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Functional adaptive landscapes predict terrestrial capacity at the origin of limbs

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.

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).

References

  1. 1.

    Pierce, S. E., Hutchinson, J. R. & Clack, J. A. Historical perspectives on the evolution of tetrapodomorph movement. Integr. Comp. Biol. 53, 209–223 (2013).

    PubMed  Google Scholar 

  2. 2.

    Ahlberg, P. E. Follow the footprints and mind the gaps: a new look at the origin of tetrapods. Earth Environ. Sci. Trans. R. Soc. Edinb. 109, 115–137 (2019).

    CAS  Google Scholar 

  3. 3.

    Shubin, N. H., Daeschler, E. B. & Jenkins, F. A. Jr. The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature 440, 764–771 (2006).

    ADS  CAS  PubMed  Google Scholar 

  4. 4.

    Coates, M. I. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution. Earth Environ. Sci. Trans. R. Soc. Edinb. 87, 363–421 (1996).

    Google Scholar 

  5. 5.

    Pierce, S. E., Clack, J. A. & Hutchinson, J. R. Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature 486, 523–526 (2012).

    ADS  CAS  PubMed  Google Scholar 

  6. 6.

    Clack, J. A. & Finney, S. M. Pederpes finneyae, an articulated tetrapod from the Tournaisian of Western Scotland. J. Syst. Palaeontol. 2, 311–346 (2005).

    Google Scholar 

  7. 7.

    Smithson, T. R. & Clack, J. A. Tetrapod appendicular skeletal elements from the Early Carboniferous of Scotland. C. R. Palevol 12, 405–417 (2013).

    Google Scholar 

  8. 8.

    Polly, P. D. et al. Combining geometric morphometrics and finite element analysis with evolutionary modeling: towards a synthesis. J. Vertebr. Paleontol. 36, e1111225 (2016).

    Google Scholar 

  9. 9.

    Dickson, B. V. & Pierce, S. E. Functional performance of turtle humerus shape across an ecological adaptive landscape. Evolution 73, 1265–1277 (2019).

    PubMed  Google Scholar 

  10. 10.

    Stayton, C. T. Performance in three shell functions predicts the phenotypic distribution of hard-shelled turtles. Evolution 73, 720–734 (2019).

    PubMed  Google Scholar 

  11. 11.

    Nyakatura, J. A., Andrada, E., Curth, S. & Fischer, M. S. Bridging “Romer’s gap”: limb mechanics of an extant belly-dragging lizard inform debate on tetrapod locomotion during the Early Carboniferous. Evol. Biol. 41, 175–190 (2014).

    Google Scholar 

  12. 12.

    Sahney, S., Benton, M. J. & Ferry, P. A. Links between global taxonomic diversity, ecological diversity and the expansion of vertebrates on land. Biol. Lett. 6, 544–547 (2010).

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Sennikov, A. G. On the dynamics of the formation of the niche space during the exploration of land by vertebrates. Paleontol. J. 43, 478–482 (2009).

    Google Scholar 

  14. 14.

    Sanchez, S., Tafforeau, P., Clack, J. A. & Ahlberg, P. E. Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography. Nature 537, 408–411 (2016).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Sanchez, S. et al. 3D microstructural architecture of muscle attachments in extant and fossil vertebrates revealed by synchrotron microtomography. PLoS ONE 8, e56992 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Molnar, J. L., Diogo, R., Hutchinson, J. R. & Pierce, S. E. Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins-to-limbs transition. Biol. Rev. Camb. Philos. Soc. 93, 1077–1107 (2018).

    PubMed  Google Scholar 

  17. 17.

    Ruta, M., Krieger, J., Angielczyk, K. D. & Wills, M. A. The evolution of the tetrapod humerus: morphometrics, disparity, and evolutionary rates. Earth Environ. Sci. Trans. R. Soc. Edinb. 109, 351–369 (2019).

    Google Scholar 

  18. 18.

    Callier, V., Clack, J. A. & Ahlberg, P. E. Contrasting developmental trajectories in the earliest known tetrapod forelimbs. Science 324, 364–367 (2009).

    ADS  CAS  PubMed  Google Scholar 

  19. 19.

    Clack, J. A. The fin to limb transition: new data, interpretations, and hypotheses from paleontology and developmental biology. Annu. Rev. Earth Planet. Sci. 37, 163–179 (2009).

    ADS  CAS  Google Scholar 

  20. 20.

    Smithson, T. R. & Clack, J. A. A new tetrapod from Romer’s gap reveals an early adaptation for walking. Earth Environ. Sci. Trans. R. Soc. Edinb. 108, 89–97 (2017).

    Google Scholar 

  21. 21.

    Ruta, M. & Wills, M. A. Comparable disparity in the appendicular skeleton across the fish–tetrapod transition, and the morphological gap between fish and tetrapod postcrania. Palaeontology 59, 249–267 (2016).

    Google Scholar 

  22. 22.

    Clack, J. A. et al. Phylogenetic and environmental context of a Tournaisian tetrapod fauna. Nat. Ecol. Evol. 1, 0002 (2016).

    Google Scholar 

  23. 23.

    Anderson, J. S., Smithson, T. R., Mansky, C. F., Meyer, T. & Clack, J. A diverse tetrapod fauna at the base of ‘Romer’s gap’. PLoS ONE 10, e0125446 (2015).

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Clarkson, E. N. K., Milner, A. R. & Coates, M. I. Palaeoecology of the Viséan of East Kirkton, West Lothian, Scotland. Earth Environ. Sci. Trans. R. Soc. Edinb. 84, 417–425 (1993).

    Google Scholar 

  25. 25.

    Milner, A. R. & Sequeira, S. E. K. The temnospondyl amphibians from the Viséan of East Kirkton, West Lothian, Scotland. Earth Environ. Sci. Trans. R. Soc. Edinb. 84, 331–361 (1993).

    Google Scholar 

  26. 26.

    Smithson, T. R., Carroll, R. L., Panchen, A. L. & Andrews, S. M. Westlothiana lizziae from the Viséan of East Kirkton, West Lothian, Scotland, and the amniote stem. Earth Environ. Sci. Trans. R. Soc. Edinb. 84, 383–412 (1993).

    Google Scholar 

  27. 27.

    Paton, R. L., Smithson, T. R. & Clack, J. A. An amniote-like skeleton from the early carboniferous of Scotland. Nature 398, 508–513 (1999).

    ADS  CAS  Google Scholar 

  28. 28.

    Andrews, S. M. & Westoll, T. S. The postcranial skeleton of Eusthenopteron foordi Whiteaves. Earth Environ. Sci. Trans. R. Soc. Edinb. 68, 207–329 (1970).

    Google Scholar 

  29. 29.

    Pierce, S. E., Lamas, L. P., Pelligand, L., Schilling, N. & Hutchinson, J. R. Patterns of limb and epaxial muscle activity during walking in the fire salamander, Salamandra salamandra. Integr. Org. Biol. 2, obaa015 (2020).

    Google Scholar 

  30. 30.

    Polly, P. D. Functional tradeoffs carry phenotypes across the Valley of the Shadow of Death. Integr. Org. Biol. icaa092 (2020).

  31. 31.

    Coates, M. I. & Clack, J. A. Romer’s gap: tetrapod origins and terrestriality. Bull. Mus. Natl Hist. Nat. 17, 373–388 (1995).

    Google Scholar 

  32. 32.

    Anderson, P. S. L., Friedman, M. & Ruta, M. Late to the table: diversification of tetrapod mandibular biomechanics lagged behind the evolution of terrestriality. Integr. Comp. Biol. 53, 197–208 (2013).

    PubMed  Google Scholar 

  33. 33.

    Cignoni, P. et al. MeshLab: an open-source mesh processing tool. In Proc. 6th Eurographics Italian Chapter Conference 129–136 (2008).

  34. 34.

    Glynn, C. & Puente, J. Auto3dgm: 3-dimensional geometric morphometrics. R package version 1.0 https://github.com/sayanmuk/Auto3DGM/ (2013).

  35. 35.

    Boyer, D. M. et al. A new fully automated approach for aligning and comparing shapes. Anat. Rec. 298, 249–276 (2015).

    Google Scholar 

  36. 36.

    Eldar, Y., Lindenbaum, M., Porat, M. & Zeevi, Y. Y. The farthest point strategy for progressive image sampling. IEEE Trans. Image Process. 6, 1305–1315 (1997).

    ADS  CAS  PubMed  Google Scholar 

  37. 37.

    Adams, D. C., Collyer, M. L. & Kaliontzopoulou, A. Geomorph: software for geometric morphometric analyses. R package version 3.0.6 https://cran.r-project.org/package=geomorph (2018).

  38. 38.

    Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 3.61 https://www.mesquiteproject.org/ (2019).

  39. 39.

    Ruta, M., Pisani, D., Lloyd, G. T. & Benton, M. J. A supertree of Temnospondyli: cladogenetic patterns in the most species-rich group of early tetrapods. Proc. R. Soc. Lond. B 274, 3087–3095 (2007).

    Google Scholar 

  40. 40.

    Ruta, M. in Studies on Fossil Tetrapods. Special Papers in Palaeontology 86 (eds Barrett, P. M. & Milner, A. R.) 31–43 (Jon Wiley and Sons, 2011).

  41. 41.

    Schoch, R. R. The evolution of major temnospondyl clades: an inclusive phylogenetic analysis. J. Syst. Paleontol. 11, 673–705 (2013).

    Google Scholar 

  42. 42.

    Bernardi, M., Angielczyk, K. D., Mitchell, J. S. & Ruta, M. Phylogenetic stability, tree shape, and character compatibility: a case study using early tetrapods. Syst. Biol. 65, 737–758 (2016).

    PubMed  Google Scholar 

  43. 43.

    Alroy, J., Marshall, C. & Miller, A. The Paleobiology Database. https://paleobiodb.org/ (2004).

  44. 44.

    Bapst, D. W. paleotree: paleontological and phylogenetic analyses of evolution. R package version 3.30 https://cran.r-project.org/web/packages/paleotree/ (2012).

  45. 45.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Google Scholar 

  46. 46.

    Adams, D. C. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst. Biol. 63, 685–697 (2014).

    PubMed  Google Scholar 

  47. 47.

    Lafarge, T. & Pateiro-Lopez, B. alphashape3d: implementation of the 3D alpha-shape for the reconstruction of 3D sets from a point cloud. R package version 1.3 https://cran.r-project.org/web/packages/alphashape3d/ (2017).

  48. 48.

    Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S 4th edn (Springer, 2002).

  49. 49.

    Jenkins, F. A. Jr. The functional anatomy and evolution of the mammalian humero-ulnar articulation. Am. J. Anat. 137, 281–297 (1973).

    PubMed  Google Scholar 

  50. 50.

    Rackoff, J. S. in The Terrestrial Environment and the Origin of Land Vertebrates (ed. Panchen, A. L.) 255–292 (Academic Press, 1980).

  51. 51.

    Hopson, J. A. in Great Transformations in Vertebrate Evolution (eds. Dial, K. P. et al.) 125–141 (Univ. Chicago Press, 2015).

  52. 52.

    Russell, A. P. & Bels, V. Biomechanics and kinematics of limb-based locomotion in lizards: review, synthesis and prospectus. Comp. Biochem. Physiol. A 131, 89–112 (2001).

    CAS  Google Scholar 

  53. 53.

    Kilbourne, B. M. & Hoffman, L. C. Scale effects between body size and limb design in quadrupedal mammals. PLoS ONE 8, e78392 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Doube, M. et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone 47, 1076–1079 (2010).

    PubMed  PubMed Central  Google Scholar 

  55. 55.

    Rueden, C. T. et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18, 529 (2017).

    PubMed  PubMed Central  Google Scholar 

  56. 56.

    Stayton, C. T. Warped finite element models predict whole shell failure in turtle shells. J. Anat. 233, 666–678 (2018).

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Germain, D. & Laurin, M. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool. Scr. 34, 335–350 (2005).

    Google Scholar 

  58. 58.

    Sanchez, S. et al. Limb-bone histology of temnospondyls: implications for understanding the diversification of palaeoecologies and patterns of locomotion of Permo-Triassic tetrapods. J. Evol. Biol. 23, 2076–2090 (2010).

    CAS  PubMed  Google Scholar 

  59. 59.

    Sanchez, S., Tafforeau, P. & Ahlberg, P. E. The humerus of Eusthenopteron: a puzzling organization presaging the establishment of tetrapod limb bone marrow. Proc. R. Soc. Lond. B 281, 20140299 (2014).

    CAS  Google Scholar 

  60. 60.

    Konietzko-Meier, D. & Sander, P. M. Long bone histology of Metoposaurus diagnosticus (Temnospondyli) from the Late Triassic of Krasiejów (Poland) and its paleobiological implications. J. Vertebr. Paleontol. 33, 1003–1018 (2013).

    Google Scholar 

  61. 61.

    Laurin, M. & de Buffrénil, V. Microstructural features of the femur in early ophiacodontids: a reappraisal of ancestral habitat use and lifestyle of amniotes. C. R. Palevol 15, 115–127 (2016).

    Google Scholar 

  62. 62.

    Konietzko-Meier, D., Shelton, C. D. & Martin, S. P. The discrepancy between morphological and microanatomical patterns of anamniotic stegocephalian postcrania from the Early Permian Briar Creek Bonebed (Texas). C. R. Palevol 15, 103–114 (2016).

    Google Scholar 

  63. 63.

    Butcher, M. T. & Blob, R. W. Mechanics of limb bone loading during terrestrial locomotion in river cooter turtles (Pseudemys concinna). J. Exp. Biol. 211, 1187–1202 (2008).

    PubMed  Google Scholar 

  64. 64.

    Kawano, S. M., Economy, D. R., Kennedy, M. S., Dean, D. & Blob, R. W. Comparative limb bone loading in the humerus and femur of the tiger salamander: testing the ‘mixed-chain’ hypothesis for skeletal safety factors. J. Exp. Biol. 219, 341–353 (2016).

    PubMed  Google Scholar 

  65. 65.

    Perry, J. M. G. & Prufrock, K. A. Muscle functional morphology in paleobiology: the past, present, and future of “paleomyology”. Anat. Rec. 301, 538–555 (2018).

    Google Scholar 

  66. 66.

    Biewener, A. A. & Patek, S. Animal Locomotion (Oxford Univ. Press, 2018).

  67. 67.

    Bishop, P. J. The humerus of Ossinodus pueri, a stem tetrapod from the Carboniferous of Gondwana, and the early evolution of the tetrapod forelimb. Alcheringa 38, 209–238 (2014).

    Google Scholar 

  68. 68.

    Arnold, S. J., Pfrender, M. E. & Jones, A. G. in Microevolution Rate, Pattern, Process (eds. Hendry, A. P. & Kinnison, M. T.) 9–32 (Springer Netherlands, 2001).

  69. 69.

    Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1944).

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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.).

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Authors

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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