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Phylogeographic and environmental correlates support the cryptic function of the zigzag pattern in a European viper

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Abstract

The predator–prey relationship is a strong agent of natural selection on phenotype, and two evolutionary strategies derived from this antagonistic interaction are crypsis and aposematism. Although usually considered as opposites, both strategies could be ascribed to the dark zigzag pattern of European vipers (Vipera). Experiments using plasticine models demonstrated its aposematic role, and no evidence had been found regarding a possible cryptic function. We examined the possibility of a cryptic role by measuring five characters related to the zigzag size and shape in 465 Vipera latastei specimens from the Iberian Peninsula to assess geographic variation in these characters. This species shows genetic substructuring resulting from population isolation and occurs in strong environmental gradients, which allows testing whether historic and/or environmental (adaptive) factors explain this variation. Spatial interpolation of zigzag characters identified two major Iberian groups: the Western and the Eastern. The Western group was characterised by a larger zigzag extension and higher number of dorsal marks; specimens within this group were in granitic grounds and areas with higher rainfall and lower solar radiation than those of the Eastern group. The correlation of the zigzag shape and size with lithology and climatic variables suggested that dorsal pattern variation is driven by: (1) its cryptic role, as detectability might be influenced by the degree of contrast between the target and background lithology, or (2) its thermal role, as the larger zigzag may allow for faster heating in Western Iberian regions with limited thermal opportunities. A log-linear analysis using dorsal pattern groups, genetic lineages and lithological classes, showed significant interactions among the three variables. These results suggest that dorsal pattern variation of V. latastei resulted from genetic (i.e. historic) as well as environmental (i.e. adaptive) factors, first by population isolation in geographic refuges and further by local adaptation to particular environments.

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Acknowledgments

We wish to thank the curators of the following institutions for permitting the analysis of preserved Vipera latastei vouchers: Centre d’Ecologie Fonctionnelle et Evolutive (CEFE-CNRS, Montpellier, France), Departament de Biologia Animal at the University of Barcelona (Barcelona, Spain), Departamento de Biología Animal at the University of Salamanca (Salamanca, Spain), Departamento de Zoología at the University of Granada (Granada, Spain), Estación Biológica de Doñana-CSIC (Sevilla, Spain), Instituto Pirenaico de Ecología-CSIC (Jaca, Spain), Monestir de Montserrat (Montserrat, Spain), Museu de História Natural of the Faculdade de Ciências do Porto (Porto, Portugal), Museu Bocage-Museu de História Natural of the Faculdade de Ciências de Lisboa (Lisboa, Portugal), Museo Nacional de Ciencias Naturales-CSIC (Madrid, Spian), and Museu de Zoologia de Barcelona (Barcelona., Spain). We also examined the private collection of J.C. Brito, and pictures from the High Course of Ebro River and Massís del Garraf. We also thank the anonymous reviewers for their useful comments on the first version of the manuscript. This study was partially supported by the project POCTI/BIA-BDE/55596/2004 from Fundação para a Ciência e Tecnologia (FCT, Portugal). Xavier Santos and Fernando Martínez-Freiría are supported by FCT (SFRH/BPD/73176/2010 and SFRH/BPD/69857/2010, respectively), and J.C. Brito by project “Biodiversity, Ecology and Global Change” cofinanced by North Portugal Regional Operational Programme 2007/2013 (ON.2—O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF).

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Authors and Affiliations

  1. CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, R. Padre Armando Quintas, 4485-661, Vairão, Portugal

    Xavier Santos, José C. Brito & Fernando Martínez-Freiría

  2. Dep. Biologia Animal, Univ. Barcelona, Avda. Diagonal 645, 08028, Barcelona, Spain

    Marta Vidal-García & Gustavo A. Llorente

  3. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua Campo Alegre s/n, 4169-007, Porto, Portugal

    José C. Brito

  4. Dép. Biologie, Fac. Sciences, Univ. Abdelmalek Essâadi, Tétouan, Morocco

    Soumia Fahd

  5. Servei de Biodiversitat i Protecció dels Animals, DAAM, Generalitat de Catalunya, 08017, Barcelona, Spain

    Xavier Parellada

  6. Dep. Zoología, Fac. Ciencias, Univ. Granada, 18071, Granada, Spain

    Juan M. Pleguezuelos

  7. Observatório Astronómico Prof. Manuel de Barros, Centro de Investigação em Ciências Geo-Espaciais CICGE, Alameda do Monte da Virgem, 4430-146, Vila Nova de Gaia, Portugal

    Neftalí Sillero

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  1. Xavier Santos
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Correspondence to Xavier Santos.

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Santos, X., Vidal-García, M., Brito, J.C. et al. Phylogeographic and environmental correlates support the cryptic function of the zigzag pattern in a European viper. Evol Ecol 28, 611–626 (2014). https://doi.org/10.1007/s10682-014-9699-6

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