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Metamorphosis shapes cranial diversity and rate of evolution in salamanders

Nature Ecology & Evolution volume 4, pages 1129–1140 (2020)Cite this article

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Abstract

Metamorphosis is widespread across the animal kingdom and induces fundamental changes in the morphology, habitat and resources used by an organism during its lifetime. Metamorphic species are likely to experience more dynamic selective pressures through ontogeny compared with species with single-phase life cycles, which may drive divergent evolutionary dynamics. Here, we reconstruct the cranial evolution of the salamander using geometric morphometric data from 148 species spanning the order’s full phylogenetic, developmental and ecological diversity. We demonstrate that life cycle influences cranial shape diversity and rate of evolution. Shifts in the rate of cranial evolution are consistently associated with transitions from biphasic to either direct-developing or paedomorphic life cycle strategies. Direct-developers exhibit the slowest rates of evolution and the lowest disparity, and paedomorphic species the highest. Species undergoing complete metamorphosis (biphasic and direct-developing) exhibit greater cranial modularity (evolutionary independence among regions) than do paedomorphic species, which undergo differential metamorphosis. Biphasic and direct-developing species also display elevated disparity relative to the evolutionary rate for bones associated with feeding, whereas this is not the case for paedomorphic species. Metamorphosis has profoundly influenced salamander cranial evolution, requiring greater autonomy of cranial elements and facilitating the rapid evolution of regions that are remodelled through ontogeny. Rather than compounding functional constraints on variation, metamorphosis seems to have promoted the morphological evolution of salamanders over 180 million years, which may explain the ubiquity of this complex life cycle strategy across disparate organisms.

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Fig. 1: Landmarks used to quantify cranial shape variation in Caudata.
Fig. 2: Phylomorphospace illustrating the first two PCs of cranial shape across Caudata.
Fig. 3: Evolution of the life cycle in Caudata.
Fig. 4: Evolutionary rates and rate shifts for cranial shape in Caudata.
Fig. 5: Modularity and integration in cranial shape for different caudatan life cycle strategies.
Fig. 6: Per-landmark evolutionary rate against Procrustes variance for different caudatan life cycle strategies.

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Data availability

The scan data that support the findings of this study have been deposited in the Phenome10K repository (http://phenome10k.org/) or are already available on MorphoSource and DigiMorph (the URLs and DOIs are available in Supplementary Data 7). The Procrustes coordinates, centroid size, life cycle and microhabitat definitions are available in Supplementary Data 12. The table of module hypotheses used in the modularity analyses is available in Supplementary Data 13. The MCC tree, scaled MCC tree and output of the Bayesian analyses are available at https://github.com/anjgoswami/salamanders. All other data analysed in this study are included in the Supplementary Information.

Code availability

The R and Bayestrait codes used in this paper are available at https://github.com/anjgoswami/salamanders.

References

  1. Hanken, J. Development and evolution in amphibians. Am. Sci. 77, 336–343 (1989).

    Google Scholar 

  2. Raff, R. A. & Raff, E. C. Development as an Evolutionary Process (Alan R. Liss, 1987).

  3. Bhullar, B.-A. S. et al. Birds have paedomorphic dinosaur skulls. Nature 487, 223–226 (2012).

    CAS  PubMed  Google Scholar 

  4. Alberch, P. in Environmental Adaptation and Evolution (eds Mossakowski, D. & Roth, G.) 19–36 (Gustav Fischer, 1982).

  5. Roth, G. in Environmental Adaptation and Evolution (eds Mossakowski, D. & Roth, G.) 37–48 (Gustav Fischer, 1982).

  6. Haeckel, E. Generelle Morphologie der Organismen Vols. 1 and 2 (G. Reimer, 1866).

  7. Duméril, A. Reproduction, dans la Ménagerie des Reptiles au Musée d’Histoire Naturelle, des axolotls, batraciens urodèles à branchies persistantes, du Mexique (Sirenodon mexicanus vel Humboldtii), qui n’avaient encore jamais été vus vivants en Europe. C. R. Acad. Sci. 60, 765–767 (1865).

    Google Scholar 

  8. Laudet, V. The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21, R726–R737 (2011).

    CAS  PubMed  Google Scholar 

  9. Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. How many species are there on Earth and in the ocean? PLoS Biol. 9, e1001127 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. McMenamin, S. K. & Parichy, D. M. in Current Topics in Developmental Biology Vol. 103 (ed. Shi, Y.-B.) 127–165 (Academic Press, 2013).

  11. McMahon, D. P. & Hayward, A. Why grow up? A perspective on insect strategies to avoid metamorphosis. Ecol. Entomol. 41, 505–515 (2016).

    Google Scholar 

  12. Rainford, J. L., Hofreiter, M., Nicholson, D. B. & Mayhew, P. J. Phylogenetic distribution of extant richness suggests metamorphosis is a key innovation driving diversification in insects. PLoS ONE 9, e109085 (2014).

    PubMed  PubMed Central  Google Scholar 

  13. Rolff, J., Johnston, P. R. & Reynolds, S. Complete metamorphosis of insects. Philos. Trans. R. Soc. B 374, 20190063 (2019).

    Google Scholar 

  14. Truman, J. W. & Riddiford, L. M. The evolution of insect metamorphosis: a developmental and endocrine view. Philos. Trans. R. Soc. B 374, 20190070 (2019).

    CAS  Google Scholar 

  15. Bonner, J. T. Size and Cycle—an Essay on the Structure of Biology (Princeton Univ. Press, 1965).

  16. Ebenman, B. Niche differences between age classes and intraspecific competition in age-structured populations. J. Theor. Biol. 124, 25–33 (1987).

    Google Scholar 

  17. Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).

    PubMed  PubMed Central  Google Scholar 

  18. Hansen, T. F. Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. BioSystems 69, 83–94 (2003).

    PubMed  Google Scholar 

  19. Drake, A. G. & Klingenberg, C. P. Large‐scale diversification of skull shape in domestic dogs: disparity and modularity. Am. Nat. 175, 289–301 (2010).

    PubMed  Google Scholar 

  20. Klingenberg, C. P. Studying morphological integration and modularity at multiple levels: concepts and analysis. Philos. Trans. R. Soc. B 369, 20130249 (2014).

    Google Scholar 

  21. Ebenman, B. Evolution in organisms that change their niches during the life cycle. Am. Nat. 139, 990–1021 (1992).

    Google Scholar 

  22. Moran, N. A. Adaptation and constraint in the complex life cycles of animals. Annu. Rev. Ecol. Evol. Syst. 25, 573–600 (1994).

    Google Scholar 

  23. Wollenberg Valero, K. C. et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nat. Commun. 8, 15213 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Goedert, D. & Calsbeek, R. Experimental evidence that metamorphosis alleviates genomic conflict. Am. Nat. 194, 356–366 (2019).

    PubMed  Google Scholar 

  25. Bonett, R. M. & Blair, A. L. Evidence for complex life cycle constraints on salamander body form diversification. Proc. Natl Acad. Sci. USA 114, 9936–9941 (2017).

    CAS  PubMed  Google Scholar 

  26. Vučić, T. et al. Testing the evolutionary constraints of metamorphosis: the ontogeny of head shape in Triturus newts. Evolution 73, 1253–1264 (2019).

    PubMed  Google Scholar 

  27. Wake, D. B. & Koo, M. S. Amphibians. Curr. Biol. 28, R1237–R1241 (2018).

    CAS  PubMed  Google Scholar 

  28. Ziermann, J. M. in Heads, Jaws, and Muscles (eds Ziermann, J., Diaz Jr, R. E. & Diogo, R.) 143–170 (Springer, 2019).

  29. Bonett, R. M. in Evolutionary Developmental Biology (eds Nuño de la Rosa, L. & Müller, G. B.) 1–14 (Springer, 2018).

  30. Bonett, R. M., Chippindale, P. T., Moler, P. E., Wayne, V. D. R. & Wake, D. B. Evolution of gigantism in amphiumid salamanders. PLoS ONE 4, e5615 (2009).

    PubMed  PubMed Central  Google Scholar 

  31. Bonett, R. M., Steffen, M. A., Lambert, S. M., Wiens, J. J. & Chippindale, P. T. Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution 68, 466–482 (2013).

    PubMed  Google Scholar 

  32. Chippindale, P. T., Bonett, R. M., Baldwin, A. S. & Wiens, J. J. Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders. Evolution 58, 2809–2822 (2004).

    CAS  PubMed  Google Scholar 

  33. Ledbetter, N. M. & Bonett, R. M. Terrestriality constrains salamander limb diversification: implications for the evolution of pentadactyly. J. Evol. Biol. 32, 642–652 (2019).

    PubMed  Google Scholar 

  34. Blankers, T., Adams, D. C. & Wiens, J. J. Ecological radiation with limited morphological diversification in salamanders. J. Evol. Biol. 25, 634–646 (2012).

    PubMed  Google Scholar 

  35. Hanken, J. & Hall, B. K. The Skull: Patterns of Structural and Systematic Diversity Vol. 2 (Univ. of Chicago Press, 1993).

  36. Vassilieva, A. B., Lai, J.-S., Yang, S.-F., Chang, Y.-H. & Poyarkov, N. A. J. Development of the bony skeleton in the Taiwan salamander, Hynobius formosanus Maki, 1922 (Caudata: Hynobiidae): heterochronies and reductions. Vert. Zool. 65, 117–130 (2015).

    Google Scholar 

  37. Truman, J. W. & Riddiford, L. M. The origins of insect metamorphosis. Nature 401, 447–452 (1999).

    CAS  PubMed  Google Scholar 

  38. Taylor, M. A. How tetrapods feed in water: a functional analysis by paradigm. Zool. J. Linn. Soc. 91, 171–195 (1987).

    Google Scholar 

  39. Schwenk, K. Feeding: Form, Function, and Evolution in Tetrapod Vertebrates (Academic Press, 2000).

  40. Bels, V. & Whishaw, I. Q. Feeding in Vertebrates: Evolution, Morphology, Behavior, Biomechanics (Springer, 2019).

  41. Duellman, W. E. & Trueb, L. Biology of Amphibians (McGraw-Hill, 1986).

  42. Johnson, C. K. & Voss, S. R. Salamander paedomorphosis: linking thyroid hormone to life history and life cycle evolution. Curr. Top. Dev. Biol. 103, 229–257 (2013).

    CAS  PubMed  Google Scholar 

  43. Wilbur, H. M. & Collins, J. P. Ecological aspects of amphibian metamorphosis. Science 182, 1305–1314 (1973).

    CAS  PubMed  Google Scholar 

  44. Clavel, J. & Morlon, H. Accelerated body size evolution during cold climatic periods in the Cenozoic. Proc. Natl Acad. Sci. USA 114, 4183–4188 (2017).

    CAS  PubMed  Google Scholar 

  45. Botero, C. A., Dor, R., McCain, C. M. & Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Mol. Ecol. 23, 259–268 (2014).

    PubMed  Google Scholar 

  46. Laurin, M. Assessment of modularity in the urodele skull: an exploratory analysis using ossification sequence data. J. Exp. Zool. B 322, 567–585 (2014).

    Google Scholar 

  47. Ivanović, A. & Kalezić, M. L. Testing the hypothesis of morphological integration on a skull of a vertebrate with a biphasic life cycle: a case study of the alpine newt. J. Exp. Zool. B 314B, 527–538 (2010).

    Google Scholar 

  48. Kerney, R. R., Blackburn, D. C., Müller, H. & Hanken, J. Do larval traits re-evolve? Evidence from the embryogenesis of a direct-developing salamander, Plethodon cinereus. Evolution 66, 252–262 (2012).

    PubMed  Google Scholar 

  49. Bon, M., Bardua, C., Goswami, A. & Fabre, A.-C. Cranial integration in the fire salamander, Salamandra salamandra (Caudata: Salamandridae). Biol. J. Linn. Soc. 130, 178–194 (2020).

    Google Scholar 

  50. Wake, D. B. Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Mem. Calif. Acad. Sci. 4, 1–111 (1966).

    Google Scholar 

  51. Reilly, S. M. Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens (Caudata: Salamandridae), and its relationship to metamorphosis and neoteny. J. Morphol. 188, 315–326 (1986).

    CAS  PubMed  Google Scholar 

  52. Ultsch, G. R. & Duke, J. T. Gas exchange and habitat selection in the aquatic salamanders Necturus maculosus and Cryptobranchus alleganiensis. Oecologia 83, 250–258 (1990).

    CAS  PubMed  Google Scholar 

  53. Hanken, J. Life-history and morphological evolution. J. Evol. Biol. 5, 549–557 (1992).

    Google Scholar 

  54. Dinis, M. & Velo-Antón, G. How little do we know about the reproductive mode in the north African salamander, Salamandra algira? Pueriparity in divergent mitochondrial lineages of S. a. tingitana. Amphib. Reptil. 38, 540–546 (2017).

    Google Scholar 

  55. Kraemer, A. C. & Adams, D. C. Predator perception of Batesian mimicry and conspicuousness in a salamander. Evolution 68, 1197–1206 (2014).

    PubMed  Google Scholar 

  56. Heiss, E. & Grell, J. Same but different: aquatic prey capture in paedomorphic and metamorphic alpine newts. Zool. Lett. 5, 5–24 (2019).

    Google Scholar 

  57. Bookstein, F. L. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1, 225–243 (1997).

    CAS  PubMed  Google Scholar 

  58. Gunz, P., Mitteroecker, P. & Bookstein, F. L. in Modern Morphometrics in Physical Anthropology (ed. Slice, D. E.) 73–98 (Springer, 2005).

  59. Bardua, C., Felice, R. N., Watanabe, A., Fabre, A. C. & Goswami, A. A practical guide to sliding and surface semilandmarks in morphometric analyses. Integr. Organism. Biol. 1, 1–34 (2019).

    Google Scholar 

  60. Parr, W. C. et al. Toward integration of geometric morphometrics and computational biomechanics: new methods for 3D virtual reconstruction and quantitative analysis of finite element models. J. Theor. Biol. 301, 1–14 (2012).

    CAS  PubMed  Google Scholar 

  61. Wiley, D. F. et al. Evolutionary morphing. In Proc. IEEE Visualization 2005 (VIS’05) 23–28 October 2005 431–438 (IEEE, 2005).

  62. Dumont, M. et al. Do functional demands associated with locomotor habitat, diet, and activity pattern drive skull shape evolution in musteloid carnivorans? Biol. J. Linn. Soc. 117, 858–878 (2016).

    Google Scholar 

  63. Fabre, A. C., Marigo, J., Granatosky, M. C. & Schmitt, D. Functional associations between support use and forelimb shape in strepsirrhines and their relevance to inferring locomotor behavior in early primates. J. Hum. Evol. 108, 11–30 (2017).

    PubMed  Google Scholar 

  64. Felice, R. N. & Goswami, A. Developmental origins of mosaic evolution in the avian cranium. Proc. Natl Acad. Sci. USA 115, 555–560 (2018).

    CAS  PubMed  Google Scholar 

  65. Watanabe, A. et al. Ecomorphological diversification in squamates from conserved pattern of cranial integration. Proc. Natl Acad. Sci. USA 116, 14688–14697 (2019).

    CAS  PubMed  Google Scholar 

  66. Bardua, C., Wilkinson, M., Gower, D. J., Sherratt, E. & Goswami, A. Morphological evolution and modularity of the caecilian skull. BMC Evol. Biol. 19, 30 (2019).

    PubMed  PubMed Central  Google Scholar 

  67. Marshall, A. F. et al. High-density three-dimensional morphometric analyses support conserved static (intraspecific) modularity in caecilian (Amphibia: Gymnophiona) crania. Biol. J. Linn. Soc. 126, 721–742 (2019).

    Google Scholar 

  68. Botton-Divet, L., Cornette, R., Fabre, A.-C., Herrel, A. & Houssaye, A. Morphological analysis of long bones in semi-aquatic mustelids and their terrestrial relatives. Integr. Comp. Biol. 56, 1298–1309 (2016).

    PubMed  Google Scholar 

  69. Schlager, S. in Statistical Shape and Deformation Analysis (eds Zheng, G. et al.) 217–256 (Academic Press, 2017).

  70. Klingenberg, C. Novelty and “homology-free” morphometrics: what’s in a name? Evol. Biol. 35, 186–190 (2008).

    Google Scholar 

  71. Cardini, A. Lost in the other half: improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Syst. Biol. 65, 1096–1106 (2016).

    PubMed  Google Scholar 

  72. Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).

    PubMed  Google Scholar 

  73. Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).

    PubMed  PubMed Central  Google Scholar 

  74. Heled, J. & Bouckaert, R. R. Looking for trees in the forest: summary tree from posterior samples. BMC Evol. Biol. 13, 221 (2013).

    PubMed  PubMed Central  Google Scholar 

  75. Parra-Olea, G. et al. Biology of tiny animals: three new species of minute salamanders (Plethodontidae: Thorius) from Oaxaca, Mexico. PeerJ 4, e2694 (2016).

    PubMed  PubMed Central  Google Scholar 

  76. Wang, B. et al. Phylogenetic surveys on the newt genus Tylototriton sensu lato (Salamandridae, Caudata) reveal cryptic diversity and novel diversification promoted by historical climatic shifts. PeerJ 6, e4384 (2018).

    PubMed  PubMed Central  Google Scholar 

  77. Collyer, M. L. & Adams, D. C. RRPP: Linear model evaluation with randomized residuals in a permutation procedure. R package version 3.1.2 https://cran.r-project.org/web/packages/RRPP (2019).

  78. Collyer, M. L. & Adams, D. C. An R package for fitting linear models to high‐dimensional data using residual randomization. Methods Ecol. Evol. 9, 1772–1779 (2018).

    Google Scholar 

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

    Google Scholar 

  80. Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. Geometric Morphometrics for Biologists: A Primer (Elsevier/Academic Press, 2012).

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

    CAS  PubMed  Google Scholar 

  82. Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).

    Google Scholar 

  83. Yang, Z. Computational Molecular Evolution (Oxford Univ. Press, 2006).

  84. Akaike, H. in Proceedings of the 2nd International Symposium on Information Theory (eds Petrov, B. N. & Csaki, F.) 267–281 (Akademiai Kiado, 1973).

  85. Goswami, A. & Finarelli, J. A. EMMLi: a maximum likelihood approach to the analysis of modularity. Evolution 70, 1622–1637 (2016).

    PubMed  Google Scholar 

  86. Adams, D. C. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7, 565–572 (2016).

    Google Scholar 

  87. Adams, D. C. & Felice, R. N. Assessing phylogenetic morphological integration and trait covariation in morphometric data using evolutionary covariance matrices. PLoS ONE 9, e9433 (2014).

    Google Scholar 

  88. Spearman, C. The proof and measurement of association between two things. Am. J. Psychol. 15, 72–101 (1904).

    Google Scholar 

  89. Pennell, M. W. et al. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216–2218 (2014).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A.-M. Ohler at the MNHN, the herpetology group at the NHM and N. Fröbisch, K. Mahlow and F. Glöckler at the Museum für Naturkunde. We also thank V. Fernandez and B. Clark for providing training for CT scanning at the NHM and J. Maisano for giving access to CT scans from DigiMorph.org on the NSF grant nos. EF-0334952, IIS-9874781 and IIS-0208675. This work was funded by the European Research Council (grant no. STG-2014–637171 to A.G.) and by a Synthesis (grant no. FR-TAF-5583 to C.B.). This research received support from the US National Science Foundation (oVert TCN; NSF grant no. DBI-1701714) and from the SYNTHESYS Project (http://www.SYNTHESYS.info/), which is financed by European Community Research Infrastructure Action under the FP7 Integrating Activities Programme. We thank B. Poole for help with the analyses.

Author information

Authors and Affiliations

  1. Department of Life Sciences, The Natural History Museum, London, UK

    Anne-Claire Fabre, Carla Bardua, Margot Bon, Julien Clavel, Jeffrey W. Streicher & Anjali Goswami

  2. Department of Genetics, Evolution and Environment, University College London, London, UK

    Carla Bardua & Jeanne Bonnel

  3. Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

    Julien Clavel

  4. Centre for Integrative Anatomy, Department of Cell and Developmental Biology, University College London, London, UK

    Ryan N. Felice

  5. Florida Museum of Natural History, University of Florida, Gainesville, FL, USA

    Edward L. Stanley & David C. Blackburn

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  1. Anne-Claire Fabre
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Contributions

A.-C.F. and A.G. conceived and designed the study. A.-C.F., C.B., M.B., D.C.B., J.B. and E.L.S. acquired and processed the CT data. A.-C.F. acquired the geometric morphometric data. A.-C.F., C.B., J.C. and R.N.F. conducted the analyses. A.-C.F. wrote the initial draft of the manuscript. C.B., M.B., J.C., R.N.F., D.C.B., J.W.S., J.B., E.L.S. and A.G. contributed to the interpretation of the data and to the editing of subsequent drafts of the manuscript.

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Correspondence to Anne-Claire Fabre.

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Extended data

Extended Data Fig. 1 Landmarks used to quantify cranial shape variation in Ambystomidae, Amphiumidae and Cryptobranchidae.

Landmarks used to quantify cranial shape variation in Ambystomidae (Ambystoma tigrinum), Amphiumidae (Amphiuma means) and Cryptobranchidae (Cryptobranchus alleganiensis). Sliding landmarks that describe the 14 bones and 19 regions of the cranium used in all shape analyses. From the left to the right: lateral, dorsal and ventral views of the cranium.

Extended Data Fig. 2 Landmarks used to quantify cranial shape variation in Dicamptodontidae, Hynobiidae and Plethodontidae.

Landmarks used to quantify cranial shape variation in Dicamptodontidae (Dicamptodon ensatus), Hynobiidae (Hynobius leechi) and Plethodontidae (Bolitoglossa salvinii). Sliding landmarks that describe the 14 bones and 19 regions of the cranium used in all shape analyses. From the left to the right: lateral, dorsal and ventral views of the cranium. See colors key in Extended Data Fig. 1.

Extended Data Fig. 3 Landmarks used to quantify cranial shape variation in Proteidae, Rhyacotritonidae, Salamandridae and Sirenidae.

Landmarks used to quantify cranial shape variation in Proteidae (Proteus anguinus), Rhyacotritonidae (Rhyacotriton variegatus), Salamandridae (Salamandra salamandra) and Sirenidae (Siren intermedia). Sliding landmarks that describe the 14 bones and 19 regions of the cranium used in all shape analyses. From the left to the right: lateral, dorsal and ventral views of the cranium. See colors key in Extended Data Fig. 1.

Extended Data Fig. 4 Phylomorphospace illustrating the first two principal components of cranial shape across Caudata depending on fine-grained classifications of life cycle.

Phylomorphospace illustrating the first two principal components of cranial shape across Caudata. Symbols indicate family-level clade and colours represent fine-grained classifications of life cycle. Abbreviations are as follows: f-bi pd1 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, a tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; f-bi pd4 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; f-bi pd4tri indicates species that are triphasic; pd1 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; pd2 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla, no prefrontal and with maxillary bones developing before adulthood; pd3 indicates paedomorphic species without external gills but with gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; pd4 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; vipu indicates strictly puereparate viviparous species; f-vila indicates facultative larviparate viviparous species; ovi indicates oviparous species.

Extended Data Fig. 5 Phylogenetic principal component on cranial shape depending on life cycle.

Phylomorphospace on skull shape of Caudata. a) Phylomorphospace of the first two phylogenetic principal component scores showing the skull shape distribution of Caudata. b) Phylomorphospace of the second and third phylogenetic principal component scores showing the skull shape distribution of Caudata. Data point shapes are coded by family group and colors represent life cycles, as indicated by the key.

Extended Data Fig. 6 Disparity depending on life cycle and on fine-grained classifications corrected by the number of landmarks per bone.

Disparity per life cycle and on fine-grained classifications corrected by the number of landmarks per bone. Left: analyses were run on the whole data set and excluded the strictly viviparous species for the classification of life cycles. Right: these analyses were run on the whole data set excluding the strictly viviparous (f-vila as n = 2 and vipu as n = 2), oviparous (n = 1) and facultative bipashic pd1(f-bi pd1 as n = 2) species for the classification of life cycles. Abbreviations are as follows: f-bi pd1 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, a tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; f-bi pd4 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; f-bi pd4tri indicates species that are triphasic; pd1 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; pd2 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla, no prefrontal and with maxillary bones developing before adulthood; pd3 indicates paedomorphic species without external gills but with gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; pd4 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; vipu indicates strictly puereparate viviparous species; f-vila indicates facultative larviparate viviparous species; ovi indicates oviparous species.

Extended Data Fig. 7 Evolution of life cycles in Caudata using fine-grained classifications.

Evolution of life cycles in Caudata using fine-grained classifications. Ancestral state estimation using a re-rooting method using the symmetric rate model (best model following results of the AIC, Supplementary Table 5). Abbreviations are as follows: f-bi pd1 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, a tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; f-bi pd4 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; f-bi pd4tri indicates species that are triphasic; pd1 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; pd2 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla, no prefrontal and with maxillary bones developing before adulthood; pd3 indicates paedomorphic species without external gills but with gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; pd4 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; vipu indicates strictly puereparate viviparous species; f-vila indicates facultative larviparate viviparous species; ovi indicates oviparous species.

Extended Data Fig. 8 Rate of evolution per life cycle.

Rate of evolution per life cycle. These analyses were run on the whole data set excluding the strictly viviparous species.

Extended Data Fig. 9 Evolutionary rates and rate shifts for cranial shape in Caudata.

Evolutionary rates and rate shifts for cranial shape in Caudata. Colour gradients on branches indicate the rate of shape evolution with warmer colours corresponding to a higher rate and cooler colours to a lower one. Grey triangles indicate the stem branch of clades with support for whole-clade shifts in evolutionary rate. Posterior probabilities (PP) of rate shifts are indicated by the relative size of the triangles (see Extended Data Fig. 10). Frequencies of the log-transformed rates of cranial shape evolution are indicated by the distribution plot. Rates and shift were estimated using BayesTraitsV3 using a variable-rates Brownian motion model. Times in the tree are indicated in millions of years (Ma). Abbreviations are as follows: f-bi pd1 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, a tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; f-bi pd4 indicates facultative biphasic species, as some populations can be paedomorphic in these species. When they are paedomorphic they display external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; f-bi pd4tri indicates species that are triphasic; pd1 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no maxillary bones, no septomaxilla and no prefrontal; pd2 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla, no prefrontal and with maxillary bones developing before adulthood; pd3 indicates paedomorphic species without external gills but with gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; pd4 indicates paedomorphic species with external gills, gill slits, tail fin, no eyelids, no septomaxilla and with maxillary and prefrontal bones developing before adulthood; vipu indicates strictly puereparate viviparous species; f-vila indicates facultative larviparate viviparous species; ovi indicates oviparous species.

Extended Data Fig. 10 Phylogeny with posterior probabilities (PP) of rate shifts.

Phylogeny with posterior probabilities (PP) of rate shifts.

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Supplementary Figs. 1–6, Tables 1–7 and references.

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Fabre, AC., Bardua, C., Bon, M. et al. Metamorphosis shapes cranial diversity and rate of evolution in salamanders. Nat Ecol Evol 4, 1129–1140 (2020). https://doi.org/10.1038/s41559-020-1225-3

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