Population structure of the oviparous South-West European common lizard

  • Jose Luis Horreo
  • María Luisa Peláez
  • Merel C. Breedveld
  • Teresa Suárez
  • María Urieta
  • Patrick S. Fitze
Original Article


Gene flow is an important factor determining the evolution of a species, since it directly affects population structure and species’ adaptation. Here, we investigated population structure, population history, and migration among populations covering the entire distribution of the geographically isolated South-West European common lizard (Zootoca vivipara louislantzi) using 34 newly developed polymorphic microsatellite markers. The analyses unravelled the presence of isolation by distance, inbreeding, recent bottlenecks, genetic differentiation, and low levels of migration among most populations, suggesting that Z. vivipara louislantzi is threatened. The results point to discontinuous populations and are in line with physical barriers hindering longitudinal migration south to the central Pyrenean cordillera and latitudinal migration in the central Pyrenees. In contrast, evidence for longitudinal migration exists from the lowlands north to the central Pyrenean cordillera and the Cantabrian Mountains. The locations of the populations south to the central Pyrenean cordillera were identified as the first to be affected by global warming; thus, management actions aimed at avoiding population declines should start in this area.


Climate change Conservation First-generation migrant, gene flow IBD Zootoca vivipara 



J.L.H. was supported by both a EU Marie Curie-Clarín CoFund grant (ACA14-26) and the Spanish Ministry of Economy and Competitiveness postdoc grants FPDI-2013-16116 and IJCI-2015-23618. Project funds were provided by the Swiss National Science Foundation (PPOOP3_128375, PP00P3_152929/1 to P.S.F.) and the Spanish Ministry of Education and Science (CGL2008-01522, CGL2012-32459, CGL2016-76918 to P.S.F.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709CrossRefGoogle Scholar
  2. Anderson BJ, Akçakaya HR, M.B Araújo MB, Fordham DA, Martinez-Meyer E, Thuiller W, Brook BW (2009) Dynamics of range margins for metapopulations under climate change. Proceedings of the Royal Society B: Biological Sciences, 276:1415–1420Google Scholar
  3. Aragon P, Fitze PS (2014) Geographical and temporal body size variation in a reptile: roles of sex, ecology, phylogeny and ecology structured in phylogeny. PLoS One 9:e104026CrossRefGoogle Scholar
  4. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, MontpellierGoogle Scholar
  5. Bestion E, Clobert J, Cote J (2015) Dispersal response to climate change: scaling down to intraspecific variation. Ecol Lett 18:1226–1233CrossRefGoogle Scholar
  6. Bretman A, Rodríguez-Muñoz R, Waklling C, Slate J, Tregenza T (2011) Fine-scale population structure, inbreeding risk and avoidance in a wild insect population. Mol Ecol 20:3045–3055CrossRefGoogle Scholar
  7. Cornetti L, Belluardo F, Ghielmi S, Giovine G, Ficetola GF, Bertorelee G, Vernesi C, Hauffe HC (2015) Reproductive isolation between oviparous and viviparous lineages of the Eurasian common lizard Zootoca vivipara in a contact zone. Biol J Linn Soc 114:566–573CrossRefGoogle Scholar
  8. Cote J, Clobert J, Fitze PS (2007) Mother-offspring competition promotes colonization success. Proc Natl Acad Sci U S A 104:9703–9708CrossRefGoogle Scholar
  9. Cotto O, Massot M, Ronce O, Clobert J (2015) Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards. Proc R Soc B Biol Sci 282:20151741CrossRefGoogle Scholar
  10. Coulon A et al (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach. Mol Ecol 13:2841–2850CrossRefGoogle Scholar
  11. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  12. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  13. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578CrossRefGoogle Scholar
  14. Fitze PS, Le Galliard JF (2008) Operational sex ratio, sexual conflict and the intensity of sexual selection. Ecol Lett 11:432–439CrossRefGoogle Scholar
  15. Fitze PS, Cote J, Clobert J (2010) Mating order-dependent female mate choice in the polygynandrous common lizard. Lacerta vivipara. Oecologia 162:331–341CrossRefGoogle Scholar
  16. Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443CrossRefGoogle Scholar
  17. Garza J, Williamson E (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefGoogle Scholar
  18. Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13:2481–2490CrossRefGoogle Scholar
  19. Horreo JL, Fitze PS (2015) Population structure of three Psammodromus species in the Iberian Peninsula. PeerJ 3:e994CrossRefGoogle Scholar
  20. Horreo JL, Machado-Schiaffino G, Ayllon F, Griffiths AM, Bright D, Stevens JR, Garcia-Vazquez E (2011) Impact of climate change and human-mediated introgression on south European Atlantic salmon populations. Glob Chang Biol 17:1778–1787Google Scholar
  21. Horreo JL, Machado-Schiaffino G, Griffiths AM, Bright D, Stevens JR, Garcia-Vazquez E (2014) Long-term effects of stock transfers: synergistic introgression of allochthonous genomes in salmonids. J Fish Biol 85:292–306CrossRefGoogle Scholar
  22. Horreo JL, Peláez ML, Suárez T, Heulin B, Fitze PS (2017) Development of thirty-four new microsatellite loci and multiplexing of seven existing loci for Zootoca vivipara. Phyllomedusa 16:89–96CrossRefGoogle Scholar
  23. Horreo JL, Pelaez ML, Suárez T, Breedveld MC, Heulin B, Surget-Groba Y, Oksanen TA, Fitze PS (2018) Phylogeography, evolutionary history, and effects of glaciations in a species (Zootoca vivipara) inhabiting multiple biogeographic regions. J Biogeogr in press 45:1616–1627CrossRefGoogle Scholar
  24. Horváthová T, Cooney CR, Fitze PS, Oksanen TA, Jelić D, Ghira I, Uller T, Jandzik D (2013) Length of activity season drives geographic variation in body size of a widely distributed lizard. Ecol Evol 3:2424–2442CrossRefGoogle Scholar
  25. Le Galliard JF, Fitze PS, Cote J, Massot M, Clobert J (2005) Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio. J Evol Biol 18:1455–1463CrossRefGoogle Scholar
  26. Li YL, Liu JX (2018) StructureSelector: a web based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour 18:176–177CrossRefGoogle Scholar
  27. Merimans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  28. Mieszkowska N, Hawkins SJ, Burrows M, Kendall M (2007) Long-term changes in the geographic distribution and population structures of Osilinus lineatus (Gastropoda: Trochidae) in Britain and Ireland. J Mar Biol Assoc U K 87:537–545Google Scholar
  29. Mila B, Surget-Groba Y, Heulin B, Gosá A, Fitze PS (2013) Multilocus phylogeography of the common lizard Zootoca vivipara at the Ibero-Pyrenean suture zone reveals lowland barriers and high-elevation introgression. BMC Evol Biol 13:192CrossRefGoogle Scholar
  30. Munday PL, Leis, JM, Lough, JM, Paris-Limouzy, CB, Kingsford, MJ, Berumen, ML, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395Google Scholar
  31. Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65CrossRefGoogle Scholar
  32. Peñalver-Alcázar M, Aragon P, Breedvled MC, Fitze PS (2016) Microhabitat selection in the common lizard: implications of biotic interactions, age, sex, local processes and model transferability among populations. Ecol Evol 6:3594–3607CrossRefGoogle Scholar
  33. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  34. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefGoogle Scholar
  35. Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627CrossRefGoogle Scholar
  36. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci U S A 94:9197–9201CrossRefGoogle Scholar
  37. Recknagel H, Kamenos N, Elmer KR (2018) Common lizards break Dollo's law of irreversibility: genome-wide phylogenomics support a single origin of viviparity and re-evolution of oviparity. Mol Phylogenet Evol 127:579–588CrossRefGoogle Scholar
  38. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  39. San-Jose LM, Peñalver-Alcázar M, Milá B, Gonzalez-Jimena V, Fitze PS (2014) Cumulative frequency-dependent selective episodes allow for rapid morph cycles and rock-paper-scissors dynamics in species with overlapping generations. Proc R Soc B Biol Sci 281:20140976CrossRefGoogle Scholar
  40. Sharma S, Dutta T, Maldonado JE, Wood TC, Panwar HS, Seidensticker J (2013) Forest corridors maintain historical gene flow in a tiger metapopulation in the highlands of Central India. Proc R Soc B Biol Sci 280:20131506. CrossRefGoogle Scholar
  41. Sinervo B, Mendez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagran-Santa Cruz M, Lara-Resendiz R, Martinez-Mendez N, Calderon-Espinosa ML, Meza-Lazaro RN, Gadsden H, Avila LJ, Morando M, de la Riva IJ, Sepulveda PV, Rocha CFD, Ibarguengoytia N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899CrossRefGoogle Scholar
  42. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefGoogle Scholar
  43. Surget-Groba Y et al (2006) Multiple origins of viviparity, or reversal from viviparity to oviparity? The European common lizard (Zootoca vivipara, Lacertidae) and the evolution of parity. Biol J Linn Soc 87:1–11CrossRefGoogle Scholar
  44. Tobler M, Riesch R, Tobler CM, Schulz-Mirbach T, Plath M (2009) Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations. J Evol Biol 22:2298–2304CrossRefGoogle Scholar
  45. Van Oosterhout C, hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in micrsaotellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Ecology and Evolution (DEE)University of LausanneLausanneSwitzerland
  2. 2.Department of Biodiversity and Evolutionary BiologyMuseo Nacional de Ciencias Naturales (MNCN-CSIC)MadridSpain
  3. 3.Department of Cellular and Molecular PhysiopathologyCentro de Investigaciones Biologicas (CSIC)MadridSpain
  4. 4.Animal EcologyUniversity of PotsdamPotsdamGermany

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