High genetic diversity but limited gene flow in Flemish populations of the crested newt, Triturus cristatus

Authors

  • Isa Schön Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000 Brussels, Belgium
  • A. Raepsaet Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000 Brussels, Belgium
  • Boudewijn Goddeeris Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000 Brussels, Belgium
  • D. Bauwens Research Institute for Nature and Forest, Kliniekstraat 25, B-1070 Brussels, Belgium
  • J. Mergeay Research Institute for Nature and Forest, Gaverstraat 4, B-9500 Geraardsbergen, Belgium
  • J. Vanoverbeke Laboratory of Aquatic Ecology and Evolutionary Biology, Catholic University of Leuven, Charles Deberiotstraat, 32, B-3000 Leuven, Belgium
  • Koen Martens Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000 Brussels, Belgium

DOI:

https://doi.org/10.26496/bjz.2011.160

Keywords:

Triturus cristatus, genetic variability, conservation, microsatellite, population genetics, crested newt

Abstract

Habitat destruction and fragmentation are among the major causes of amphibian decline. We investigated to what extent geographic distance and barriers affect the genetic composition of the crested newt, Triturus cristatus in Flanders (North Belgium), causing inbreeding or loss of genetic diversity. Data from seven microsatellite loci and 170 individuals from seven metapopulations up to 180km apart revealed heterozygosities of 0.53 to 0.67 within populations and moderate levels of genetic divergence between populations (FST values from 0.074 to 0.141, harmonic means of Dest between 0.070 and 0.189). In all Flemish meta-populations, more than 90% of the individuals from a given geographic region were assigned to the same genetic cluster indicating little genetic exchange, even in De Panne where the two populations Oosthoek and Westhoek are only a few kilometres apart. Such sub-structuring on a micro-scale has also been described in other amphibians. Unique alleles in most populations further support the probability that genetic drift has already led to some isolation. With the exception of the Oosthoek population, however, we found no significant evidence for bottlenecks. Connectivity within pool clusters seems essential to the maintenance of genetic diversity in crested newts as is indicated by our findings from Tommelen, the population with the largest number of pools in close proximity, which also shows the highest levels of heterozygosity (He and Ho) and the second highest number and richness of alleles. In conclusion, our study indicates that dispersal and migration rates between the Flemish populations of Triturus cristatus are limited at the geographic scale studied here but that habitat fragmentation has not yet led to a significant loss of genetic diversity of the studied Flemish populations, possibly because crested newts are relatively long-lived, fragmentation of their habitat is relatively recent in Flanders, and most investigated pools are still connected at the local scale.

References

ALTENTOFT ME & O’ BRIEN J (2010). Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity, 2:47-71.

ANDERSEN LW, FOG K & DAMGAARD C (2004). Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proceedings of the Royal Society of London, Biological Sciences, 271:1293-1302.

ARNTZEN JW, SMITHSON A & OLDHAM RS (1999). Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus. Journal of Herpetology, 33:567-576.

BAUWENS D & CLAUS K (1996). Verspreiding van amfibieën en reptielen in Vlaanderen. De Wielewaal Natuurvereniging v.z.w., Turnhout.

BEEBEE TJC (2005). Short review: Conservation genetics of amphibians. Heredity, 95:423-427.

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 5171, Université de Montpellier II, Montpellier.

BLITTERSWIJK VAN H, STUMPEL AHP, ARENS PFP & OTTBURG FGWA (2005). Adders onder het gras. Beschikbaarheid en bruikbaarheid van ecologische en genetische kennis over amfibieën en reptielen en de knelpunten voor beleid en beheer. Alterra-report, 1149, Altera, Wageningen, The Netherlands: 37-40.

BURNS EL, ELRIDGE BMD & HOULDEN BA (2004). Microsatellite variation and population structure in a declining Australian Hylid Litoria aurea. Molecular Ecology, 13:1745-1757.

CORNUET JM & LUIKART G (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144:2001-2014.

CRAWFORD NG (2010). SMOGD: Software for the measurement of genetic diversity. Molecular Ecology Resources, 10:556-557.

CUSHMAN SA (2006). Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation, 128:231-240.

DECLERCK S, DE BIE T, ERCKEN D, HAMPEL H, SCHRIJVERS S, VAN WICHELEN J, GILLARD V, MANDIKI R, LOSSON B, BAUWENS D, KEIJERS S, VYVERMAN W, GODDEERIS B, DE MEESTER L, BRENDONCK L & MARTENS K (2006). Ecological characteristics of small farm land ponds: associations with land-use practices at multiple spatial scales. Biological Conservation, 131:523-532.

DESCAMPS S & BAERT P (2003). De kamsalamander in Tommelen ; een unieke waterdraak. In: STEVENS J & CRÉVECOEUR L (eds) Likona-jaarboek 2003, Likona, Hasselt, Belgium.

DRISCOLL D (1998). Genetic structure of the frogs Geocrinia lutea and Geocrinia rosea reflects extreme population divergence and range changes, not dispersal barriers. Evolution, 52:1147-1157.

FAHRIG L (2002). Effects of habitat fragmentation on the extinction treshold: a synthesis. Ecological Applications, 12:346-353.

FAHRIG L & MERRIAM G (1985). Habitat patch connectivity and population survival. Ecology, 66:1762-1768.

FRANKEL OH & SOULÉ ME (1981). Conservation and evolution. Cambridge University Press, Cambridge.

FRANKHAM R, BALLOU DJ & BRISCOE DA (2002) Introduction to conservation genetics. Cambridge University Press.

FRANKHAM R, LEES K, MONTGOMERY ME, ENGLAND PR, LOWE E & BRISCOE DA (1999). Do population size bottlenecks reduce evolutionary potential ? Animal Conservation 2:255-260.

FROGLIFE (2001). The Great Crested Newt Conservation Handbook. (Internet address: http://www.froglife.org/GCNCH/GCNCH.htm).

GOLDSTEIN DB & SCHLÖTTERER C (1999). Microsatellites – Evolution and applications. Oxford University Press.

GRIFFITHS RA (1996). Newts and salamanders of Europe. Poyser Natural history, London.

GRIFFITHS RC (1979). A Transition Density Expansion for a Multi-Allele Diffusion Model. Advances in Applied Probability, 11:310-325.

GRIFFITHS RC, SEWELL D & MCREA RS (2010). Dynamics of a declining amphibian metapopulation: Survival, dispersal and the impact of climate. Biological Conservation, 143:485-491.

GUO SW & THOMPSON EA (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48:361-372.

HITCHINGS SP & BEEBEE TJC (1998). Loss of genetic diversity and fitness in Common toad (Bufo bufo) populations isolated by inimical habitats. Journal of Evolutionary Biology, 11:269-283.

HOULAHAN JE, FINDLAY CS, SCHMIDT BR, MEYER AH & KUZMIN SL (2000). Quantitative evidence for global amphibian population declines. Nature, 404:752-755.

JAMES TY, LITVINTSEVA AP, VILGALYS R, MORGAN JAT, TAYLOR JW, FISHER MC, BERGER L, WELDON C, DU PREEZ L & LONGCORE JE (2009). Rapid global expansion of the fungal disease cytridiomycosis into declining and healthy amphibian populations. PLoS Pathogens, 5:e10000458.

JEHLE R & ARNTZEN JW (2002). Review: Microsatellite markers in amphibian conservation genetics. Herpetological Journal, 12:1-9.

JEHLE R, ARNTZEN JW, BURKE T, KRUPA A & HÖDL W (2001). The annual number of breeding adults and the effective population size of syntopic newts (Triturus cristatus, T. marmoratus). Molecular Ecology, 10:839-850.

JEHLE R, WILSON GA, ARNTZEN JW & BURKE T (2005). Contemporary gene flow and the spatio-temporal genetic structure of subdivided newt populations (Triturus cristatus, T. marmoratus). Journal of Evolutionary Biology, 18:619-628.

JOST L (2008). GST and its relatives do not measure differentiation. Molecular Ecology, 17:4015-4026.

KALINOWSKI ST (2005). HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Molecular Ecology Notes, 5:187-189.

KRAAIJVELD-SMIT FJL, BEEBEE TJC, GRIFFITHS RA, MOORE RD & SCHLEY L (2005). Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis. Molecular Ecology, 14:3307-3315.

KRUPA AP, JEHLE R, DAWSON DA, GENTLE LK, GIBBS M, ARNTZEN JW & BURKE T (2002). Microsatellite loci in the crested newt (Triturus cristatus) and their utility in other newt taxa. Conservation Genetics, 3:87-89.

KUPFER A (1998). Migration distances of some crested newts (Triturus cristatus) within an agricultural landscape. Zeitschrift für Feldherpetologie, 5:238-242.

LANDE R (1988). Genetics and demography in biological conservation. Science 241:1455-1460.

LUIKART G, SHERWIN WB, STEELE BM & ALLENDORF FW (1998). Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Molecular Ecology, 7:963-974.

MAES D & VAN DYCK H (2001). Butterfly diversity loss in Flanders (north Belgium): Europe’s worst case scenario ? Biological Conservation, 99:263-276.

MALETZKY A, KAISER R & MIKULICEK P (2010) Conservation genetics of crested newt species Triturus cristatus and T. carnifex within a contact zone in a central Europe: impact of interspecific introgression and gene flow. Diversity, 2:28-46.

MANTEL N (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27:209-220.

MCLEE AG & SCAIFE RW (1993). The colonisation by great crested newt (Triturus cristatus) of a water body following treatment with a piscicide to remove a large population of sticklebacks (Gasterosteus aculeatus). British Herpetological Society Bulletin, 42:6-9.

MEYER S (2005). Untersuchung zur Überlebensstrategie der Kammmolchpopulationen (Triturus cristatus, Laurenti 1768) in der Kulturlandschaft Sachsen-Anhalts. Dissertation Universität Halle-Wittenberg, Germany.

MIKULICEK P (2005). Hybridization and genetic differentiation of the crested newts (Triturus cristatus superspecies) in Central Europe – analysis of nuclear markers. PhD thesis, University of Prague, Czech Republic.

MONSEN KJ & BLOUIN MS (2003). Genetic structure in a montane ranid frog: restricted gene flow and nuclear-mitochondrial discordance. Molecular Ecology, 12:3275-3286.

NEI M & CHESSER RK (1983). Estimation of fixation indices and gene diversities. Annals of Human Genetics, 47:253-259.

NEWMAN RA & SQUIRE T (2001). Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Molecular Ecology, 10:1087-1100.

NÖLLERT A & NÖLLERT C (2001). Amfibieëngids van Europa, Tirion, Baarn.

PRITCHARD JK, STEPHENS M & DONNELLY P (2000). Inference of population structure using multilocus genotype data. Genetics, 155:945-959.

RAEPSAET A (2007). Population genetics of Triturus cristatus from Flanderen. Honour’s Thesis, University Ghent.

ROUSSET F (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8:103-106.

ROUTMAN E (1993). Population structure and genetic diversity of metamorphic and paedomorphic populations of the tiger salamander, Ambystoma tigrinum. Journal of Evolutionary Biology, 6:329-357.

ROWE G, BEEBEE TJC & BURKE T (2000). A microsatellite analysis of natterjack toad, Bufo calamita, metapopulations. Oikos, 88:641-651.

SACCHERI I, KUUSSAARI M, KANKARE M, VIKMAN P, FORTELIUS W & HANSKI I (1998). Inbreeding and extinction in a butterfly metapopulation. Nature, 392:491-494.

SEPPA P & LAURILA A (1999). Genetic structure of island populations of the anurans Rana temporaria and Bufo bufo. Heredity, 82:309-317.

SHAFFER HB, FELLERS GM, MAGEE A & VOSS SR (2000). The genetics of amphibian declines: population substructure and molecular differentiation in the Yosemite toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymporphism analysis (SSCP) and mitochondrial DNA sequence data. Molecular Ecology, 9:245-257.

SODHI NS, BICKFORD D, DIESMOST AC, LEE TM, KOH LP, BROOK BW, SEKERCIOGLU CH & BRADSHAW CJ (2008). Measuring the meltdown: drivers of global amphibian extinction and decline. PloS ONE, 3:e1636.

STUART SN, CHANSON JS, COX NA, YOUNG BE, RODRIGUES ASL, FISCHMANN DL & WALLER RW (2004). Status and trends of amphibian declines and extinctions worldwide. Science, 306:1783-1786.

TALLMON DA, FUNK WC, DUNLAP WW & ALLENDORF FW (2000). Genetic differentiation among long-toed salamander (Ambystoma macrodactylum) populations. Copeia, 1:27-35.

THIESMEIER B & KUPFER A (2000). Der Kammmolch: ein Wasserdrache in Gefahr, Laurenti-Verlag, Bochum.

VAN OOSTERHOUT C, HUTCHINSON WF, WILLS DPM & SHIPLEY P (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4:535-538.

VENCES M & KÖHLER J (2008). Global diversity of amphibians (Amphibia) in freshwater. Hydrobiologia, 595:569-580.

VOS CC, ANTONISSE-DE JONG AG, GOEDHART PW & SMULDERS MJM (2001). Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity, 86:598-608.

VOS CC & CHARDON JP (1998). Effects of habitat fragmentation and road density on the distribution pattern of the moor frog Rana arvalis. Journal of Applied Ecology, 35:44-56.

WAHLUND S (1928). Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas, 11:65-106.

WALLACE H (1987). Abortive development in the crested newt Triturus cristatus. Development, 100:65-72.

WEIR BS & COCKERHAM CC (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38:1358-1370.

WILCOX B & MURPHY DD (1985). Conservation strategy: the effects of fragmentation on extinction. American Naturalist, 125:879-887.

ZAMUDIO KR & WIECZOREK AM (2007). Fine-scale spatial genetic structure and dispersal among spotted salamander (Ambystoma maculatum) breeding populations. Molecular Ecology, 16:257-274.

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Published

2024-03-20

How to Cite

Schön, I., Raepsaet, A., Goddeeris, B., Bauwens, D., Mergeay, J., Vanoverbeke, J., & Martens, K. (2024). High genetic diversity but limited gene flow in Flemish populations of the crested newt, Triturus cristatus. Belgian Journal of Zoology, 141(1), 3–13. https://doi.org/10.26496/bjz.2011.160

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