Skip to main content

Advertisement

SpringerLink
Log in

The role of landscape and history on the genetic structure of peripheral populations of the Near Eastern fire salamander, Salamandra infraimmaculata, in Northern Israel

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Genetic studies on core versus peripheral populations have yielded many patterns. This diversity in genetic patterns may reflect diversity in the meaning of “peripheral populations” as defined by geography, gene flow patterns, historical effects, and ecological conditions. Populations at the lower latitude periphery of a species’ range are of particular concern because they may be at increased risk for extinction due to global climate change. In this work we aim to understand the impact of landscape and ecological factors on different geographical types of peripheral populations with respect to levels of genetic diversity and patterns of local population differentiation. We examined three geographical types of peripheral populations of the endangered salamander, Salamandra infraimmaculata, in Northern Israel, in the southernmost periphery of the genus Salamandra, by analyzing the variability in 15 microsatellite loci from 32 sites. Our results showed that: (1) genetic diversity decreases towards the geographical periphery of the species’ range; (2) genetic diversity in geographically disjunct peripheral areas is low compared to the core or peripheral populations that are contiguous to the core and most likely affected by a founder effect; (3) ecologically marginal conditions enhance population subdivision. The patterns we found lead to the conclusion that genetic diversity is influenced by a combination of geographical, historical, and ecological factors. These complex patterns should be addressed when prioritizing areas for conservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data Accessibility

The full microsatellite genotypeing data can be found at: http://spatialepidemiologylab.weebly.com/data.html.

References

  • Bar-David S, Segev O, Peleg N et al (2007) Long-distance movements by Fire Salamanders (Salamandra infraimmaculata) and implications for habitat fragmentation. Israel Journal of Ecology and Evolution 53:143–159

    Article  Google Scholar 

  • Blank L, Blaustein L (2012) Using ecological niche modeling to predict the distributions of two endangered amphibian species in aquatic breeding sites. Hydrobiologia 693:157–167

    Article  Google Scholar 

  • Blank L, Blaustein L (2014) A multi-scale analysis of breeding site characteristics of the endangered fire salamander (Salamandra infraimmaculata) at its extreme southern range limit. Hydrobiologia 726:229–244

    Article  Google Scholar 

  • Blank L, Sinai I, Bar-David S et al (2013) Genetic population structure of the endangered fire salamander (Salamandra infraimmaculata) at the southernmost extreme of its distribution. Anim Conserv 16:412–421

    Article  Google Scholar 

  • Blaustein L, Segev O, Rovelli V et al (2017) Compassionate approaches for the conservation and protection of fire salamanders. Israel Journal of Ecology and Evolution 63:43–51

    Article  Google Scholar 

  • Bogaerts S, Sparreboom M, Pasmans F et al (2013) Distribution, ecology and conservation of Ommatotriton vittatus and Salamandra infraimmaculata in Syria. Salamandra 49:87–96

    Google Scholar 

  • Brussard PF (1984) Geographic patterns and environmental gradients: the central-marginal model in Drosophila revisited. Ann Rev Ecol Syst 15:25–64

    Article  Google Scholar 

  • Cahill AE, Aiello-Lammens ME, Fisher-Reid MC et al (2013) How does climate change cause extinction? Proc R Soc B-Biol Sci 280(1750):20121890

    Article  Google Scholar 

  • Carson HL (1955) The genetic characteristics of marginal populations of Drosophila. Cold Spring Harb Symp Quant Biol 20:276–287

    Article  CAS  PubMed  Google Scholar 

  • Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Chesser RK, Smith MH, Brisbin IL Jr. (1980) Management and maintenance of genetic variability in endangered species. Int Zoo Yearb 20:146–154

    Article  Google Scholar 

  • Chesser RK, Rhodes OE, Sugg DW, Schnabel A (1993) Effective sizes for subdivided populations. Genetics 135:1221–1232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorchin A, Shanas U (2010) Assessment of pollution in road runoff using a Bufo viridis biological assay. Environ Pollut 158:3626–3633

    Article  CAS  PubMed  Google Scholar 

  • Dubey S, Pike DA, Shine R (2013) Predicting the impacts of climate change on genetic diversity in an endangered lizard species. Clim Change 117:319–327

    Article  Google Scholar 

  • Duncan SI, Crespi EJ, Mattheus NM, Rissler LJ (2015) History matters more when explaining genetic diversity within the context of the core-periphery hypothesis. Mol Ecol 24:4323–4336

    Article  PubMed  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Elith J, Phillips SJ, Hastie T et al (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14(1):21

    Article  Google Scholar 

  • Garriga N, Santos X, Montori A et al (2012) Are protected areas truly protected? The impact of road traffic on vertebrate fauna. Biodivers Conserv 21:2761–2774

    Article  Google Scholar 

  • Gaston KJ (2003) The structure and dynamics of geographic ranges. Oxford University Press, Oxford

    Google Scholar 

  • Givati A, Rosenfeld D (2013) The Arctic Oscillation, climate change and the effects on precipitation in Israel. Atmos Res 132:114–124

    Article  Google Scholar 

  • Goldberg T, Nevo E, Degani G (2011) Genetic diverseness and different ecological conditions in Salamandra infraimmaculata larvae from various breeding sites. Anim Biol J 2:37–49

    Google Scholar 

  • Gorodkov KB (1986) Three-dimensional climatic model of potential range and some of its characteristics. II. Entomol Rev 65:1–18

    Google Scholar 

  • Greenbaum G, Templeton AR, Zarmi Y, Bar-David S (2014) Allelic richness following population founding events—a stochastic modeling framework incorporating gene flow and genetic drift. PLoS ONE 9:e115203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenbaum G, Templeton AR, Bar-David S (2016) Inference and analysis of population structure using genetic data and network theory. Genetics 202:1299–1312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths RA, Sewell D, McCrea RS (2010) Dynamics of a declining amphibian metapopulation: survival, dispersal and the impact of climate. Biol Conserv 143:485–491

    Article  Google Scholar 

  • Haan SS, Desmond MJ, Gould WR, Ward JP (2007) Influence of habitat characteristics on detected site occupancy of the New Mexico endemic Sacramento Mountains Salamander, Aneides hardii. J Herpetol 41:1–8

    Article  Google Scholar 

  • Hall JK, Schwartz E, Cleave RL (2013) The Israeli DTM (digital terrain map) project. Microcomput Appl Geol 2:111–118

    Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467

    Article  PubMed  Google Scholar 

  • Hardy R (1945) The influence of types of soil upon the local distribution of some mammals in southwestern Utah. Ecol Monogr 15:71–108

    Article  Google Scholar 

  • Harless ML, Huckins CJ, Grant JB, Pypker TG (2011) Effects of six chemical deicers on larval wood frogs (Rana sylvatica). Environ Toxicol Chem 30:1637–1641

    Article  CAS  PubMed  Google Scholar 

  • Hartel T, Nemes S, Demeter L, Ollerer K (2008) Pond and landscape characteristics—which is more important for common toads (Bufo bufo)? A case study from central Romania. Appl Herpetol 5:1–12

    Article  Google Scholar 

  • Hendrix R, Hauswaldt JS, Veith M, Steinfartz S (2010) Strong correlation between cross-amplification success and genetic distance across all members of ‘True Salamanders’ (Amphibia: Salamandridae) revealed by Salamandra salamandra-specific microsatellite loci. Mol Ecol Resour 10:1038–1047

    Article  CAS  PubMed  Google Scholar 

  • Hernandez PA, Franke I, Herzog SK et al (2008) Predicting species distributions in poorly-studied landscapes. Biodivers Conserv 17:1353–1366

    Article  Google Scholar 

  • Hocking DJ, Connette GM, Conner CA et al (2013) Effects of experimental forest management on a terrestrial, woodland salamander in Missouri. For Ecol Manag 287:32–39

    Article  Google Scholar 

  • Hoffmann AA, Blows MW (1994 ) Species borders: ecological and evolutionary perspectives. Trends In Evol Ecol 9:223–237

    Article  CAS  Google Scholar 

  • Holt RD, Keitt TH (2005) Species’ borders: a unifying theme in ecology. Oikos 108:3–6

    Article  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914

    Article  PubMed  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632

    Article  CAS  PubMed  Google Scholar 

  • Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342

    Article  Google Scholar 

  • Kershenbaum A, Blank L, Sinai I et al (2014) Landscape influences on dispersal behaviour: a theoretical model and empirical test using the fire salamander, Salamandra infraimmaculata. Oecologia 175:509–520

    Article  PubMed  Google Scholar 

  • Larson A (1984) Neontological inferences of evolutionary pattern and process in the salamander family Plethodontidae. Evol Biol 17:119–217

    Article  Google Scholar 

  • Larson A, Wake DB, Yanev KP (1984) Measuring gene flow among populations having high levels of genetic fragmentation. Genetics 106:293–308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leshner A, Ramon O (2013) The Israeli mapping guide for Mediterranean vegetation. Ministry of the Environment, Kharkov

    Google Scholar 

  • Levin N, Harari-Kremer R, Carmel Y (2011) Remote sensing of Israel’s Natural Habitats. Unpublished Report for the Israeli Nature and Parks Authority, Jerusalem

    Google Scholar 

  • Mac Nally R, Horrocks GFB, Lada H (2017) Anuran responses to pressures from high-amplitude drought-flood-drought sequences under climate change. Clim Change 141:243–257

    Article  Google Scholar 

  • Manenti R, Ficetola GF, De Bernardi F (2009) Water, stream morphology and landscape: complex habitat determinants for the fire salamander Salamandra salamandra. Amphibia-Reptilia 30:7–15

    Article  Google Scholar 

  • Navarro-Cerrillo RM, Hernandez-Bermejo JE, Hernandez-Clemente R (2011) Evaluating models to assess the distribution of Buxus balearica in southern Spain. Appl Veg Sci 14:256–267

    Article  Google Scholar 

  • Nevo E (1998) Genetic diversity in wild cereals—regional and local studies and their bearing on conservation ex situ and in situ. Genet Resour Crop Evol 45:355–370

    Article  Google Scholar 

  • O’Donnell KM, Thompson FR, Semlitsch RD (2014) Predicting variation in microhabitat utilization of terrestrial salamanders. Herpetologica 70:259–265

    Article  Google Scholar 

  • Peleg N (2009) Studies on the conservation of the fire salamander (Salamander Infraimmaculata) in Israel. University of Haifa, Haifa

    Google Scholar 

  • Perez MF, Franco FF, Bombonato JR et al (2018) Assessing population structure in the face of isolation by distance: are we neglecting the problem? Divers Distrib 24:1883–1889

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259

    Article  Google Scholar 

  • Pironon S, Papuga G, Villellas J et al (2017) Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol Rev 92:1877–1909

    Article  PubMed  Google Scholar 

  • Pisa G, Orioli V, Spilotros G et al (2015) Detecting a hierarchical genetic population structure: the case study of the Fire Salamander (Salamandra salamandra) in Northern Italy. Ecol Evol 5:743–758

    Article  PubMed  PubMed Central  Google Scholar 

  • Ray N, Lehmann A, Joly P (2002) Modeling spatial distribution of amphibian populations: a GIS approach based on habitat matrix permeability. Biodivers Conserv 11:2143–2165

    Article  Google Scholar 

  • Rosenberg MS, Anderson CD (2011) PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Met Ecol Evol 2:229–232

    Article  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Roy DP, Wulder MA, Loveland TR et al (2014) Landsat-8: science and product vision for terrestrial global change research. Remote Sens Environ 145:154–172

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000. A software for population genetics data analysis Genetics and Biometry Laboratory, University of Geneva, Switzerland

  • Segev O, Polevikove A, Blank L et al (2015) Effects of tail clipping on larval performance and tail regeneration rates in the Near Eastern Fire Salamander, Salamandra infraimmaculata. PloS one 10:e0128077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segev O, Hill N, Templeton AR, Blaustein L (2010) Population size, structure and phenology of an endangered salamander at temporary and permanent breeding sites. J Nat Conserv 18:189–195

    Article  Google Scholar 

  • Semlitsch RD, Anderson TL (2016) Structure and dynamics of Spotted Salamander (Ambystoma maculatum) populations in Missouri. Herpetologica 72:81–89

    Article  Google Scholar 

  • Sepulveda AJ, Lowe WH (2009) Local and landscape-scale influences on the occurrence and density of Dicamptodon aterrimus, the Idaho Giant Salamander. J Herpetol 43:469–484

    Article  Google Scholar 

  • 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. Mol Ecol 9:397–410

    Article  CAS  PubMed  Google Scholar 

  • Steinfartz S, Kusters D, Tautz D (2004) Isolation and characterization of polymorphic tetranucleotide microsatellite loci in the fire salamander Salamandra salamandra (Amphibia: Caudata). Mol Ecol Notes 4:626–628

    Article  CAS  Google Scholar 

  • Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293

    Article  CAS  PubMed  Google Scholar 

  • Templeton AR, Routman E, Phillips C (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the Tiger Salamander, Ambystoma tigrinum. Genetics 140:767–782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker CJ (1979) Red and photographic infrared linear combinations for monitoring vegetation. Remote Sens Environ 8:127–150

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vucetich JA, Waite TA (2003) Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics. Conserv Genet 4:639–645

    Article  Google Scholar 

  • Warburg MR (2011) Changes in recapture rate of a rare salamander in an isolated metapopulation studied for 25 years. Rus J Herpetol 15:11–18

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was funded by ISF Grant No. 961-2008 awarded to Leon Blaustein, German-Israel Project BL 1271/1-1 awarded to Leon Blaustein and Alan R. Templeton and STE 1130/8-1 awarded to Sebastian Steinfartz and Arne Nolte and Grant Nos. 129662 and 134728 from the Academy of Finland awarded to Juha Merilä, and partial funding from the Israel Nature and Parks Authority. The field collection of salamanders, experimentation, and their release were conducted according to the Nature and Parks Authority Permit 2015/41180 and with accordance to the guidelines of the Animal Experimentation Ethics Committee at Haifa University Permit Number 033_b9947_6. We thank Kirsi Kähkönen for her help with lab work and Antonina Polevikov for her help with field work.

Author information

Authors and Affiliations

  1. Institute of Evolution and Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, 3498838, Haifa, Israel

    Iftah Sinai, Ori Segev, Alan R. Templeton & Leon Blaustein

  2. Israel Nature and Parks Authority, Jerusalem, Israel

    Iftah Sinai, Gilad Weil & Talya Oron

  3. Ecological Genetics Research Unit, Organismal and Evolutionary Biology Research Programme, Faculty Biological & Environmental Sciences, University of Helsinki, Helsinki, Finland

    Juha Merilä

  4. Department of Biology, Washington University, St. Louis, MO, 63130, USA

    Alan R. Templeton

  5. Department of Biology, Stanford University, Palo Alto, CA, 94305-5020, USA

    Gili Greenbaum

  6. Department of Plant Pathology and Weed Research, ARO, Volcani Center, Bet Dagan, 50250, Israel

    Lior Blank

Authors
  1. Iftah Sinai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ori Segev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gilad Weil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Talya Oron
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juha Merilä
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alan R. Templeton
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Leon Blaustein
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gili Greenbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lior Blank
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iftah Sinai.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sinai, I., Segev, O., Weil, G. et al. The role of landscape and history on the genetic structure of peripheral populations of the Near Eastern fire salamander, Salamandra infraimmaculata, in Northern Israel. Conserv Genet 20, 875–889 (2019). https://doi.org/10.1007/s10592-019-01181-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-019-01181-5

Keywords

Search

Navigation