Evolutionary History and Not Heterochronic Modifications Associated with Viviparity Drive Head Shape Differentiation in a Reproductive Polymorphic Species, Salamandra salamandra

  • Lucía Alarcón-RíosEmail author
  • Alfredo G. Nicieza
  • Antigoni Kaliontzopoulou
  • David Buckley
  • Guillermo Velo-AntónEmail author
Research Article


Identifying the evolutionary processes that underlie morphological variation at the intraspecific level is cornerstone for understanding the drivers of phenotypic diversity at higher macro-evolutionary scales. The fire salamander, Salamandra salamandra, exhibits exceptional intraspecific variation in multiple phenotypic traits (i.e. body size, head shape, coloration, reproductive modes). Pueriparity (females laying fully metamorphosed juveniles) in S. salamandra entails modifications during embryonic development in comparison to larviparity (females laying aquatic larvae), which is the ancestral reproductive mode. These heterochronic modifications involve a general acceleration of development and mainly focus on cephalic structures to facilitate intrauterine active feeding, which might impact head shape in the adult stage. In the present study, we (i) describe the main features of head shape variation in adults of the two distinct subspecies of Salamandra salamandra that independently evolved to pueriparity, and (ii) explore the morphological consequences of developmental and functional changes related to this major evolutionary shift. Our results show that evolutionary history, and not reproductive mode, is the main driver of head shape variation in S. salamandra. These results suggest different evolutionary processes acting differentially on each subspecies, at least at the adult stage. The present study highlights the importance of comparative studies integrating evolutionary histories and ontogenetic trajectories to explore the different sources of observed morphological diversification.


Development Geometric morphometrics Head shape Intraspecific diversity Life-history Pueriparity 



We are thankful to G. Palomar, R. Álvarez and A. Cordero-Rivera for their help and assistance during fieldwork. We also thank all the employees of the National Park that facilitated our trips to the islands. This work is funded by the Ministerio de Economía y Competitividad (Grants Nos. CGL2012-40246-C02-02 and CGL2017-86924-P); by FEDER funds through the Operational Programme for Competitiveness Factors – COMPETE (FCOMP-01-0124-FEDER-028325 and POCI-01- 0145-FEDER-006821); and by National Funds through FCT – Foundation for Science and Technology (EVOVIV: PTDC/BIA-EVF/3036/2012; SALOMICS: PTDC/BIA-EVL/28475/2017). L.A.-R. was supported by a FPU grant (FPU14/03015) from the Ministerio de Educación, Cultura y Deporte (MECD, Spain) and and G.V.-A. and A.K. by IF contracts (IF/01425/2014 and IF/00641/2014, respectively). from Fundação para a Ciência e a Tecnologia (FCT, Portugal). All applicable national and institutional guidelines for the care and use of animals were followed.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11692_2019_9489_MOESM1_ESM.pdf (859 kb)
Supplementary file1 (PDF 858 kb)


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Authors and Affiliations

  1. 1.Departamento de Biología de Organismos y Sistemas, Área de EcologíaUniversidad de OviedoOviedoSpain
  2. 2.Unidad Mixta de Investigación en Biodiversidad (UMIB), CSIC-Universidad de Oviedo-Principado de AsturiasOviedoSpain
  3. 3.CIBIO/InBIO, Centro de Investigacão em Biodiversidade e Recursos Genéticos, Instituto de Ciências Agrárias de Vairão 7Universidade Do PortoVairãoPortugal
  4. 4.Departamento de Biodiversidad y Biología EvolutivaMuseo Nacional de Ciencias Naturales MNCN-CSICMadridSpain
  5. 5.Departamento de Biología (Unidad de Genética)Universidad Autónoma de Madrid (UAM)MadridSpain
  6. 6.Centro de Investigaciones en Biodiversidad y Cambio Global CIBC-UAM, Facultad de CienciasUniversidad Autónoma de MadridMadridSpain

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