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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
  • 56 Downloads

Abstract

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.

Keywords

Development Geometric morphometrics Head shape Intraspecific diversity Life-history Pueriparity 

Notes

Acknowledgements

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)

References

  1. Adams, D. C. (2010). Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evolutionary Biology,10(1), 72.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adams, D. C., Berns, C. M., Kozak, K. H., & Wiens, J. J. (2009). Are rates of species diversification correlated with rates of morphological evolution? Proceedings of the Royal Society B,276(1668), 2729–2738.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Adams, D. C., Collyer, M. L., Kaliontzopoulou, A., & Sherratt, E. (2017). Geomorph: Software for geometric morphometric analyses. R package version 3.0.5. Retrieved from https://cran.r-project.org/package=geomorph
  4. Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology,10(1), 216.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Adams, D. C., & Otárola-Castillo, E. (2013). geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution,4, 393–399.CrossRefGoogle Scholar
  6. Adams, D. C., & Rohlf, F. J. (2000). Ecological character displacement in Plethodon: Biomechanical differences found from a geometric morphometric study. Proceedings of the National Academy of Sciences,97(8), 4106–4111.CrossRefGoogle Scholar
  7. Adriaens, D., & Verraes, W. (1998). Ontogeny of the osteocranium in the African catfish, Clarias gariepinus Burchell (1822) (Siluriformes: Clariidae): Ossification sequence as a response to functional demands. Journal of Morphology,235(3), 183–237.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Alarcón-Ríos, L., Nicieza, A. G., Kaliontzopoulou, A., Buckley, D., & Velo-Antón, G. (2019). AlarconRiosetal2019_EvolBiol.figshare.  https://doi.org/10.6084/m9.figshare.10392239.v1.
  9. Alarcón-Ríos, L., Velo-Antón, G., & Kaliontzopoulou, A. (2017). A non-invasive geometric morphometrics method for exploring variation in dorsal head shape in urodeles: Sexual dimorphism and geographic variation in Salamandra salamandra. Journal of Morphology,278(4), 475–485.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Alberch, P. (1980). Ontogenesis and morphological diversification. American Zoologist,20(4), 653–667.CrossRefGoogle Scholar
  11. Alberch, P. (1987). Evolution of a developmental process—irreversibility and redudancy in amphibian metamorphosis. In R. A. Raff & E. C. Raff (Eds.), Development as an evolutionary process (pp. 23–46). New York: Alan R. Lissm Inc.Google Scholar
  12. Alberch, P., & Blanco, M. J. (1996). Evolutionary patterns in ontogenetic transformation: From laws to regularities. International Journal of Developmental Biology,40, 845–858.PubMedPubMedCentralGoogle Scholar
  13. Alcobendas, M., & Castanet, J. (2000). Bone growth plasticity among populations of Salamandra salamandra: Interactions between internal and external factors. Herpetologica,56, 14–26.Google Scholar
  14. Antunes, B., Lourenço, A., Caeiro-Dias, G., Dinis, M., Gonçalves, H., Martínez-Solano, I., et al. (2018). Combining phylogeography and landscape genetics to infer the evolutionary history of a short-range Mediterranean relict Salamandra salamandra longirostris. Conservation Genetics,19(6), 1411–1424.CrossRefGoogle Scholar
  15. Arbour, J., & Brown, C. (2014). Incomplete specimens in geometric morphometric analyses. Methods in Ecology and Evolution,5, 16–26.CrossRefGoogle Scholar
  16. Bas, S., & Gasser, F. (1994). Polytypism of Salamandra salamandra (L.) in north-western Iberia. Mertensiella,4, 41–74.Google Scholar
  17. Beukema, W., Nicieza, A. G., Lourenço, A., & Velo-Antón, G. (2016b). Colour polymorphism in Salamandra salamandra (Amphibia: Urodela), revealed by a lack of genetic and environmental differentiation between distinct phenotypes. Journal of Zoological Systematics and Evolutionary Research,54(2), 127–136.CrossRefGoogle Scholar
  18. Beukema, W., Speybroeck, J., & Velo-Antón, G. (2016a). Salamandra. Current Biology,26(15), R696–R697.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Blackburn, D. G. (2015). Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis. Journal of Morphology,276(8), 961–990.PubMedCrossRefPubMedCentralGoogle Scholar
  20. Blankers, T., Adams, D. C., & Wiens, J. J. (2012). Ecological radiation with limited morphological diversification in salamanders. Journal of Evolutionary Biology,25(4), 634–646.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Brodie, E. D. (1983). Antipredator adaptations of salamanders: Evolution and convergence among terrestrial species. In N. S. Margaris, M. Arianoutsou-Faraggitaki, & R. J. Reiter (Eds.), Adaptations to terrestrial environments (pp. 109–133). Boston: Springer.CrossRefGoogle Scholar
  22. Bruce, R. C. (2003). Life histories. In B. Jamieson (Ed.), Reproductive biology and phylogeny of Urodela (Vol. 1, pp. 477–525). New Hampshire: Science Publisher.Google Scholar
  23. Buckley, D., Alcobendas, M., García-París, M., & Wake, M. H. (2007). Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. Evolution & Development,9(1), 105–115.CrossRefGoogle Scholar
  24. Carroll, S. B. (2001). Chance and necessity: The evolution of morphological complexity and diversity. Nature,409(6823), 1102.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Collins, J. P., & Cheek, J. E. (1983). Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum. American Zoologist,23(1), 77–84.CrossRefGoogle Scholar
  26. Collyer, M. L., & Adams, D. C. (2013). Phenotypic trajectory analysis: Comparison of shape change patterns in evolution and ecology. Hystrix, the Italian Journal of Mammalogy,24, 75–83.Google Scholar
  27. Collyer, M. L., Sekora, D., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high- dimensional data. Heredity,115, 357–365.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cvijanović, M., Ivanović, A., Kalezić, M. L., & Zelditch, M. L. (2014). The ontogenetic origins of skull shape disparity in the Triturus cristatus group. Evolution & Development,16(5), 306–317.CrossRefGoogle Scholar
  29. Donaire-Barroso, D., & Rivera, X. (2016). La salamandra común Salamandra salamandra(Linnaeus, 1758) en el subcantábrico: Origen, dispersión, subespeciesy zonas de introgresión. Butlletí Societat Catalana de Herpetología,23, 7–38.Google Scholar
  30. Dopazo, H., & Alberch, P. (1994). Preliminary results on optional viviparity and intrauterine siblicide in Salamandra salamandra populations from Northern Spain. Mertensiella,4, 125–137.Google Scholar
  31. Dryden, I. L., & Mardia, K. V. (2016). Statistical shape analysis, with applications in R (2nd ed.). Chichester: Wiley.CrossRefGoogle Scholar
  32. Duellman, W. E., & Trueb, L. (1986). Biology of amphibians. New York: JHU press.Google Scholar
  33. Frederich, B., Adriaens, D., & Vandewalle, P. (2008). Ontogenetic shape changes in Pomacentridae (Teleostei, Perciformes) and their relationships with feeding strategies: A geometric morphometric approach. Biological Journal of the Linnean Society,95(1), 92–105.CrossRefGoogle Scholar
  34. Galán, P. (2007). Viviparismo y distribución de Salamandra salamandra bernardezi en el norte de Galicia. Boletín de la Asociación Herpetológica Española,18, 44–48.Google Scholar
  35. García-París, M., Alcobendas, M., Buckley, D., & Wake, D. B. (2003). Dispersal of viviparity across contact zones in Iberian populations of fire salamanders (Salamandra) inferred from discordance of genetic and morphological traits. Evolution,57(1), 129–143.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Gomez-Mestre, I., Pyron, R. A., & Wiens, J. J. (2012). Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution,66(12), 3687–3700.  https://doi.org/10.1111/j.1558-5646.2012.01715.x.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge: Harvard University Press.Google Scholar
  38. Greven, H. (2003). Larviparity and pueriparity. In D. M. Sever (Ed.), Reproductive biology and phylogeny of urodela (Amphibia) (pp. 447–475). New Hampshire: Science Publishers.Google Scholar
  39. Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G. W., & Bookstein, F. L. (2009). Principles for the virtual reconstruction of hominin crania. Journal of Human Evolution,57(1), 48–62.  https://doi.org/10.1016/j.jhevol.2009.04.004.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hanken, J. (1989). Development and evolution in amphibians. American Scientist,77(4), 336–343.Google Scholar
  41. Hanken, J. (1999). Larvae in amphibian development and evolution. In B. K. Hall & M. H. Wake (Eds.), The origin and evolution of larval forms (pp. 61–108). Amsterdam: Elsevier.CrossRefGoogle Scholar
  42. Ivanović, A., Cvijanović, M., & Kalezić, M. L. (2011). Ontogeny of body form and metamorphosis: Insights from the crested newts. Journal of Zoology,283(3), 153–161.CrossRefGoogle Scholar
  43. Kaliontzopoulou, A., Carretero, M. A., & Llorente, G. A. (2012). Morphology of the Podarcis wall lizards (Squamata: Lacertidae) from the Iberian Peninsula and North Africa: Patterns of variation in a putative cryptic species complex. Zoological Journal of the Linnean Society,164(1), 173–193.CrossRefGoogle Scholar
  44. Kapralova, K. H., Jónsson, Z. O., Palsson, A., Franzdóttir, S. R., le Deuff, S., Kristjánsson, B. K., et al. (2015). Bones in motion: Ontogeny of craniofacial development in sympatric arctic charr morphs. Developmental Dynamics,244(9), 1168–1178.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Kleinteich, T. (2010). Ontogenetic differences in the feeding biomechanics of oviparous and viviparous caecilians (Lissamphibia: Gymnophiona). Zoology,113(5), 283–294.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Koyabu, D., & Son, N. T. (2014). Patterns of postcranial ossification and sequence heterochrony in bats: Life histories and developmental trade-offs. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution,322(8), 607–618.CrossRefGoogle Scholar
  47. Labus, N., Cvijanović, M., & Vukov, T. D. (2013). Sexual size and shape dimorphism in Salamandra salamandra (Amphibia, Caudata, Salamandridae) from the central Balkans. Archives of Biological Sciences,65, 969–975.CrossRefGoogle Scholar
  48. Levis, N. A., de la Serna Buzón, S., & Pfennig, D. W. (2015). An inducible offense: Carnivore morph tadpoles induced by tadpole carnivory. Ecology and Evolution,5(7), 1405–1411.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lourenço, A., Álvarez, D., Wang, I. J., & Velo-Antón, G. (2017). Trapped within the city: Integrating demography, time since isolation and population-specific traits to assess the genetic effects of urbanization. Molecular Ecology,26(6), 1498–1514.  https://doi.org/10.1111/mec.14019.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lourenço, A., Antunes, B., Wang, I. J., & Velo-Antón, G. (2018). Fine-scale genetic structure in a salamander with two reproductive modes: Does reproductive mode affect dispersal? Evolutionary Ecology,32(6), 699–732.  https://doi.org/10.1007/s10682-018-9957-0.CrossRefGoogle Scholar
  51. Lourenço, A., Gonçalves, J., Carvalho, F., Wang, I. J., & Velo-Antón, G. (2019). Comparative landscape genetics reveals the evolution of viviparity reduces genetic connectivity in fire salamanders. Molecular Ecology,28(20), 4573–4591.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Manenti, R., Perreau, L., Ficetola, G. F., & Mangiacotti, M. (2018). Effects of diet quality on morphology and intraspecific competition ability during development: The case of fire salamander larvae. European Zoological Journal,85(1), 322–331.  https://doi.org/10.1080/24750263.2018.1501103.CrossRefGoogle Scholar
  53. McKinney, M. L. (1988). Heterochrony in evolution. In M. McKinney (Ed.), Heterochrony in evolution (pp. 327–340). New York: Springer.CrossRefGoogle Scholar
  54. McNamara, K. J., & McKinney, M. L. (2005). Heterochrony, disparity, and macroevolution. Paleobiology,31(S2), 17–26.CrossRefGoogle Scholar
  55. Moran, N. A. (1994). Adaptation and constraint in the complex life cycles of animals. Annual Review of Ecology and Systematics,25(1), 573–600.CrossRefGoogle Scholar
  56. Pereira, R. J., Martínez-Solano, I., & Buckley, D. (2016). Hybridization during altitudinal range shifts: Nuclear introgression leads to extensive cyto-nuclear discordance in the fire salamander. Molecular Ecology,25(7), 1551–1565.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Pfennig, D. (1990). The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia,85(1), 101–107.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology & Evolution,25(8), 459–467.CrossRefGoogle Scholar
  59. R Development Core Team. (2016). R: A language and environ- ment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  60. Rohlf, F. J. (1999). Shape statistics: Procrustes superimpositions and tangent spaces. Journal of Classification,16(2), 197–223.CrossRefGoogle Scholar
  61. Rohlf, F. J. (2015). TpsDig2, digitize landmarks and outlines [software version 2.20]. State University of New York.Google Scholar
  62. Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology,39, 40–59.Google Scholar
  63. Sears, K. E. (2014). Quantifying the impact of development on phenotypic variation and evolution. Journal of Experimental Biology Part B,322B, 643–653.  https://doi.org/10.1002/.22592.CrossRefGoogle Scholar
  64. Sherratt, E., Vidal-García, M., Anstis, M., & Keogh, J. S. (2017). Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nature Ecology & Evolution,1(9), 1385.CrossRefGoogle Scholar
  65. Smith, F. J., Percival, C. J., Young, N. M., Hu, D., Schneider, R. A., Marcucio, R. S., et al. (2015). Divergence of craniofacial developmental trajectories among avian embryos. Developmental Dynamics,244(9), 1158–1167.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Smith, K. K. (2003). Time’s arrow: Heterochrony and the evolution of development. International Journal of Developmental Biology,47(7–8), 613–621.PubMedPubMedCentralGoogle Scholar
  67. Smith, T. B., & Skúlason, S. (1996). Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annual Review of Ecology and Systematics,27(1), 111–133.CrossRefGoogle Scholar
  68. Steinfartz, S., Veith, M., & Tautz, D. (2000). Mitochondrial sequence analysis of Salamandra taxa suggests old splits of major lineages and postglacial recolonizations of Central Europe from distinct source populations of Salamandra salamandra. Molecular Ecology,9, 397–410.PubMedCrossRefPubMedCentralGoogle Scholar
  69. Turner, C. H. (1998). Three rules for bone adaptation to mechanical stimuli. Bone,23(5), 399–407.PubMedCrossRefPubMedCentralGoogle Scholar
  70. Uotila, E., Díaz, A. C., Azkue, I. S., & Rubio Pilarte, X. (2013). Variation in the reproductive strategies of Salamandra salamandra (Linnaeus, 1758) populations in the province of Gipuzkoa (Basque Country). Munibe Ciencias Naturales Natur zientziak,61, 91–101.Google Scholar
  71. Urošević, A., Ljubisavljević, K., & Ivanović, A. (2013). Patterns of cranial ontogeny in lacertid lizards: Morphological and allometric disparity. Journal of Evolutionary Biology,26(2), 399–415.PubMedCrossRefPubMedCentralGoogle Scholar
  72. Velo-Antón, G., & Buckley, D. (2015). Salamandra común–Salamandra salamandra. Enciclopedia Virtual de los Vertebrados Españoles 2–12. Madrid: Museo Nacional de Ciencias Naturales.Google Scholar
  73. Velo-Antón, G., & Cordero-Rivera, A. (2017). Ethological and phenotypic divergence in insular fire salamanders: Diurnal activity mediated by predation? Acta Ethologica,20(3), 243–253.  https://doi.org/10.1007/s10211-017-0267-2.CrossRefGoogle Scholar
  74. Velo-Antón, G., García-París, M., Galán, P., & Cordero-Rivera, A. (2007). The evolution of viviparity in holocene islands: Ecological adaptation versus phylogenetic descent along the transition from aquatic to terrestrial environments. Journal of Zoological Systematics and Evolutionary Research,45(4), 345–352.CrossRefGoogle Scholar
  75. Velo-Antón, G., Santos, X., Sanmartín-Villar, I., Cordero-Rivera, A., & Buckley, D. (2015). Intraspecific variation in clutch size and maternal investment in pueriparous and larviparous Salamandra salamandra females. Evolutionary Ecology,29(1), 185–204.CrossRefGoogle Scholar
  76. Velo-Antón, G., Zamudio, K. R., & Cordero-Rivera, A. (2012). Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra). Heredity,108(4), 410.PubMedCrossRefPubMedCentralGoogle Scholar
  77. Vučić, T., Sibinović, M., Vukov, T. D., Tomašević Kolarov, N., Cvijanović, M., & Ivanović, A. (2019). Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape in Triturus newts. Evolution,73(6), 1253–1264.PubMedCrossRefPubMedCentralGoogle Scholar
  78. Wainwright, P. C., & Reilly, S. M. (1994). Ecological morphology: Integrative organismal biology. Chicago: University of Chicago Press.Google Scholar
  79. Wake, D. B., & Hanken, J. (1996). Direct development in the lungless salamanders: What are the consequences for developmental biology, evolution and phylogenesis? International Journal of Developmental Biology,40(4), 859–869.PubMedPubMedCentralGoogle Scholar
  80. Wake, D. B., Wake, M. H., & Specht, C. D. (2011). Homoplasy: From detecting pattern and mechanism of evolution. Science,331(6020), 1032–1035.  https://doi.org/10.1126/science.1188545.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wake, M. H. (2003). Reproductive modes, ontogenies, and the evolution of body form. Animal Biology,53, 209–224.CrossRefGoogle Scholar
  82. Wake, M. H. (2015). Fetal adaptations for viviparity in amphibians. Journal of Morphology,276(8), 941–960.PubMedCrossRefPubMedCentralGoogle Scholar
  83. Wake, M. H., & Hanken, J. (1982). Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. Journal of Morphology,173(2), 203–223.PubMedCrossRefPubMedCentralGoogle Scholar
  84. Wells, K. D. (2007). The ecology and behavior of amphibians. Chicago: University of Chicago Press.CrossRefGoogle Scholar
  85. West-Eberhard, M. (2003). Developmental plasticity and evolution. Oxford, UK: Oxford University Press.Google Scholar
  86. West-Eberhard, M. J. (2005). Phenotypic acommodation: Adaptive innovation due to developmental plasticity. Journal of Experimental Zoology Part B,304(6), 610.CrossRefGoogle Scholar
  87. Wimberger, P. H. (1994). Trophic polymorphisms, plasticity, and speciation in vertebrates. In D. J. Stouder, K. L. Fresh, R. J. Feller, & B. W. Baruch (Eds.), Theory and application in fish feeding ecology (pp. 19–43). Columbia: University o South Carolina Press.Google Scholar

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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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