Abstract
Introduction of individuals from multiple sources could create opportunities for hybridization between previously isolated lineages, which may impact on the invasion process. Identifying the phylogeographic origin of introduced populations is therefore an important task to further test the causes and consequences of human-mediated translocations. The common wall lizard (Podarcis muralis) shows a strong phylogeographic structure as a result of past isolation in glacial refugia, but it has also been commonly introduced outside of its native range. Here we analysed 655 base pairs (bp) of the cytochrome b sequence from 507 individuals from 23 introduced populations of P. muralis in England. We identified 12 unique haplotypes in the introduced populations that were nested into five native geographically distinct clades with genetic divergences ranging from 2.1 to 5.7 %. Multiple clade origin was common within populations, with a maximum of three different haplotype clades being represented within a single population. The genetic data are consistent with a scenario whereby initial establishment was a result of translocation of animals from their native range, whereas more recent establishment (i.e. since the mid-1980s) is the result of translocations of animals from previously established non-native populations. However, this requires further study. Overall, our results show that human introductions have created substantial opportunities for hybridization between genetically and phenotypically distinct lineages, which may have important consequences for the establishment success and long-term viability of introduced wall lizard populations.
Similar content being viewed by others
References
Allan GM, Prelypchan CJ, Gregory PT (2006) Population profile of an introduced species, the common wall lizard (Podarcis muralis), on Vancouver Island, Canada. Can J Zool 84(1):51–57
Arnold M (1997) Natural hybridization and evolution. Oxford University Press, New York
Arnold ML, Martin NH (2010) Hybrid fitness across time and habitats. Trends Ecol Evol 25(9):530–536
Avise JC (1994) Molecular markers, natural history, and evolution. Chapman & Hall, New York
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48
Bellati A, Pellitteri-Rosa D, Sacchi R, Nistri A, Galimberti A, Casiraghi M, Fasola M, Galeotti P (2011) Molecular survey of morphological subspecies reveals new mitochondrial lineages in Podarcis muralis (Squamata: Lacertidae) from the Tuscan Archipelago (Italy). J Zoolog Syst Evol Res 49:240–250
Böhme MU, Fritz U, Kotenko T, Georg D, Ljubisavljević K, Tzankov N, Berendonk TU (2007) Phylogeography and cryptic variation within the Lacerta viridis complex (Lacertidae, Reptilia). Zoolog Scr 36(2):119–131
Burke R, Deichsel G (2008) Lacertid lizard introductions into North America: history and future. In: Mitchell JC, Brown REJ, Bartholomew B (eds) Urban herpetology. Society for the Study of Amphibians and Reptiles, Salt Lake City, UT, pp 347–353
Chapple DG, Miller KA, Kraus F, Thompson MB (2012) Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Divers Distrib. doi:10.1111/j.1472-4642.2012.00919.x
Crispo E, Moore J-S, Lee-Yaw JA, Gray SM, Haller BC (2011) Broken barriers: human-induced changes to gene flow and introgression in animals. BioEssays 33(7):508–518
Davison J, Ho SYW, Bray SC, Korsten M, Tammeleht E, Hindrikson M, Østbye K, Østbye E, Lauritzen SE, Austin J (2011) Late-quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species. Quat Sci Rev 30(3):418–430
Deichsel G, Schwiger S (2004) Podarcis muralis (common wall lizard). Herpetol Rev 35:289–290
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4
Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19(19):4113–4130
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10(3):564–567
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Frazer JFD (1964) Introduced species of amphibians and reptiles in mainland Britain. Br J Herpetol 3:145–150
Giovannotti M, Nisi-Cerioni P, Caputo V (2010) Mitochondrial DNA sequence analysis reveals multiple Pleistocene glacial refugia for Podarcis muralis (Laurenti, 1768) in the Italian Peninsula. Italian J Zool 77:277–288. doi:10.1080/11250000903143885
Glandt D (2010) Taschenlexikon der Amphibien und Reptilien Europas. Quelle & Meyer, Wiebelsheim
Gleed-Owen CP (2004) Green lizards and wall lizards on Bournemouth cliffs. Herpetol Bull 88:3–7
Grant PR, Grant BR, Petren K (2005) Hybridization in the recent past. Am Nat 166(1):56–67
Gruschwitz M, Böhme W (1986) Podarcis muralis (Laurenti, 1768)—Mauereidechse. In: Handbuch der Amphibien und Reptilien Europas. Bandll/2, Echsen (Sauria) III (Lacertidae lIl; Podarcis). Aula-Verlag, Wiesbaden, pp 155–208
Harris DJ, Sá-Sousa P (2002) Molecular phylogenetics of Iberian Wall Lizards (Podarcis): is Podarcis hispanica a species complex? Mol Phylogenet Evol 23(1):75–81
Hewitt GM (1996) Some genetic consequences of ice ages and theur role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt GM (2004) Genetic consequences of climatic oscillations in the quaternary. Philos Trans Royal Soc B: Biol Sci 359(1442):183–195
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755
Joger U, Fritz U, Guicking D, Kalyabina-Hauf S, Nagy ZT, Wink M (2007) Phylogeography of western palaearctic reptiles-spatial and temporal speciation patterns. Zool Anz J Comp Zool 246(4):293–313
Kalyabina S, Milto KD, Ananjeva NB, Legal L, Joger U, Wink M (2001) Phylogeography and systematics of Lacerta agilis based on mitochondrial cytochrome b gene sequences: first results. Russ J Herpetol 8:149–159
Katoh K, Misawa K, Kuma K-i, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 30(14):3059–3066
Kolbe JJ, Glor RE, Schettino LRG, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431(7005):177–181
Kolbe JJ, Lavin BR, Burke RL, Rugiero L, Capula M, Luiselli L (2012) The desire for variety: Italian wall lizard (Podarcis siculus) populations introduced to the United States via the pet trade are derived from multiple native-range sources. Biol Invasions. doi:10.1007/s10530-012-0325-7
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104(10):3883
Lever C (1977) The naturalized animals of the British Isles. Hutchinson & Co, London
Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol Harlequin Ladybird. PLoS One 5(3):e9743
Lunt DH, Ibrahim KM, Hewitt GM (1998) MtDNA phylogeography and postglacial patterns of subdivision in the meadow grasshopper Chorthippus parallelus. Heredity 80:633–641. doi:10.1046/j.1365-2540.1998.00311.x
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20(5):229–237. doi:10.1016/j.tree.2005.02.010
Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge
Nadachowska-Brzyska K, Zielinski P, Radwan J, Babik W (2012) Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol Ecol 21(4):887–906. doi:10.1111/j.1365-294X.2011.05347.x
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76(10):5269–5273
Olsson M, Ujvari B, Madsen T, Uller T, Wapstra E (2004) Haldane rules: costs of outbreeding at production of daughters in sand lizards. Ecol Lett 7(10):924–928
Palo JU, Schmeller DS, Laurila A, Primmer CR, Kuzmin SL, Merila J (2004) High degree of population subdivision in a widespread amphibian. Mol Ecol 13(9):2631–2644
Podnar M, Mayer W, Tvrtković N (2005) Phylogeography of the Italian wall lizard, Podarcis sicula, as revealed by mitochondrial DNA sequences. Mol Ecol 14(2):575–588
Podnar M, Haring E, Pinsker W, Ballantine WJ (2007) Unusual origin of a nuclear pseudogene in the Italian wall lizard: intergenomic and interspecific transfer of a large section of the mitochondrial genome in the genus Podarcis (Lacertidae). J Mol Evol 64(3):308–320
Poulakakis N, Lymberakis P, Antoniou A, Chalkia D, Zouros E, Mylonas M, Valakos E (2003) Molecular phylogeny and biogeography of the wall-lizard Podarcis erhardii (Squamata: Lacertidae). Mol Phylogenet Evol 28(1):38–46
Poulakakis N, Lymberakis P, Valakos E, Pafilis P, Zouros E, Mylonas M (2005a) Phylogeography of Balkan wall lizard (Podarcis taurica) and its relatives inferred from mitochondrial DNA sequences. Mol Ecol 14(8):2433–2443
Poulakakis N, Lymberakis P, Valakos E, Zouros E, Mylonas M (2005b) Phylogenetic relationships and biogeography of Podarcis species from the Balkan Peninsula, by Bayesian and maximum likelihood analyses of mitochondrial DNA sequences. Mol Phylogenet Evol 37:845–857
R_Development_Core_Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22(9):454–464
Rykena S (1991) Hybridization experiments as tests for species boundaries in the genus Lacerta sensu stricto. Mitt Zool Mus Berl 67:55–68
Rykena S (1996) Experimental interspecific hybridization in the genus Lacerta. Israel J Zool 42:171–184
Schulte U (2007) Die Mauereidechse. Laurenti Verlag, Bielefeld
Schulte U, Hochkirch A, Lötters S, Rödder D, Schweiger S, Weimann T, Veith M (2012) Cryptic niche conservatism among evolutionary lineages of an invasive lizard. Glob Ecol Biogeogr 21(2):198–211
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19(4):198–207
Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455(7213):620–626
Stelkens RB, Schmid C, Selz O, Seehausen O (2009) Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol Biol 9(1):283
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19(17):3496–3514. doi:10.1111/j.1365-294X.2010.04691.x
Stumpel AHP (2004) Reptiles and amphibians as targets for nature management. Alterra Green World Research, Wageningen
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7(4):453–464. doi:10.1046/j.1365-294x.1998.00289.x
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Uller T, Leimu R (2011) Founder events predict changes in genetic diversity during human-mediated range expansions. Glob Chang Biol 17(11):3478–3485. doi:10.1111/j.1365-2486.2011.02509.x
Vonlanthen P, Bittner D, Hudson AG, Young KA, Muller R, Lundsgaard-Hansen B, Roy D, Di Piazza S, Largiader CR, Seehausen O (2012) Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482(7385):357–362. doi:10.1038/nature10824
Acknowledgments
We are immensely grateful to Steve Langham (Surrey Amphibian and Reptile Group) for his efforts at mapping the occurrence of P. muralis in England and for generously providing detailed information about introduced populations. We are also grateful to all land owners for their permission to catch lizards on their property and to Natural England for permits (20091978; 20102163; 20112817). We are particularly indebted to Charles Snell, Martin Noble, Fred and Pat Howarth, Shona McDonough, the Lever family, Tony Pashley, Mark Anderson, Ian Boyd, Nick Squirrel, Tim Bernhard, Tanya French, and Anthony Mitchell for outstanding help with getting access to private gardens and lands, giving us pointers that helped establish the geographic limits of populations, and retrieve details on the introduction history. We are also grateful to Robert Heathcote and Ben Daly for assistance with catching lizards and to Alicia Davies for assistance in the molecular lab. We thank two anonymous reviewers for helpful comments on the manuscript. This research was funded by the British Ecological Society, the National Geographic Society, and the Royal Society of London (all to TU), a FP7 Marie Curie Fellowship (GMW) and a Biotechnology and Biological Sciences Research Council (BBSRC) scholarship (SM).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Michaelides, S., While, G.M., Bell, C. et al. Human introductions create opportunities for intra-specific hybridization in an alien lizard. Biol Invasions 15, 1101–1112 (2013). https://doi.org/10.1007/s10530-012-0353-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0353-3