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Chronicle of an extinction foretold: genetic properties of an extremely small population of Iberolacerta monticola

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Abstract

The fragmentation and destruction of natural habitats by human intervention is producing a continuous and inexorable reduction of the size of populations in multitude of species all over the world. Small and isolated populations face higher extinction risks, due to demographic and environmental stochasticity, and also because of several genetic threats, among which inbreeding is considered the most important one. For many of these species, the extinction of a population is an irreversible event, so that determining the immediate importance of these risk factors and understanding their interactions is crucial for conservation plans. Iberolacerta monticola is a small lacertid endemic to the northwestern Iberian Peninsula, distributed mainly across moderate/high altitude mountainous regions. Some populations are found nearly at sea-level, though, in fluvial valleys with relict Atlantic forests, in the severely fragmented western part of its range. One of them has been dramatically reduced over the last 30 years, and presently is on the brink of extinction. Using microsatellite nuclear markers, we obtained different measures of genetic variation at this site, together with demographic and breeding data. Both the level of heterozygosity and the number of alleles per locus indicate that the level of variation in this population is comparatively high, and the average inbreeding coefficient is very low. Individuals appear healthy and long-lived, and are related by a few different lines of descent. These findings are discussed in the context of current theories and experimental evidence of associative overdominance and purging of the genetic load of populations, with special emphasis on the evolutionary potential of recovery of small evolutionary units.

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References

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  PubMed  CAS  Google Scholar 

  • Aragón P, López P, Martín J (2001a) Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications of field spatial relationships between males. Behav Ecol Sociobiol 50:128–133

    Article  Google Scholar 

  • Aragón P, López P, Martín J (2001b) Seasonal changes in activity and spatial and social relationships of the Iberian rock lizard, Lacerta monticola. Can J Zool 79:1965–1971

    Article  Google Scholar 

  • Aragón P, Meylan S, Clobert J (2006) Dispersal status-dependent response to the social environment in the Common Lizard, Lacerta vivipara. Funct Ecol 20:900–907

    Article  Google Scholar 

  • Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031

    Article  PubMed  CAS  Google Scholar 

  • 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, Population, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France. http://www.genetix.univ-montp2.fr/genetix/genetix.htm

  • Bierne N, Tsitrone A, David P (2000) An inbreeding model of associative overdominance during a population bottleneck. Genetics 155:1981–1990

    PubMed  CAS  Google Scholar 

  • Blomqvist D, Pauliny A, Larsson M, Flodin LA (2010) Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population. BMC Evol Biol 10(33):1–9

    Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    PubMed  CAS  Google Scholar 

  • Boudjemadi K, Martin O, Simon J-C, Estoup A (1999a) Development and cross-species comparison of microsatellite markers in two lizard species: Lacerta vivipara and Podarcis muralis. Mol Ecol 8:518–520

    PubMed  CAS  Google Scholar 

  • Boudjemadi K, Lecomte J, Clobert J (1999b) Influence of connectivity on demography and dispersal in two contrasting habitats: an experimental approach. J Anim Ecol 68:1207–1224

    Article  Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  PubMed  CAS  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Campos JL, Posada D, Caballero A, Moran P (2007) Spatio-temporal genetic variability in sea trout (Salmo trutta) populations form north-western Spain. Freshw Biol 52:510–524

    Article  Google Scholar 

  • Carranza S, Arnold EN, Amat F (2004) DNA phylogeny of Lacerta (Iberolacerta) and other lacertine lizards (Reptilia: Lacertidae): did competition cause long-term mountain restriction? System Biodivers 2:57–77

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis models and estimation procedures. Am J Hum Genet 19:233–257

    PubMed  CAS  Google Scholar 

  • Chakraborty R, Weiss KM (1991) Genetic variation of the mitochondrial DNA genome in American Indians is at mutation-drift equilibrium. Am J Phys Anthropol 86:497–506

    Article  PubMed  CAS  Google Scholar 

  • Chybicki IJ, Dzialuk A, Trojankiewicz M, Slawski M, Burczyk J (2008) Spatial genetic structure within two contrasting stands of Scots pine (Pinus sylvestris L.). Silvae Genet 57:4–5

    Google Scholar 

  • Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • Coltman DW, Slate J (2003) Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971–983

    PubMed  CAS  Google Scholar 

  • Cote J, Clobert J, Brodin T, Fogarty S, Sih A (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos Trans R Soc Lond B Biol Sci 365:4065–4076

    Article  PubMed  CAS  Google Scholar 

  • Crnokrak P, Barrett SCH (2007) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    Google Scholar 

  • Crochet PA, Chaline O, Surget-Groba Y, Debain C, Cheylan M (2004) Speciation in mountains: phylogeography and phylogeny of the rock lizards genus Iberolacerta (Reptilia: Lacertidae). Mol Phylogenet Evol 30:860–866

    Article  PubMed  CAS  Google Scholar 

  • Estoup A, Garnery L, Solignac M, Cornuet JM (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679–695

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP: phylogenetic inference package, version 3.68. Department of Genome Sciences, University of Washington, Seattle. http://evolution.genetics.washington.edu/phylip.html

  • Fernández J, Toro MA (2006) A new method to estimate relatedness from molecular markers. Mol Ecol 15:1657–1667

    Article  PubMed  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Galán P (1999) Declive y extinciones puntuales en poblaciones de baja altitud de Lacerta monticola cantabrica. Bol Asoc Herpetol Esp 10:47–51

    Google Scholar 

  • Galán P (2008) Ontogenetic and sexual variation in the coloration of the lacertid lizards Iberolacerta monticola and Podarcis bocagei. Do the females prefer the greener males? Anim Biol 58:173–198

    Article  Google Scholar 

  • Galán P, Vila M, Remón N, Naveira H (2007) Caracterización de las poblaciones de Iberolacerta monticola en el Noroeste ibérico mediante la combinación de datos morfológicos, ecológicos y genéticos. Munibe (Suplemento) 25:34–43

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Gilligan DM, Briscoe DA, Frankham R (2005) Comparative losses of quantitative and molecular genetic variation in finite populations of Drosophila melanogaster. Genet Res 85:47–55

    Article  PubMed  CAS  Google Scholar 

  • Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471

    PubMed  CAS  Google Scholar 

  • Goudet J (2001) FSTAT: a program to estimate and test gene diversities and fixation indices. Department of Ecology & Evolution, UNIL, Lausanne. http://www.unil.ch/izea/softwares/fstat.html

  • Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) Conservation biology: ‘Ghost’ alleles of the Mauritius kestrel. Nature 403:616

    Article  PubMed  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hoffman JI, Forcada J, Trathan PN, Amos W (2007) Female fur seals show active choice for males that are heterozygous and unrelated. Nature 445:912–914

    Article  PubMed  CAS  Google Scholar 

  • Holsinger KE (2000) Demography and extinction in small populations. In: Young AG, Clarke GM (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, pp 55–74

    Chapter  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kimura M, Ota T (1975) Distribution of allelic frequencies in a finite population under stepwise production of neutral alleles. Proc Natl Acad Sci USA 72:2761–2764

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lacy RC, Ballou JD (1998) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution 52:900–909

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  PubMed  CAS  Google Scholar 

  • Latter BD, Mulley JC, Reid D, Pascoe L (1995) Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster. Genetics 139:287–297

    PubMed  CAS  Google Scholar 

  • Lawrence HA, Taylor GA, Millar CD, Lambert DM (2008) High mitochondrial and nuclear genetic diversity in one of the world’s most endangered seabirds, the Chatham Island Taiko (Pterodroma magentae). Conserv Genet 9:1293–1301

    Article  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • López P, Martín J, Cuadrado M (2004) The role of lateral blue spots in intrasexual relationships between male Iberian rock-lizards, Lacerta monticola. Ethology 110:543–561

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • Marshall TC, Slate J, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A 196:729–749

    Article  CAS  Google Scholar 

  • Mayer W, Arribas O (2003) Phylogenetic relationships of the European lacertid genera Archaeolacerta and Iberolacerta and their relationships to some other ‘Archaeolacertae’ (sensu lato) from Near East, derived from mitochondrial DNA sequences. J Zool Syst Evol Res 41:157–161

    Article  Google Scholar 

  • Moreira PL, Almeida AP, Delgado H, Salgueiro O, Crespo EG (1999) Bases para a conservação da lagartixa da montanha (Lacerta monticola). Estudos de Biologia e Conservaçao da Natureza 25:1–68

    Google Scholar 

  • Nembrini M, Oppliger A (2003) Characterization of microsatellite loci in the wall lizard Podarcis muralis (Sauria: Lacertidae). Mol Ecol Notes 3:123–124

    Article  CAS  Google Scholar 

  • Ohta T (1971) Associative overdominance caused by linked detrimental mutations. Genet Res 18:277–286

    Article  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204

    Article  Google Scholar 

  • Olsson M, Shine R (2003) Female-biased natal and breeding dispersal in an alpine lizard, Niveoscincus microlepidotus. Biol J Linn Soc Lond 79:277–283

    Article  Google Scholar 

  • Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Dissertation, University of Dublin, Dublin, Ireland

  • Pérez-Mellado V, Sá-Sousa P, Marquez R, Martínez-Solano I (2009) Iberolacerta monticola. IUCN Red List of Threatened Species. Version 2009.1

  • Pinho C, Sequeira F, Godinho R, Harris DJ, Ferrand N (2004) Isolation and characterization of nine microsatellite loci in Podarcis bocagei (Squamata: Lacertidae). Mol Ecol Notes 4:286–288

    Article  CAS  Google Scholar 

  • 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 90:502–503

    Article  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Reich DE, Goldstein DB (1998) Genetic evidence for a Paleolithic human population expansion in Africa. Proc Natl Acad Sci USA 95:8119–8123

    Article  PubMed  CAS  Google Scholar 

  • Reich DE, Feldman MW, Goldstein DB (1999) Statistical properties of two tests that use multilocus data sets to detect population expansions. Mol Biol Evol 16:453–466

    CAS  Google Scholar 

  • Remón N, Vila M, Galán P, Naveira H (2008) Isolation and characterization of polymorphic microsatellite markers in Iberolacerta monticola, and cross-species amplification in Iberolacerta galani and Zootoca vivipara. Mol Ecol Res 8:1351–1353

    Article  Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    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 

  • Rúa M, Galán P (2003) Reproductive characteristics of a lowland population of an alpine lizard: Lacerta monticola (Squamata, Lacertidae) in north-west Spain. Anim Biol 53:347–366

    Article  Google Scholar 

  • Rumball W, Franklin IR, Frankham R, Sheldon BL (1994) Decline in heterozygosity under full-sib and double first-cousin inbreeding in Drosophila melanogaster. Genetics 136:1039–1049

    PubMed  CAS  Google Scholar 

  • Saccheri IJ, Brakefield PM, Nichols RA (1998) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (satyridae). Evolution 50:2000–2013

    Article  Google Scholar 

  • Salvador A, Diaz JA, Veiga JP, Bloor P, Brown RP (2008) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19:169–176

    Article  Google Scholar 

  • Schroeder H, Yanbaev Y, Degen B (2010) A very small and Isolated population of the Green Oak Leaf Roller, Tortrix viridana L., with high genetic diversity–How does this work? J Hered 101:780–783

    Article  PubMed  Google Scholar 

  • Sinervo B, Clobert J (2003) Morphs, dispersal behavior, genetic similarity, and the evolution of cooperation. Science 300:1949–1951

    Article  PubMed  CAS  Google Scholar 

  • Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Victoriano Sepulveda P, Rocha CF, Ibargüengoytía N, Aguilar Puntriano C, 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 328:894–899

    Article  PubMed  CAS  Google Scholar 

  • Sivasundar A, Hey J (2003) Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163:147–157

    PubMed  CAS  Google Scholar 

  • Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265

    Article  PubMed  CAS  Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264

    Article  PubMed  CAS  Google Scholar 

  • Srikwan S, Woodruff DS (2000) Genetic erosion in isolated small-mammal populations following rainforest fragmentation. In: Young AG, Clarke GM (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, pp 149–172

    Chapter  Google Scholar 

  • Streiff R, Labbe T, Bacilieri R, Steinkellner H, Gloessl J, Kremer A (1998) Within-population genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites. Mol Ecol 7:317–328

    Article  Google Scholar 

  • Szulkin M, Garant D, McCleery RH, Sheldon BC (2007) Inbreeding depression along a life-history continuum in the great tit. J Evol Biol 20:1531–1543

    Article  PubMed  CAS  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Waldman B, McKinnon JS (1993) Inbreeding and outbreeding in fishes, amphibians, and reptiles. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. The University of Chicago Press, Chicago, pp 250–282

    Google Scholar 

  • Wang J, Hill WG, Charlesworth D, Charlesworth B (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet Res 74:165–178

    Article  PubMed  CAS  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC (2002) Selection, load and inbreeding depression in a large metapopulation. Genetics 160:1191–1202

    PubMed  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Zamudio KR, Sinervo B (2003) Ecological and social contexts for the evolution of alternative mating strategies. In: Fox SF, McCoy JK, Baird TA (eds) Lizard social behavior. The Johns Hopkins University Press, Baltimore, pp 83–106

    Google Scholar 

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Acknowledgments

This research was supported by grants PGIDIT03RFO10301PR and PGIDIT06RFO10301PR, from Xunta de Galicia, and REN2003-02931/GLO from Ministerio de Ciencia y Tecnología (Spain), awarded to Horacio F. Naveira. Special thanks are given to Union Fenosa, owner of the Güimil Powerplant, for granting access to its facilities. The partial physical map of Europe displayed in Fig. 1a was obtained from the Centro Nacional de Información Cartográfica (www.cnig.es, didactic resources), Ministerio de Fomento (Spain). This study was completed in partial fulfillment of the Ph. D. of N. R. at the Universidade da Coruña.

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Remón, N., Galán, P. & Naveira, H. Chronicle of an extinction foretold: genetic properties of an extremely small population of Iberolacerta monticola . Conserv Genet 13, 131–142 (2012). https://doi.org/10.1007/s10592-011-0272-3

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