Skip to main content

Advertisement

Log in

Human introductions create opportunities for intra-specific hybridization in an alien lizard

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

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

    Article  Google Scholar 

  • Arnold M (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Arnold ML, Martin NH (2010) Hybrid fitness across time and habitats. Trends Ecol Evol 25(9):530–536

    Article  PubMed  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history, and evolution. Chapman & Hall, New York

    Book  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Deichsel G, Schwiger S (2004) Podarcis muralis (common wall lizard). Herpetol Rev 35:289–290

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Frazer JFD (1964) Introduced species of amphibians and reptiles in mainland Britain. Br J Herpetol 3:145–150

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Glandt D (2010) Taschenlexikon der Amphibien und Reptilien Europas. Quelle & Meyer, Wiebelsheim

    Google Scholar 

  • Gleed-Owen CP (2004) Green lizards and wall lizards on Bournemouth cliffs. Herpetol Bull 88:3–7

    Google Scholar 

  • Grant PR, Grant BR, Petren K (2005) Hybridization in the recent past. Am Nat 166(1):56–67

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages and theur role in divergence and speciation. Biol J Linn Soc 58:247–276

    Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the quaternary. Philos Trans Royal Soc B: Biol Sci 359(1442):183–195

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lever C (1977) The naturalized animals of the British Isles. Hutchinson & Co, London

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • R_Development_Core_Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22(9):454–464

    Article  PubMed  Google Scholar 

  • Rykena S (1991) Hybridization experiments as tests for species boundaries in the genus Lacerta sensu stricto. Mitt Zool Mus Berl 67:55–68

    Article  Google Scholar 

  • Rykena S (1996) Experimental interspecific hybridization in the genus Lacerta. Israel J Zool 42:171–184

    Google Scholar 

  • Schulte U (2007) Die Mauereidechse. Laurenti Verlag, Bielefeld

    Google Scholar 

  • 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

    Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19(4):198–207

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Stumpel AHP (2004) Reptiles and amphibians as targets for nature management. Alterra Green World Research, Wageningen

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Tobias Uller.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 156 kb)

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-012-0353-3

Keywords

Navigation