in the adaptive radiation of cichlid fishes of Lake Tanganyika. Sci. Adv. 9, eadg6568 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brawand, D. et al. The evolution of gene expression levels in mammalian organs. Nature 478, 343–348 (2011).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Xu, C. et al. Histological and transcriptomic responses of two immune organs, the spleen and head kidney, in Nile tilapia (Oreochromis niloticus) to long-term hypersaline stress. Fish Shellfish Immunol. 76, 48–57 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xia, J. H., Li, H. L., Li, B. J., Gu, X. H. & Lin, H. R. Acute hypoxia stress induced abundant differential expression genes and alternative splicing events in heart of tilapia. Gene 639, 52–61 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ellison, A. R. et al. Transcriptomic response to parasite infection in Nile tilapia (Oreochromis niloticus) depends on rearing density. BMC Genomics 19, 723 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lemos, B., Meiklejohn, C. D. & Hartl, D. L. Regulatory evolution across the protein interaction network. Nat. Genet. 36, 1059–1060 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • He, X. & Zhang, J. Toward a molecular understanding of pleiotropy. Genetics 173, 1885–1891 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bozhilova, L. V., Whitmore, A. V., Wray, J., Reinert, G. & Deane, C. M. Measuring rank robustness in scored protein interaction networks. BMC Bioinformatics 20, 446 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703 (2002).

    Article 

    Google Scholar
     

  • Zihler, F. Gross morphology and configuration of digestive tracts of Cichlidae (teleostei, Perciformes): phylogenetic and functional, significance. Neth. J. Zool. 32, 544–571 (1981).

    Article 

    Google Scholar
     

  • Keppeler, F. W., Montaña, C. G. & Winemiller, K. O. The relationship between trophic level and body size in fishes depends on functional traits. Ecol. Monogr. 90, e01415 (2020).

    Article 

    Google Scholar
     

  • Ghilardi, M. et al. Phylogeny, body morphology, and trophic level shape intestinal traits in coral reef fishes. Ecol. Evol. 11, 13218–13231 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Phipson, B. et al. propeller: testing for differences in cell type proportions in single cell data. Bioinformatics 38, 4720–4726 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liao, W. B., Jiang, Y., Jin, L. & Lüpold, S. How hibernation in frogs drives brain and reproductive evolution in opposite directions. eLife 12, RP88236 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aitchison, J. The statistical analysis of compositional data. J. R. Stat. Soc. Series B 44, 139–160 (1982).

    Article 

    Google Scholar
     

  • Van Den Boogaart, K. G., Tolosana-Delgado, R. & Bren, M. compositions: compositional data analysis. R package version 2.0–9 (2025).

  • Orme, D. The caper package: comparative analysis of phylogenetics and evolution in R. GitHub https://github.com/davirdorme/caper (2013).

  • Clavel, J., Aristide, L. & Morlon, H. A penalized likelihood framework for high-dimensional phylogenetic comparative methods and an application to New-World monkeys brain evolution. Syst. Biol. 68, 93–116 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Clavel, J. & Morlon, H. Reliable phylogenetic regressions for multivariate comparative data: illustration with the MANOVA and application to the effect of diet on mandible morphology in Phyllostomid bats. Syst. Biol. 69, 927–943 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Baken, E. K., Collyer, M. L., Kaliontzopoulou, A. & Adams, D. C. geomorph v4.0 and gmShiny: enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Methods Ecol. Evol. 12, 2355–2363 (2021).

    Article 

    Google Scholar
     

  • Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Burnham, K. & Anderson, D. R. Model Selection and Multi-Model Inference (Springer, 2002).

  • Revell, L. J. phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things). PeerJ 12, e16505 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Venditti, C., Meade, A. & Pagel, M. Multiple routes to mammalian diversity. Nature 479, 393–396 (2011).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).


    Google Scholar
     

  • Cooney, C. R. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344–347 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Engel, J. et al. Regularized MANOVA (rMANOVA) in untargeted metabolomics. Anal. Chim. Acta 899, 1–12 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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