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Sustained high rates of morphological evolution during the rise of tetrapods

Nature Ecology & Evolution volume 5, pages 1403–1414 (2021)Cite this article

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Abstract

The fish-to-tetrapod transition is one of the most iconic events in vertebrate evolution, yet fundamental questions regarding the dynamics of this transition remain unresolved. Here, we use advances in Bayesian morphological clock modelling to reveal the evolutionary dynamics of early tetrapodomorphs (tetrapods and their closest fish relatives). We show that combining osteological and ichnological calibration data results in major shifts on the time of origin of all major groups of tetrapodomorphs (up to 25 million years) and that low rates of net diversification, not fossilization, explain long ghost lineages in the early tetrapodomorph fossil record. Further, our findings reveal extremely low rates of morphological change for most early tetrapodomorphs, indicating widespread stabilizing selection upon their ‘fish’ morphotype. This pattern was broken only by elpistostegalians (including early tetrapods), which underwent sustained high rates of morphological evolution for ~30 Myr during the deployment of the tetrapod body plan.

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Fig. 1: Comparison of evolutionary trees and divergence times for the major groups of tetrapodomorphs using distinct tree calibration strategies.
Fig. 2: Shifts in diversification parameter estimates from the FBD process and LTT across time bins.
Fig. 3: Relative overall rates of morphological evolution in early tetrapodomorphs.
Fig. 4: Relative rates of evolution and inferred mode of selection across subdivisions of the phenotype in early tetrapodomorphs.
Fig. 5: Distribution of relative rates of evolution for each morphological partition across tetrapodomorphs.

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Data availability

All data generated and analysed are available online as Supplementary Data 1–3 at Harvard’s Dataverse Repositoryhttps://doi.org/10.7910/DVN/NNVTTD80. Source data are provided with this paper.

Code availability

All R scripts, MrBayes command blocks and BEAST2 XML files are freely available online at Harvard’s Dataverse Repositoryhttps://doi.org/10.7910/DVN/NNVTTD80. R scripts for all protocols are also available on GitHub: https://github.com/tiago-simoes/MorphoEvol_Tetrapods.git.

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Acknowledgements

We thank C. Zhang for discussions and J. Barido-Sottani for valuable assistance with the treeWoffset operator of BEAST2. We also thank M. Caldwell and K. Jones for comments on an earlier version of the manuscript. T.R.S. was supported by an Alexander Agassiz postdoctoral fellowship (Museum of Comparative Zoology, Harvard University) and a National Sciences and Engineering Council of Canada (NSERC) postdoctoral fellowship. Additional funds were provided by Harvard University to S.E.P.

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Authors and Affiliations

  1. Museum of Comparative Zoology & Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Tiago R. Simões & Stephanie E. Pierce

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  1. Tiago R. Simões
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Contributions

T.R.S. and S.E.P. conceived and designed the project. T.R.S. updated the morphological dataset, conducted phylogenetic and statistical analyses, interpreted the data and wrote the manuscript. S.E.P. updated the morphological dataset, interpreted the data and wrote the manuscript.

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Correspondence to Tiago R. Simões.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Neil Brocklehurst and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Violin plots for estimates from SFBD free parameters across time bins.

a, violin plots from main tip-dating only analysis. b, violin plots after incorporating the age of the Zachełmie tracks. Net diversification nearly halves for the first and second time bins using the new divergence times. Relative extinction values also decrease but, to a lower extent, whereas median relative fossilization remains similar between analyses (see also Fig. 2). However, the new diversification scenario (B) suggests a less drastic reduction in net diversification values across time bins during early tetrapodomorph evolution.

Source data

Extended Data Fig. 2 Kernel density plot for the base of the clock rate among different calibration strategies.

Results for the main tip-dating analysis using the SFBD tree model (see also Supplementary Fig. 12, 13) and results from the main tip+node dating analysis (including trackway data) using the SFBD tree model (see also Supplementary Figs. 16, 17), with medians = 0.01083 vs 0.03514, respectively.

Source data

Extended Data Fig. 3 Comparison of divergence time and MCT topologies obtained across distinct analyses using distinct calibration strategies.

a, results from the main tip-dating analysis using the SFBD tree model (see also Supplementary Information Figs. 12, 13). b, results from the main tip+node dating analysis (including trackway data) using the SFBD tree model (see also Supplementary Information Figs. 16, 17). c, Results from the main tip+node dating analysis (including trackway data) using partitioned morphological clocks (see also Supplementary Information Figs. 18, 19). Node values represent median ages and purple error bars represent the 95% highest posterior density (HPD) intervals.

Extended Data Fig. 4 Overall relative rates of morphological evolution in early tetrapodomorphs using distinct calibration strategies.

a, rates of morphological evolution obtained from the main tip-dating only analysis. b, overall relative rates of morphological evolution obtained from the main tip+node dating analysis (including trackway age data) using a single clock partition. Under the new evolutionary scenario, (b) estimated rates of morphological evolution within Elpistostegalians are closer in magnitude to evolutionary rates in other clades in the tree. However, as the branches leading up to other tetrapodomorph lineages also become somewhat proportionally longer chronologically, Elpistostegalians still retained the highest relative rates of morphological evolution in the entire tree.

Extended Data Fig. 5 Relative rates of morphological evolution using partitioned morphological clocks.

Models and calibration parameters as in Extended Data Fig. 4b.

Extended Data Fig. 6 Display of significantly accelerating or decelerating rates of evolution across lineages.

Relative rates of morphological evolution using the same models and calibrations as in Extended Data Fig. 4b but using partitioned morphological clocks. Branch colouring indicates whether rates are significantly higher (> 1.297040, in red) or lower (< 0.735828, in blue) by one standard deviation from the background rate (=1.0). Grey branches indicate rates are not significantly different from background rates.

Extended Data Fig. 7 Nonlinear multidimensional scaling analysis using t-SNE plotted with morphological character clusters identified by the PAM+Si method highlighted in different colours.

Numbers indicate character numbers in the updated character list available as Supplementary Data 1.

Source data

Extended Data Fig. 8 Histograms of depositional paleo-environment of all occurrences of all dipnomorphans and early tetrapodomorphs taxa assessed here.

Data obtained from the Paleobiology Database and from literature survey. For raw data, see Dataset S3.

Source data

Supplementary information

Supplementary Information

Supplementary Methods, dataset updates, Figs. 1–30, Tables 1–13 and references.

Reporting Summary

Peer Review Information

Source data

Source Data Fig. 2

Bayesian posterior output for clock and FBD parameters across time bins for tip and tip + node calibrated analyses.

Source Data Fig. 5

Bayesian summary tree output for each clock partition per clade.

Source Data Extended Data Fig. 1

Bayesian posterior output for clock and FBD parameters across time bins for tip and tip + node calibrated analyses.

Source Data Extended Data Fig. 2

Bayesian posterior output for clock and FBD parameters across time bins for tip and tip + node calibrated analyses.

Source Data Extended Data Fig. 7

Gower distance matrix.

Source Data Extended Data Fig. 8

Statistical source data obtained from PBDB and additional sources (listed within file).

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Simões, T.R., Pierce, S.E. Sustained high rates of morphological evolution during the rise of tetrapods. Nat Ecol Evol 5, 1403–1414 (2021). https://doi.org/10.1038/s41559-021-01532-x

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