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The evolution of fast-growing coral reef fishes

Nature volume 618, pages 322–327 (2023)Cite this article

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Abstract

Individual growth is a fundamental life history trait1,2,3,4, yet its macroevolutionary trajectories have rarely been investigated for entire animal assemblages. Here we analyse the evolution of growth in a highly diverse vertebrate assemblage—coral reef fishes. We combine state-of-the-art extreme gradient boosted regression trees with phylogenetic comparative methods to detect the timing, number, location and magnitude of shifts in the adaptive regime of somatic growth. We also explored the evolution of the allometric relationship between body size and growth. Our results show that the evolution of fast growth trajectories in reef fishes has been considerably more common than the evolution of slow growth trajectories. Many reef fish lineages shifted towards faster growth and smaller body size evolutionary optima in the Eocene (56–33.9 million years ago), pointing to a major expansion of life history strategies in this Epoch. Of all lineages examined, the small-bodied, high-turnover cryptobenthic fishes shifted most towards extremely high growth optima, even after accounting for body size allometry. These results suggest that the high global temperatures of the Eocene5 and subsequent habitat reconfigurations6 might have been critical for the rise and retention of the highly productive, high-turnover fish faunas that characterize modern coral reef ecosystems.

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Fig. 1: Phylogenetic reconstruction of reef fish growth.
Fig. 2: The location and magnitude of growth regime shifts in the reef fish phylogeny.
Fig. 3: Evolutionary regime shifts in the allometry between growth and maximum body length in reef fishes.

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Data availability

The datasets generated and/or analysed as part of this study are available at Zenodo (https://doi.org/10.5281/zenodo.7797270)67. There are no restrictions on data availability. The phylogeny used in the main analyses was downloaded from The Fish Tree of Life (https://fishtreeoflife.org). Publicly available datasets used in the study include: FishBase (http://www.fishbase.org) and the data repository of ref. 26 (https://doi.org/10.4225/28/5ae8f3cc790f9). Source data are provided with this paper.

Code availability

The R (v.4.1.0) packages used were as follows: tidyverse, ggplot2, ape, phytools, geiger, ggtree, cowplot, viridis, raster, parallel, XGBoost, Matrix, pdp, data.table, png, grid, phangorn, bayou, mvMORPH, PCMBase, PCMBaseCpp and PCMFit. Package versions are provided in the Reporting Summary. The codes used during this study are available at Zenodo (https://doi.org/10.5281/zenodo.7797270)67.

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Acknowledgements

We thank J. Uyeda and V. Mitov for assistance with their R packages. Funding was provided by the Australian Research Council (D.R.B., LF190100062), with a Postdoctoral Fellowship to A.C.S. and a PhD Scholarship to H.F.Y. Funding for H.F.Y. was also provided by a Natural Sciences and Engineering Research Council of Canada Postgraduate Doctoral Scholarship. R.A.M. is supported by a Branco Weiss Fellowship Society in Science and a PSL Junior Fellowship.

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Author notes

  1. These authors contributed equally: Alexandre C. Siqueira, Helen F. Yan

Authors and Affiliations

  1. Research Hub for Coral Reef Ecosystem Functions, College of Science and Engineering, James Cook University, Townsville, Queensland, Australia

    Alexandre C. Siqueira, Helen F. Yan, Renato A. Morais & David R. Bellwood

  2. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

    Alexandre C. Siqueira, Helen F. Yan, Renato A. Morais & David R. Bellwood

  3. Paris Sciences et Lettres Université, École Pratique des Hautes Études, EPHE-UPVD-CNRS, USR 3278 CRIOBE, Perpignan, France

    Renato A. Morais

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Contributions

A.C.S., H.F.Y., R.A.M. and D.R.B. conceived the study. A.C.S., H.F.Y. and R.A.M. collected the data. A.C.S. and H.F.Y. performed the analyses and wrote the first draft of the manuscript. R.A.M. and D.R.B. contributed substantially to revisions.

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Correspondence to Alexandre C. Siqueira.

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Extended data figures and tables

Extended Data Fig. 1 Phylogenetic reconstruction of reef fish growth.

Standardized growth coefficient (Kmax) reconstructed through time across the phylogenetic tree of coral reef-associated fishes. The points represent estimated shifts in the evolutionary regime of growth detected through multi-optima Ornstein–Uhlenbeck models, using 50% as the threshold for posterior probabilities. Light-yellow points represent shifts toward higher values of evolutionary optima (i.e. faster growth rates), while dark-blue points represent the opposite. Please note that the y-axis is on a log10 scale. The inset depicts the number of positive shifts divided by the total branch length in the phylogeny per geological epoch (y-axis) through time (x-axis). This metric gives an indication of the probability of shifts controlled by the availability of locations for them to occur, which is biased towards very old shifts. We note that the higher number of shifts/branch length detected for the Jurassic is a product of this bias and should be interpreted with caution given that it is the result of only one shift in that Period. The red line represents the Cretaceous-Paleogene (K/Pg) boundary. Pi: Pliocene; Pe: Pleistocene.

Source data

Extended Data Fig. 2 Proportional change in reef fish Kmax evolutionary optima through time.

Light-yellow points represent shifts toward higher values of evolutionary optima (i.e. faster growth rates), while the dark-blue point represents the opposite. The size of points is scaled according to their posterior probability in Ornstein–Uhlenbeck models.

Source data

Extended Data Fig. 3 Phylogenetic reconstruction of reef fish growth.

Standardized growth coefficient (Kmax) reconstructed through time across the phylogenetic tree of coral reef-associated fishes, recalibrated based on Ghezelayagh et al. 32 (see Methods). The points represent estimated shifts in the evolutionary regime of growth detected through multi-optima Ornstein–Uhlenbeck models. Light-yellow points represent shifts toward higher values of evolutionary optima (i.e. faster growth rates), while dark-blue points represent the opposite. Please note that the y-axis is on a log10 scale. The inset depicts the number of positive shifts divided by the total branch length in the phylogeny per geological epoch (y-axis) through time (x-axis). This metric gives an indication of the probability of shifts controlled by the availability of locations for them to occur. The red line represents the Cretaceous-Paleogene (K/Pg) boundary. Pi: Pliocene; Pe: Pleistocene.

Source data

Extended Data Fig. 4 Phylogenetic reconstruction of reef fish body size.

Maximum body length reconstructed through time across the phylogenetic tree of coral reef-associated fishes. The points represent estimated shifts in the evolutionary regime of body size detected through multi-optima Ornstein–Uhlenbeck models. Light-yellow points represent shifts toward higher values of evolutionary optima (i.e. larger body sizes), while dark-blue points represent the opposite. Please note that the y-axis is on a log10 scale. The inset depicts the number of negative shifts (i.e. towards smaller body sizes) divided by the total branch length in the phylogeny per geological epoch (y-axis) through time (x-axis). This metric gives an indication of the probability of shifts controlled by the availability of locations for them to occur. The red line represents the Cretaceous-Paleogene (K/Pg) boundary. Pi: Pliocene; Pe: Pleistocene.

Source data

Extended Data Fig. 5 Evolutionary regimes in the allometry growth/body size in reef fishes.

Reef fish phylogeny at the genus level with depicted evolutionary regimes for the allometric relationship between the growth coefficient (Kmax) and maximum body length. The different colours across the branches represent the clades with different evolutionary regimes detected by the mixed Gaussian phylogenetic model (see Methods). The coefficients estimated for each regime are shown in Fig. 3, with the respective colours. External arcs show the extant families represented by each clade, along with respective allometric evolutionary regime.

Source data

Extended Data Fig. 6 Empirical Kmax values for reef vs. non-reef fish species.

Density plots illustrating the distribution of empirical Kmax values for coral reef-associated species considered in this study (orange) and non-reef-associated species (blue). Details on data collection for non-reef-associated species can be found in the supplementary material. The thick lines indicate the median Kmax values for each group. Please note that the x-axis is on a log10 scale.

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Siqueira, A.C., Yan, H.F., Morais, R.A. et al. The evolution of fast-growing coral reef fishes. Nature 618, 322–327 (2023). https://doi.org/10.1038/s41586-023-06070-z

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