Origin and genetic diversity of an introduced wall lizard population and its cryptic congener
Identifieur interne : 000F21 ( Istex/Corpus ); précédent : 000F20; suivant : 000F22Origin and genetic diversity of an introduced wall lizard population and its cryptic congener
Auteurs : Michael Veith ; Philippe Geniez ; Franz Gassert ; Axel Hochkirch ; Ulrich SchulteSource :
- Amphibia-Reptilia [ 0173-5373 ] ; 2012.
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DOI: 10.1163/156853812X626160
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Gassert</name></author><author><name sortKey="Hochkirch, Axel" sort="Hochkirch, Axel" uniqKey="Hochkirch A" first="Axel" last="Hochkirch">Axel Hochkirch</name></author><author><name sortKey="Schulte, Ulrich" sort="Schulte, Ulrich" uniqKey="Schulte U" first="Ulrich" last="Schulte">Ulrich Schulte</name></author></analytic><monogr></monogr><series><title level="j">Amphibia-Reptilia</title><title level="j" type="sub">Publication of the Societas Europaea Herpetologica</title><title level="j" type="abbrev">AMRE</title><idno type="ISSN">0173-5373</idno><idno type="eISSN">1568-5381</idno><imprint><publisher>BRILL</publisher><pubPlace>The Netherlands</pubPlace><date type="published" when="2012">2012</date><biblScope unit="volume">33</biblScope><biblScope unit="issue">1</biblScope><biblScope unit="page" from="129">129</biblScope><biblScope unit="page" to="140">140</biblScope></imprint><idno type="ISSN">0173-5373</idno></series><idno 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Veith</name></json:item><json:item><name>Philippe Geniez</name></json:item><json:item><name>Franz Gassert</name></json:item><json:item><name>Axel Hochkirch</name></json:item><json:item><name>Ulrich Schulte</name></json:item></author><subject><json:item><lang><json:string>eng</json:string></lang><value>bottleneck effect</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>mtDNA</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>hybridization</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>invasive species</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>genetic variability</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>microsatellite</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>effective population size</value></json:item></subject><language><json:string>eng</json:string></language><originalGenre><json:string>research-article</json:string></originalGenre><qualityIndicators><score>5.512</score><pdfVersion>1.4</pdfVersion><pdfPageSize>481.89 x 697.323 pts</pdfPageSize><refBibsNative>false</refBibsNative><keywordCount>7</keywordCount><abstractCharCount>0</abstractCharCount><pdfWordCount>6125</pdfWordCount><pdfCharCount>41258</pdfCharCount><pdfPageCount>12</pdfPageCount><abstractWordCount>1</abstractWordCount></qualityIndicators><title>Origin and genetic diversity of an introduced wall lizard population and its cryptic congener</title><refBibs><json:item><host><author><json:item><name>G Altherr</name></json:item></author><title>From genes to habitats – effects of urbanisation and urban areas on biodiversity</title><publicationDate>2007</publicationDate></host></json:item><json:item><author><json:item><name>W Amos</name></json:item><json:item><name>A 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<article-id pub-id-type="doi">10.1163/156853812X626160</article-id>
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<article-title>Origin and genetic diversity of an introduced wall lizard population and its cryptic congener</article-title>
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<surname>Veith</surname>
<given-names>Michael</given-names>
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<surname>Geniez</surname>
<given-names>Philippe</given-names>
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<surname>Gassert</surname>
<given-names>Franz</given-names>
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<surname>Hochkirch</surname>
<given-names>Axel</given-names>
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<surname>Schulte</surname>
<given-names>Ulrich</given-names>
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<pub-date pub-type="epub">
<year>2012</year>
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<volume>33</volume>
<issue>1</issue>
<fpage>129</fpage>
<lpage>140</lpage>
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<copyright-statement>© Koninklijke Brill NV, Leiden, The Netherlands</copyright-statement>
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<kwd-group>
<kwd>bottleneck effect</kwd>
<kwd>mtDNA</kwd>
<kwd>hybridization</kwd>
<kwd>invasive species</kwd>
<kwd>genetic variability</kwd>
<kwd>microsatellite</kwd>
<kwd>effective population size</kwd>
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<p>Amphibia-Reptilia 33 (2012): 129-140 Origin and genetic diversity of an introduced wall lizard population and its cryptic congener Ulrich Schulte 1, ∗ , Franz Gassert 2 , Philippe Geniez 3 , Michael Veith 1 , Axel Hochkirch 1 Abstract. The Common Wall Lizard ( Podarcis muralis ) has been introduced within large parts of Central Europe, the UK and parts of North America. In an introduced population of this species in Lower Saxony, Germany, we found in addition to mtDNA haplotypes of P. muralis also haplotypes of its congener Podarcis liolepis , a species that hitherto has never been recorded outside its native range. We therefore, (1) wanted to identify the geographic origin of the founder individuals of both non-native populations, (2) test for hybridization between introduced individuals of both species in Germany and (3) compare levels of genetic diversity between native and introduced populations. We sequenced a fragment of the mitochondrial cytochrome b gene and genotyped individuals of the introduced as well as native populations of both species at eleven microsatellite loci. Our results suggest that the founders presumably stem from a region in the eastern Pyrenees, where sympatric populations of P. muralis and P. liolepis are known. No evidence for gene flow between the two species was found in the introduced population. These results are consistent with behavioural observations indicating agonistic interactions of P. muralis towards P. liolepis rather than cross-species attraction. Compared to the native populations, high levels of genetic diversity have been retained in the introduced population of both species and no evidence for a genetic bottleneck was found. The effective population size was high in P. muralis , but substantially smaller in P. liolepis . Keywords : bottleneck effect, effective population size, genetic variability, hybridization, invasive species, microsatellite, mtDNA. Introduction Globalization has favoured an exponential in- crease in the rate and spatial extent of alien species introductions worldwide. The ecologi- cal threat posed by alien invasive species is a severe problem in nature conservation (Strayer et al., 2006; Perrings et al., 2010). During recent decades, a considerable amount of research has been carried out to study contemporary evolu- tionary events in the process of biological inva- sions in order to determine which mechanisms drive invasions and to evaluate the impact of invasions. It is generally believed that genetic attributes like additive genetic variance, epis- tasis, heterosis, genetic drift and genomic re- arrangements promote the success of invaders 1 - Department of Biogeography, Trier University, D-54286 Trier, Germany 2 - Section Zoologie des Vertébrés, Musée National d’Histoire Naturelle, L-2160 Luxembourg 3 - Ecologie et Biogéographie des Vertébrés, Ecole Pratique des Hautes Etudes, UMR 5175, CEFE-CNRS, Montpel- lier, France ∗ Corresponding author; e-mail: schulte@uni-trier.de as they provide a buffer to respond to natu- ral selection and allow adapting to new envi- ronments (reviewed in Lee, 2002). Several re- cent studies have shown that invasive popula- tions often exhibit only minimal reductions in genetic diversity as a consequence of a large number of founders or multiple introductions (Holsbeek et al., 2008; Simberloff, 2009). Fur- thermore, admixture of genotypes from differ- ent source populations often boosts genetic di- versity and therefore, may support the invasive- ness of species (Kolbe et al., 2004; Pairon et al., 2010). As a consequence of genetic drift, se- lection and hybridization, a rapid genetic diver- gence of invasive populations from their ances- tral source population is often observed (Boss- dorf et al., 2005). Due to the inevitable bias of nearly exclu- sively sampling successful invasive populations, a loss of genetic diversity associated with popu- lation bottlenecks during the invasion processes is reported less frequently (Kelly et al., 2006). In general, a loss of genetic diversity occurs in introduced populations that have been founded by a few closely related individuals, which only © Koninklijke Brill NV, Leiden, 2012. DOI:10.1163/156853812X626160</p>
<p>130 U. Schulte et al. represent a subset of the genetic variability of a certain source population within the native range (so called founder effect). Although many studies found patterns of inbreeding and out- breeding in invasive populations (e.g. Huxel, 1999; Facon et al., 2011), a small number of founders, high inbreeding and low genetic vari- ation does not necessarily lead to negative fit- ness consequences or extinction of invasive populations (Verhoeven et al., 2011). The Common Wall Lizard ( Podarcis muralis ) is one of the few reptile species that has success- fully colonized regions in north-western Eu- rope and North America far outside its sub- Mediterranean native range. While determin- ing the origin of 77 introduced wall lizard populations in Central Europe, we discovered one mitochondrial haplotype of the Catalonian wall lizard ( Podarcis liolepis ) at one location (Nörten-Hardenberg, Germany) together with two haplotypes of the Western France P. mu- ralis Clade (see fig. 1; Schulte et al., 2012). Based upon information of local residents, the population stems from an intentional introduc- tion and exist at least since the end of the 1980s (Schulte et al., 2011). Recently considered as a valid species within the P. hispanicus complex (Renoult et al., 2009, 2010), Podarcis liolepis is distributed in the northern Iberian Peninsula (Catalonia, the Ebro Valley, Basque Country, the northern Castilian Plateau southwards to Va- lencia) and in southern France up to the Rhone river (Carretero, Marcos and de Prado, 2006; Renoult et al., 2010; Kaliontzopoulou et al., 2011; fig. 2). Morphologically, P. muralis and P. liolepis are relatively difficult to distinguish (Gosá, 1985; Pérez-Mellado, 1998; Vacher and Geniez, 2010). Introduced populations might thus be overlooked, particularly as the latter species is usually not expected outside its native range. In order to gain a deeper understanding of the rapid parallel establishment of these two non-native wall lizards at a single locality in Germany, we focused on their genetic architec- ture by using a combination of phylogeographic marker systems (mtDNA) and highly variable microsatellite markers. We specifically wanted to (1) identify the putative source region of the introduced populations of both species, (2) test for hybridization between introduced individu- als of both species in Nörten-Hardenberg (Ger- many) and (3) compare levels of genetic diver- sity between native and introduced populations. Figure 1. Lateral view of a male specimen (NOE14) from Nörten-Hardenberg (Germany) attributed to Podarcis liolepis liolepis . Photo: US (16.06.2010). This figure is published in colour in the online version.</p>
<p>Genetic diversity of introduced Podarcis 131 Figure 2. Location of the introduced population in Germany (NOE, Nörten-Hardenberg, Lower Saxony) and geographic range of P. liolepis (upward diagonal shaded area, from Renoult et al., 2010 and Kaliontzopoulou et al., 2011) and P. muralis (downward diagonal shaded area, from Schulte, 2008) in western Europe. Sampled localities within the native ranges correspond to symbols (black dots: P. muralis Western France Clade; white triangles: P. liolepis ; white square: P. hispanicus sensu stricto). Black squares within Germany and Austria correspond to introduced P. muralis populations representing six different genetic lineages (see Appendix): BR1 = Bramsche; BOT2 = Bottrop; UU60 = Duisburg- Hüttenheim; UU70 = Mainz; NOE, Nörten-Hardenberg; HAN1 = Halle a. d. Saale; UU89 = Altenhain; SD1 = Schärding; BA18 = Klosterneuburg; LB, Labeaume; AM, Amboise; ST, St. Malo; LR, La Rochelle; LS, Lourdes; AY2, Benasque (AY234155); AF#42, Pyrenees (AF469442); AY1, Andorra (AY151908); MS, Montségur; PL, Planoles; AF#40, Girona (AF469440); AF#32/34, Barcelona (AF469432, AF469434); AF#38, Tarragona (AF469438); AF0, Valencia (AF052635); AF4, Medinaceli (AF469436); and DQ0, Burgos (DQ08114). Materials and methods Sampling A total of 51 lizards (juveniles and adults of both sexes) were captured by hand or by noosing randomly from the introduced mixed population in Nörten-Hardenberg in July 2010 (Lower Saxony, Germany, figs 1 and 2). Lizards autotomized the tail tip after exerting light pressure and were immediately released afterwards. Tail tips were stored in 99.8% ethanol p.a. Additionally, 15 individuals were sampled at a locality in Labeaume (Département Ardèche, Southern France), where P. muralis and P. liolepis also occur in syntopy. We added 25 samples of P. muralis from Montségur ( n = 13; Département Ariège), Lourdes ( n = 6; Département Hautes-Pyrénées) and La Rochelle ( n = 6; Département Charente-Maritime). For the mtDNA analyses we used samples of P. muralis from Amboise and Saint- Malo as well as a museum specimen of P. liolepis from Planoles (Spain, fig. 2). Assignment of geographic origin Sequence data were collected for ten morphologically vari- able specimens from the introduced German population, for ten samples from six native French populations (Labeaume, Montségur, Lourdes, La Rochelle, Amboise and Saint- Malo) and for one specimen from Planoles (Spain) (fig. 2). DNA was extracted from muscle tissue of autotomized tail tips or of the tongue (museum specimens) using the QIAGEN DNEasy Blood and Tissue Kit (QIAGEN, Hilden) following the manufacturers’ protocol. For amplifications of</p>
<p>132 U. Schulte et al. cytochrome b PCR fragments we used 50 μ l reaction tubes containing: 27 μ l purified water, 20 μ l of Taq polymerase (QIAGEN Hotstar), 1 μ l of each PCR primer and 1 μ l of genomic DNA. Reaction conditions comprised an initial de- naturation step for 15 min at 95°C, 35 cycles of 30 s at 94°C, 30 s at 43°C, 90 s at 72°C, and a final extension step of 10 min at 72°C. We sequenced a 656- to 887-bp fragment of the mitochondrial cytochrome b gene using the primers LGlulk (5 ′ -AACCGCCTGTTGTCTTCAACTA-3 ′ ), Sicnt (5 ′ -TTTGGATCCCTGTTAGGCCTCTGTT-3 ′ ) and HPod (3 ′ -GGTGGAATGGGATTTTGTCTG-5 ′ ) (Podnar et al., 2007; Schulte et al., 2012). Sequencing was performed with the DYEnamic ET Terminator Cycle Sequencing Pre- mixkit (GE Healthcare, Munich) for sequencing reactions run on a MegaBACE 1000 automated sequencer. DNA se- quences were corrected and aligned by eye. Sequences were deposited in GenBank under the accession num- bers JQ403287-JQ403304. For lineage assignment, the se- quences were aligned to sequences from individuals sam- pled within the native range of P. muralis (Carranza, Arnold and Amat, 2004; Busack, Lawson and Arjo, 2005; Giovan- notti, Nisi-Cerioni and Caputo, 2010) or within the inva- sive range, when the geographic origin of the introduced population was known (see Schulte et al., 2012). Therefore, we included twelve P. muralis sequences of a preliminary study (Schulte et al., 2012) representing six different ge- netic lineages of the species which have been introduced in Germany. Sequences of the Podarcis hispanicus species complex, including seven of P. liolepis from Tarragona, Barcelona, Girona, the Pyrenees, Burgos and Medinaceli (Castilla y León), one of Podarcis vaucheri from Morocco, one of P. hispanicus sensu stricto from Valencia as well as one sequence of Podarcis siculus as outgroup were obtained from GenBank (AF052633, AF052635; Castilla et al., 1998; AF469432, AF469434, AF469436, AF469438, AF469440, AF469442, Harris and Sá-Sousa, 2002; DQ081144; Pinho, Ferrand and Harris, 2006; FJ867396, Giovannotti, Nisi- Cerioni and Caputo, 2010; see figs 2 and 3). As we focused on detecting the geographic origin within the native ranges of P. liolepis and P. muralis (Western France Clade), we ig- nored additional sequences from other Spanish lineages or species (Kaliontzopoulou et al., 2011). In order to assign introduced haplotypes to intraspecific evolutionary lineages of P. muralis and P. liolepis and their respective geographic Figure 3. Bayesian consensus tree for the mitochondrial cytB gene for Podarcis muralis and Podarcis liolepis . Numbers are posterior probabilities. Filled circles represent samples from introduced populations in Nörten-Hardenberg (Lower Saxony, Germany), open circles represent P. liolepis samples from the native population in Labeaume (France) (for population names see Appendix).</p>
<p>Genetic diversity of introduced Podarcis 133 range via a phylogenetic tree, we used Bayesian inference in MrBayes 3.1.1 (Ronquist and Huelsenbeck, 2003). We applied the best-fit substitution model (GTR + I + G) sug- gested by MrModeltest 2.2 (Nylander, 2004). We ran four Monte Carlo Markov chains for one million generations each and sampled a tree every 100 generations. This was sufficient to let the average standard deviation drop below 0.01. We discarded 2500 trees as burn-in after checking for stationary and convergence of the chains. Support of the nodes was assessed with the posterior probabilities of re- constructed clades as estimated in MrBayes (Ronquist and Huelsenbeck, 2003). Genotyping We genotyped 51 individuals of the introduced wall lizard population, 14 individuals of the native Podarcis liolepis population from Labeaume and 25 P. muralis individuals from three native populations in south-western France. All individuals were genotyped at eleven microsatellite loci, six of which have been developed for Podarcis muralis (A7, B3, B4, B7, C8, C9; Nembrini and Oppliger, 2003), two for Zootoca vivipara (Lv-4-alpha, Lv-472, Boudjemadi et al., 1999) and three for Podarcis bocagei (Pb10, Pb50, Pb73; Pinho et al., 2004). Amplification was performed in a Multigene Gradient Thermal Cycler (Labnet) using the 2.5 × 5PRIME HotMasterMix (5PRIME). For each PCR we used 5 μ l reaction mix containing: 1.2 μ l genomic DNA, 2.2 μ l HotMasterMix, 2.2 μ l water and 0.1 μ l of the forward and reverse primers. The PCR conditions were as recommended by the manufacturer, with locus-specific annealing temperature between 53°C and 61°C. The 5 ′ - end of each forward primer was labelled with a fluorescent dye, either FAM, TAMRA or HEX. PCR products were run on a MegaBACE 1000 automated sequencer. Fragment lengths were determined using MegaBACE ET550-R size standard and MegaBACE Fragment Profiler (Amersham Biosciences). Data analysis and descriptive statistics We tested our data for the occurrence of null alleles with MICRO-CHECKER 2.2.3 (Van Oosterhout et al., 2004) and for linkage disequilibrium with Fstat 2.9.3.2 (Goudet, 2001). STRUCTURE 2.3.3 (Pritchard, Stephens and Don- nelly, 2000) was used to analyse for genetic structuring among subpopulations. The admixture model was used as we wanted to test for potential hybridization. We chose the correlated allele frequency model with a burn-in of 100 000 simulations followed by one million Markov chain Monte Carlo simulations. Tests were run for K = 1-10 with ten it- erations per K . This range of values for K was chosen taken into consideration that we have sampled four P. muralis populations and two P. liolepis populations. Several meth- ods have been proposed to infer the optimal K value from STRUCTURE runs. The method described by Pritchard, Stephens and Donnelly (2000) is known to sometimes lead to asymptotic convergence and tends to result in too high K values. The optimal K value suggested by Evanno, Reg- naut and Goudet (2005) is based on the second order rate of change ( K ) and tends to result in low K values (Haus- dorf and Hennig, 2010; Campana et al., 2011). Recently, a new method ( F ST ) has been proposed by Campana et al. (2011). We compared all three methods in the CorrSieve package for R (Campana et al., 2011). However, based upon our sampling design, we expected that a biologically mean- ingful minimum value for K would be four (as we sampled two species and each from at least two very distant locali- ties). The results obtained using F ST ( K = 2) and K ( K = 3) both suggested values that appeared not biologi- cal meaningful. We suppose that this is caused by the strong differentiation at the species level. As our ln P (D) values showed no asymptotic convergence and K was biological meaningful, we used the K value with the highest average ln P (D) value as suggested by Pritchard, Stephens and Don- nelly (2000). We used GenAlEx 6.4.1 (updated from Peakall and Smouse, 2006) to calculate the number of alleles ( N A ), the inbreeding coefficient ( F IS ), as well as for expected and observed heterozygosities ( H E and H O ) for each locus and population. Fstat was used to calculate allelic richness ( A R ). As traditional methods of population differentiation ( F ST , G ST ) have recently been strongly criticized, we cal- culated D EST as an estimate of population differentiation (e.g. Jost, 2008; Gerlach et al., 2010) using the DEMEtics package for R (Gerlach et al., 2010). However, in our case F ST and D EST had a strong linear correlation ( R 2 = 0 . 91). Therefore, we used F ST in an AMOVA with 9999 itera- tions in GenAlEx with the genetic clusters suggested by STRUCTURE as populations and the two species as “re- gions”. We estimated the effective population size ( N E ) of clusters identified by STRUCTURE using ONeSAMP, which uses an approximate Bayesian computation for es- timating N E and 95% confidence limits (CL) (Tallmon et al., 2008). The program generates 50 000 simulated popu- lations with N E between a conservatively estimated lower and upper bound for N E (for all four populations: 2-500). After executing ten iterations of estimating N E we calcu- lated the mean and standard deviation of N E for each popu- lation. To detect recent bottlenecks in the introduced popula- tions, the program BOTTLENECK 1.2.02 was used (Cor- nuet and Luikart, 1996). Recent bottlenecks (0.2-4 N E gen- erations) can create a heterozygosity excess compared to populations at mutation-drift equilibrium, because rare al- leles that have little impact on heterozygosity can be lost quickly. We calculated H EQ using the two-phase model with a variance of 30 and a proportion of 70% of the step-wise mutation model in the two-phase model (Di Rienzo et al., 1994), as this is believed to be the most likely mutation model for microsatellites (Piry, Luikart and Cornuet, 1999). Statistical significance was assessed with a one-tailed Wilcoxon-test, since this test proved to be the best for less than 20 loci (Piry, Luikart and Cor- nuet, 1999). Analyses were performed with 1000 itera- tions.</p>
<p>134 U. Schulte et al. Results Geographic origin of the introduced populations The introduced population of P. muralis in Nörten-Hardenberg belongs to the Western France mtDNA clade (fig. 3). This lineage differs substantially from seven other intro- duced P. muralis lineages found in Central Eu- rope (Schulte et al., 2012), with an average p-distance of 0.049 to its sister clade (East- ern France clade). Three of four individuals shared one haplotype, while the fourth individ- ual had a very similar haplotype (p-distance of 0.002). These haplotypes were most sim- ilar to haplotypes found in Andorra and Be- nasque (Carranza, Arnold and Amat, 2004; Bu- sack, Lawson and Arjo, 2005) and differed substantially from another introduced popula- tion of this lineage in Germany (Mainz), which originated from the Atlantic coast of south- ern France. Therefore, the P. muralis popula- tion in Nörten-Hardenberg most probably orig- inated from a region in the eastern Pyrenees. Six haplotypes that differed in two substitu- tions were found among the introduced P. li- olepis individuals. These haplotypes confirmed an affiliation to the subspecies P. l. liolepis (Boulenger, 1905), which occurs at the north- eastern coast of Spain, in the Central and East Pyrenees as well as in departments Pyrenées- Orientales, parts of Aude and occasionally in Haute-Garonne (Geniez and Deso, 2009). In the phylogenetic tree the haplotypes from the in- troduced population form a strongly supported group with the haplotype from Planoles in the province of Girona (fig. 3, p-distance: 0.01). The haplotypes of P. liolepis from the native population sampled in France (Labeaume) were rather different from the introduced clade (p- distance: 0.038) and confirmed an affiliation to the subspecies P. l. cebennensis (Guillaume and Geniez, 1986), which occurs in south-western France up to the departments Drôme and Vau- cluse east of the river Rhone (Geniez et al., 2008). One haplotype from Labeaume repre- sented the Eastern France Clade of P. muralis (fig. 3). Genetic structure All microsatellite markers proved to be poly- morphic for both species. We found evidence for null alleles at locus B3 in all populations and, therefore, excluded this locus from further analyses. There was no evidence for large al- lele drop-out or other scoring errors. All pair- wise tests for linkage disequilibrium were non- significant ( p > 0 . 05). The most likely num- ber of genetic clusters ( K ) among all analysed populations revealed by model-based clustering in STRUCTURE was five (fig. 4). There was no indication for hybridization between both Figure 4. Genetic clusters obtained from the S TRUCTURE analysis ( K = 5) for all 90 samples. Each individual is represented by a single vertical line, divided into K colours. The coloured segment shows the individual’s estimated proportion of membership to that genetic cluster. NOE1: P. muralis , introduced (Nörten-Hardenberg); MS: P. muralis , native (Montségur); LS: P. muralis , native (Lourdes); LR: P. muralis , native (La Rochelle); NOE2: P. liolepis , introduced (Nörten-Hardenberg); LB: P. liolepis , native (Labeaume). This figure is published in colour in the online version.</p>
<p>Genetic diversity of introduced Podarcis 135 Table 1. Pairwise D EST values (upper right part) and pairwise F ST values (lower left part) between the native and introduced populations of Podarcis muralis and Podarcis liolepis . Population names: NOE, Nörten-Hardenberg; LB, Labeaume; LR, La Rochelle; LS, Lourdes; MS, Montségur. P. muralis P. muralis P. muralis P. liolepis P. liolepis (NOE, introduced) (LS/LR, native) (MS, native) (NOE, introduced) (LB, native) P. muralis 0.496 0.374 0.797 0.768 (NOE, introduced) P. muralis 0.142 0.131 0.771 0.669 (LS/LR, native) P. muralis 0.098 0.048 0.780 0.680 (MS, native) P. liolepis 0.268 0.268 0.263 0.496 (NOE, introduced) P. liolepis 0.287 0.287 0.276 0.179 (LB, native) Table 2. Comparison of genetic variability and effective population size ( N E ) in introduced and native populations of Podarcis muralis and Podarcis liolepis ; with n = number of samples, N A = mean number of alleles, A R = allelic richness, H O and H E = observed and expected heterozygosity, F IS = inbreeding coefficient. Population names: NOE, Nörten-Hardenberg; LB, Labeaume; LR, La Rochelle; LS, Lourdes; MS, Montségur. Species/origin n N E N A A R H O H E F IS Podarcis muralis (NOE, introduced) 40 89 ± 13 . 35 9 6.43 0.691 0.685 0.042 Podarcis muralis (LS/LR, native) 12 25 ± 3 . 4 6.9 6.72 0.695 0.668 − 0.042 Podarcis muralis (MS, native) 13 32 ± 2 7.2 6.73 0.708 0.658 − 0.081 Podarcis liolepis (NOE, introduced) 11 23 ± 3 . 69 6.6 6.70 0.564 0.648 0.138 Podarcis liolepis (LB, native) 14 30 ± 2 . 69 6 5.95 0.621 0.601 − 0.029 species at lower numbers of genetic clusters. If a higher K was chosen, likelihood values de- creased and new genetic clusters appeared with no individual having a high probability (using a strict threshold value of q = 0 . 20) of belonging to it. A clear separation of the introduced and native P. liolepis population as well as between the native and introduced P. muralis popula- tion was found. This result was confirmed by the AMOVA, which revealed that a significant portion ( p < 0 . 001) of the genetic variation was explained by “species” (16%) and “popu- lations” (11%). Differentiation between native and introduced populations was high and only exceeded by differentiation among species (ta- ble 1). The lowest D EST and F ST values were found between the two native populations of P. muralis . Genetic diversity between native and introduced populations Compared to the native populations of P. mu- ralis , the introduced population had a lower al- lelic richness, but rather similar values of H E and H O (table 2). On the contrary, the intro- duced P. liolepis population had a higher al- lelic richness and expected heterozygosity than the native population. Only H O was higher in the native than in the introduced popula- tion. Within the introduced populations, P. mu- ralis had higher H E and H O values than P. li- olepis (table 2). Native P. liolepis from south- ern France had the lowest H E and H O . The in- breeding coefficient ( F IS ) was highest in the in- troduced P. liolepis population and lowest in the native P. muralis population from Montségur (table 2). Nevertheless, the introduced P. li- olepis population exhibited a high genetic diver- sity.</p>
<p>136 U. Schulte et al. The estimated N E of the introduced P. li- olepis was much smaller than that of the intro- duced P. muralis (23 ± 3 . 69 vs. 89 ± 13 . 35, table 2). Effective population size of the na- tive P. liolepis population in Labeaume was 30 ± 2 . 69, whereas the native P. muralis popu- lations had an estimated N E of 32 ± 2 (Mont- ségur) and 25 ± 3 . 4 (cluster Lourdes/La Rochelle, table 2). We found no evidence for a genetic bottleneck (heterozygote excess) in any of the analysed populations of either species. Neither of the introduced populations exhibited significant departures from Hardy- Weinberg equilibrium. Discussion Geographical origin of the introduced populations Our results suggest that both non-native wall lizard species stem from a region in the east- ern Pyrenees, where the native ranges of both species overlap (see fig. 2) and syntopic popu- lations of P. liolepis and P. muralis are frequent (Geniez and Deso, 2009). Although the tempo- ral course of introductions remains unknown, we hypothesize that both populations were in- troduced simultaneously, as it is rather unlikely that they have been transported two times in- dependently from the same area to exactly the same locality in Germany. This represents the first record of the Catalonian wall lizard ( Po- darcis liolepis ) as a non-native species in Ger- many. The pathway of the introduction remains unclear, but an intended introduction is most likely as more than 73% of all known introduced populations in Germany can be traced back to human-mediated introductions (Schulte et al., 2008, 2011). Based upon the information of lo- cal residents, the introduction took place at least in the 1980s. Genetic structure and diversity within the native and invasive range Even though the native P. liolepis population was not the source population of the intro- duced population in Nörten-Hardenberg and more populations need to be analysed for fur- ther comparisons, we compare both populations regarding their genetic diversity. The high al- lelic richness of the introduced P. liolepis popu- lation might be caused by its origin in the centre of the species’ distribution (eastern Pyrenees), while the native P. liolepis population analysed occurs at the northern edge of the species’ range in the department Ardéche in France (fig. 2). A reduced genetic diversity at a species’ north- ern range margin is rather typical due to smaller population sizes, partial isolation, stronger ge- netic drift and higher selection pressure (Hewitt, 2001; Böhme et al., 2007). The effective popu- lation size of P. liolepis was rather small, while N E in the introduced P. muralis population even exceeded the values found in the native popu- lations. This might have been caused either by different founder numbers, different time of in- troductions or by an initial decrease in popula- tion size in the introduced P. liolepis population. Our observation of a reduced allelic rich- ness, but similar heterozygosity in the intro- duced P. muralis population compared to the native populations from Western France is in line with the expectation that allelic richness is more strongly affected by genetic drift than heterozygosity (Amos and Balmford, 2001). Compared to the available literature on ge- netic diversity within native P. muralis popu- lations in Central Europe (Gassert, 2005; Al- therr, 2007), heterozygosity and allelic richness of the native and introduced P. muralis popula- tions were rather high. The Montségur popula- tion is located in the south-western part of the range, where Pleistocene glacial refugia may have existed. This might explain, why the popu- lation has conserved a higher genetic diver- sity than populations further north, such as in Switzerland (Altherr, 2007; Blondel and Aron- son, 2010). The high genetic diversity of the in-</p>
<p>Genetic diversity of introduced Podarcis 137 troduced population might also be influenced by its origin from a hotspot of genetic diver- sity. Compared to an introduced population in Cincinnati, Ohio (Lescano, 2010) and other in- troduced populations in Germany (Schulte et al., unpublished data), originating from northern Italy (a hotspot of genetic diversity for P. mu- ralis ) the genetic diversity of the introduced P. muralis population in Nörten-Hardenberg was much higher. We thus hypothesize that propag- ule pressure of both species must have been quite high, since no sign for a recent bottleneck was detected within the introduced populations. Indeed, introductions of numerous individuals might occur frequently among hobby herpetol- ogists, as a high propagule size has for example been reported from a population in Linz (Aus- tria, 130 introduced individuals; Schulte, 2008). It is possible that the high genetic diversity of both non-native populations has facilitated their establishment success. However, in Cincinnati P. muralis appears to be a successful colonizer despite originating from a small number of only twelve founders and multiple bottlenecks (Les- cano, 2010). Inbreeding and a loss of genetic di- versity, therefore, do not necessarily hamper the successful establishment and spread of intro- duced species (Lindholm et al., 2005; Schmid- Hempel et al., 2007; Ficetola, Bonin and Miaud, 2008). Although Pinho, Harris and Ferrand (2008) suggested that Podarcis species take a long time of divergence to acquire complete reproductive isolation and detected gene flow between P. mu- ralis and P. liolepis , we did not find evidence for hybridization among the introduced popula- tions. In contrast, we observed occasionally ag- gressive and territorial interactions of both sexes of P. muralis towards P. liolepis , with matings occurring exclusively among conspecifics. Fur- thermore, we observed a microhabitat segrega- tion between both species ( P. muralis : widely distributed even within the moister talus, P. li- olepis : restricted to vertical structures in rocky habitats with crevices), which is known from sympatric populations throughout the range (Salvador, 1986; Castilla and Bauwens, 1991; Martín-Vallejo et al., 1995; Carretero, Marcos and de Prado, 2006). In a recent study, Gabirot et al. (2010) suggest that chemical cues may reduce the occurrence of hybridization even between the genetically more closely related species P. liolepis from Columbretes islands and P. hispanicus (morphotypes 1 or 2) from Madrid. Hence, olfactory traits might also act as premating barriers between P. muralis and P. liolepis and it is likely that premating bar- riers are well developed considering the diver- gence times and overlapping distribution of both species (fig. 2). Acknowledgements. This work benefited from a grant of the ‘Deutsche Bundesstiftung Umwelt’ (DBU, grant num- ber 27282/33/2). We thank Werner Mayer, Guntram Deich- sel and Burkhard Thiesmeier for sharing their knowledge on introduced wall lizards. Literature of both species and in- formation about morphology and distribution of P. liolepis in France and Spain were provided by Oscar Arribas and Michael Kroninger. For sampling permits and information on the locality in Nörten-Hardenberg we thank Richard Pod- loucky, S. Barbeln and M. Schöfer and the responsible ad- ministration (Naturschutz und Veterinärdienste, Landkreis Northeim) of Lower Saxony. We are grateful to Kenneth Pe- tren and Ninnia Lescano for the possibility to cite their un- published data on wall lizards in Cincinnati. We thank five referees for providing very helpful comments which greatly improved our manuscript. References Altherr, G. (2007): From genes to habitats – effects of ur- banisation and urban areas on biodiversity. Ph.D. thesis, Faculty of Life Sciences, Basel University. Amos, W., Balmford, A. (2001): When does conservation genetics matter? Heredity 87 : 257-265. Blondel, J., Aronson, J. (2010): Biology and Wildlife of the Mediterranean Region, 2nd Edition. Oxford University Press, USA. Böhme, M.U., Schneeweiss, N., Fritz, U., Schlegel, M., Berendonk, T.U. (2007): Small edge populations at risk: genetic diversity of the green lizard ( Lacerta viridis viridis ) in Germany and implications for conservation management. Conserv. Gen. 8 : 555-563. Bossdorf, O., Auge, H., Lafuma, L., Rogers, W.E., Siemann, E., Prati, D. (2005): Phenotypic and genetic differentia- tion between native and invasive plant populations. Oe- cologia 144 : 1-11.</p>
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<p>140 U. Schulte et al. Appendix. Podarcis muralis and Podarcis liolepis populations sampled and used from GenBank with information on sample ID, species and clade affiliation, sampling locality, GenBank accession numbers and references. Sample ID Species (clade affiliation) Sampling locality GenBank Reference accession number NOE1 P. muralis (Western France Clade) Nörten-Hardenberg HQ652969 Schulte et al., 2012 NOE3 P. muralis (Western France Clade) Nörten-Hardenberg HQ652966 Schulte et al., 2012 NOE4 P. muralis (Western France Clade) Nörten-Hardenberg JQ403287 This study NOE38 P. muralis (Western France Clade) Nörten-Hardenberg JQ403288 This study LB169 P. muralis (Eastern France Clade) Labeaume, France JQ403289 This study MS3 P. muralis (Western France Clade) Montségur, France JQ403290 This study LS6 P. muralis (Western France Clade) Lourdes, France JQ403291 This study LRo1 P. muralis (Western France Clade) La Rochelle, France JQ403292 This study StM1 P. muralis (Western France Clade) St. Malo, France JQ403293 This study Amb2 P. muralis (Western France Clade) Amboise, France JQ403294 This study AY151908 P. muralis (Western France Clade) Andorra AY151908 Carranza et al., 2004 AY234155 P. muralis (Western France Clade) Benasque, Spain AY234155 Busack et al., 2005 BR1 P. muralis (Salps Clade) Bramsche, Germany HQ652960 Schulte et al., 2012 UU54 P. muralis (Salps Clade) Bramsche, Germany HQ652944 Schulte et al., 2012 HAN1 P. muralis (Central Balkan Clade) Halle a. d. Saale, HQ652958 Schulte et al., 2012 Germany UU89 P. muralis (Central Balkan Clade) Altenhain, Germany HQ652886 Schulte et al., 2012 UU60 P. muralis (Eastern France Clade) Duisburg-Hüttenheim, HQ652880 Schulte et al., 2012 Germany BOT2 P. muralis (Eastern France Clade) Bottrop, Germany HQ652955 Schulte et al., 2012 UU134 P. muralis (Eastern France Germany HQ652908 Schulte et al., 2012 Languedoc subclade) UU67 P. muralis (Western France Clade) Mainz, Germany HQ652893 Schulte et al., 2012 UU70 P. muralis (Western France Clade) Mainz, Germany HQ652894 Schulte et al., 2012 UU75 P. muralis (Western France Clade) Mainz, Germany HQ652896 Schulte et al., 2012 BA18 P. muralis (Venetian Clade) Klosterneuburg, HQ652943 Schulte et al., 2012 Austria SD1 P. muralis (Tuscany Clade) Schärding, Austria HQ652937 Schulte et al., 2012 NOE2 P. liolepis Nörten-Hardenberg HQ652946 Schulte et al., 2012 NOE11 P. liolepis Nörten-Hardenberg JQ403295 This study NOE19 P. liolepis Nörten-Hardenberg JQ403296 This study NOE24 P. liolepis Nörten-Hardenberg JQ403297 This study NOE36 P. liolepis Nörten-Hardenberg JQ403298 This study NOE37 P. liolepis Nörten-Hardenberg JQ403299 This study Planoles P. liolepis Planoles, Spain JQ403300 This study LB165 P. liolepis Labeaume, France JQ403301 This study LB166 P. liolepis Labeaume, France JQ403302 This study LB167 P. liolepis Labeaume, France JQ403303 This study LB168 P. liolepis Labeaume, France JQ403304 This study AF469432 P. liolepis Barcelona, Spain AF469432 Harris and Sá-Sousa, 2002 AF469434 P. liolepis Barcelona, Spain AF469434 Harris and Sá-Sousa, 2002 AF469436 P. liolepis Medinaceli, Spain AF469436 Harris and Sá-Sousa, 2002 AF469438 P. liolepis Tarragona, Spain AF469438 Harris and Sá-Sousa, 2002 AF469440 P. liolepis Girona, Spain AF469440 Harris and Sá-Sousa, 2002 AF469442 P. liolepis Pyrenees, Spain AF469442 Harris and Sá-Sousa, 2002 DQ081144 P. liolepis Burgos, Spain DQ081144 Pinho et al., 2006 AF052635 P. hispanicus sensu stricto Valencia, Spain AF052635 Castilla et al., 1998 AF052633 P. vaucheri Atlas, Maroc AF052633 Castilla et al., 1998 FJ867396 P. siculus (outgroup) Italy FJ867396 Giovannotti et al., 2010</p>
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