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Functional adaptive landscapes predict terrestrial capacity at the origin of limbs

Nature volume 589, pages 242–245 (2021)Cite this article

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Abstract

The acquisition of terrestrial, limb-based locomotion during tetrapod evolution has remained a subject of debate for more than a century1,2. Our current understanding of the locomotor transition from water to land is largely based on a few exemplar fossils such as Tiktaalik3, Acanthostega4, Ichthyostega5 and Pederpes6. However, isolated bony elements may reveal hidden functional diversity, providing a more comprehensive evolutionary perspective7. Here we analyse 40 three-dimensionally preserved humeri from extinct tetrapodomorphs that span the fin-to-limb transition and use functionally informed ecological adaptive landscapes8,9,10 to reconstruct the evolution of terrestrial locomotion. We show that evolutionary changes in the shape of the humerus are driven by ecology and phylogeny and are associated with functional trade-offs related to locomotor performance. Two divergent adaptive landscapes are recovered for aquatic fishes and terrestrial crown tetrapods, each of which is defined by a different combination of functional specializations. Humeri of stem tetrapods share a unique suite of functional adaptations, but do not conform to their own predicted adaptive peak. Instead, humeri of stem tetrapods fall at the base of the crown tetrapod landscape, indicating that the capacity for terrestrial locomotion occurred with the origin of limbs. Our results suggest that stem tetrapods may have used transitional gaits5,11 during the initial stages of land exploration, stabilized by the opposing selective pressures of their amphibious habits. Effective limb-based locomotion did not arise until loss of the ancestral ‘L-shaped’ humerus in the crown group, setting the stage for the diversification of terrestrial tetrapods and the establishment of modern ecological niches12,13.

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Fig. 1: Three stages of humerus morphological evolution.
Fig. 2: Phylogenetic sample, morphospace and functional performance surfaces.
Fig. 3: Adaptive landscapes.

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Data availability

The data supporting the findings of this study are available within the paper and its Supplementary Information. Supplementary Data 1 includes the functional trait data for replicating the performance surfaces (Fig. 2), adaptive landscapes (Fig. 3) and ancestral state reconstructions (Extended Data Figs. 3, 4); it also includes the specimen information as well as first–last occurrence data. Occurrence data were extracted from the literature, as listed in Supplementary Data 1, and the Paleobiology Database (http://fossilworks.org). Supplementary Data 2 includes the landmark coordinates for replicating the morphospace (Fig. 2 and Extended Data Figs. 1, 2). Supplementary Data 3 includes the time-calibrated phylogenetic tree (Fig. 2) and provides the data needed to replicate the phylomorphospace (Fig. 2 and Extended Data Fig. 1, 2), ancestral state reconstructions (Extended Data Figs. 3, 4) and transitional landscape (Fig. 3 and Extended Data Fig. 4). All other data that support the findings of this study are available from the corresponding authors on request.

Code availability

All code required to replicate this study has been compiled into the R package Morphoscape and is available on github (https://github.com/blakedickson/Morphoscape).

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Acknowledgements

We thank P. Ahlberg, K. Angielczyk, A. Biewener, D. Brinkman, C. Capobianco, S. Chapman, J. Cundiff, T. Fedak, J. Hanken, Z. Johanson, G. Lauder, J. Long, C. Mansky, K. Ogden, P. D. Polly, D. Skilliter, K. Smithson and S. Walsh for their support during project development. The research was funded by the Museum of Comparative Zoology Putnam Expedition Grants (S.E.P.), Robert A. Chapman Fellowship (B.V.D.), Harvard University (S.E.P. and B.V.D.) and a NERC consortium grant (NE/J022713/1 to J.A.C. and T.R.S.).

Author information

Author notes

  1. Deceased: Jennifer A. Clack

Authors and Affiliations

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

    Blake V. Dickson & Stephanie E. Pierce

  2. University Museum of Zoology, University of Cambridge, Cambridge, UK

    Jennifer A. Clack & Timothy R. Smithson

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  1. Blake V. Dickson
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Contributions

S.E.P. and B.V.D. conceived and designed the study. B.V.D. collected, analysed and interpreted data, made the figures and wrote the manuscript. J.A.C. and T.R.S. collected data and edited the manuscript. S.E.P. collected and interpreted data, guided figure construction and wrote the manuscript. All authors approved the final draft of the manuscript.

Corresponding authors

Correspondence to Blake V. Dickson or Stephanie E. Pierce.

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The authors declare no competing interests.

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Peer review information Nature thanks Kenneth Angielczyk 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 figures and tables

Extended Data Fig. 1 Temporal distribution of specimens in morphospace.

Species (n = 38) are colour-coded by geological time period or stage. Brown, Upper Devonian (Frasnian and Famennian stages); light green, Romer’s gap (Tournaisian stage); grey blue, Carboniferous period (Middle–Late Mississippian and Pennsylvanian); red, Permian period; purple, Triassic period.

Extended Data Fig. 2 Taxonomic distribution of specimens in morphospace.

a, Morphospace (Fig. 2b) with the 38 species colour-coded by broad taxonomic group. b, The ‘Stem’ region of the morphospace enlarged to resolve densely clustered specimens. Magenta, tetrapodomorph fish; green, stem tetrapods; tan, Amphibia; Orange, reptilomorphs; Red, Amniota. See Supplementary Data 1 for specimen abbreviations.

Extended Data Fig. 3 Six function traits mapped to the phylogeny.

Functional traits measured for each fossil species and specimen and plotted onto the phylogeny using maximum likelihood ancestral state reconstruction. Warm colours indicate higher performance; cool colours indicate lower performance. See Supplementary Data 1 for specimen abbreviations and tip values.

Extended Data Fig. 4 Transitional landscape node and tip values.

Contour mapping of the transitional adaptive landscape (Fig. 3b) projected onto the phylogeny, with height values on the landscape provided for nodes and tips. The landscape is centred around 1 (white), with values less than 1 (blue) representing an aquatic regime, and values greater than 1 (brown) representing a terrestrial regime.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Results 1-4 and Supplementary Notes 1-5.

Reporting Summary

Supplementary Data

Supplementary Data 1 includes the functional trait data for replicating the performance surfaces (Fig. 2), adaptive landscapes (Fig. 3), and ancestral state reconstructions (Extended Data Figs. 3 and 4); it also includes the specimen information as well as first-last occurrence data. Occurrence data were extracted from the literature, as listed in Source Data 1, and the Paleobiology Database (http://fossilworks.org).

Supplementary Data

Supplementary Data 2 includes the landmark coordinates for replicating the morphospace (Fig. 2, Extended Data Figs. 1, 2).

Supplementary Data

Supplementary Data 3 includes the time-calibrated phylogenetic tree (Fig. 2) and provides data needed to replicate the phylomorphospace (Fig. 2, Extended Data Fig.1, 2), ancestral state reconstructions (Extended Data Figs. 3, 4) and transitional landscape (Fig. 3, Extended Data Fig. 4).

Video 1

: Extended Data Figure 1 animation.

.Peer Review File

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Dickson, B.V., Clack, J.A., Smithson, T.R. et al. Functional adaptive landscapes predict terrestrial capacity at the origin of limbs. Nature 589, 242–245 (2021). https://doi.org/10.1038/s41586-020-2974-5

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