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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.

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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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