Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard

BMC Evolutionary Biology

Catarina Pinho¹  Miguel A Carretero¹  Antigoni Kaliontzopoulou¹  D James Harris¹  Daniele Salvi¹ 

[1] CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto; Campus Agrário de Vairão, 4485-661, Vairão, Portugal

关键词: Temperate species;    Genetic diversity;    Mediterranean peninsulas;    Glacial refugia;    Western Palaearctic;    Phylogeography;    Podarcis muralis;   

Others  :  1086840
DOI  :  10.1186/1471-2148-13-147

 received in 2013-01-07, accepted in 2013-07-08,  发布年份 2013

【 摘 要 】

Background

Pleistocene climatic oscillations have played a major role in structuring present-day biodiversity. The southern Mediterranean peninsulas have long been recognized as major glacial refugia, from where Northern Europe was post-glacially colonized. However, recent studies have unravelled numerous additional refugia also in northern regions. We investigated the phylogeographic pattern of the widespread Western Palaearctic lizard Podarcis muralis, using a range-wide multilocus approach, to evaluate whether it is concordant with a recent expansion from southern glacial refugia or alternatively from a combination of Mediterranean and northern refugia.

Results

We analyzed DNA sequences of two mitochondrial (cytb and nd4) and three nuclear (acm4, mc1r, and pdc) gene fragments in individuals from 52 localities across the species range, using phylogenetic and phylogeographic methods. The complex phylogeographic pattern observed, with 23 reciprocally monophyletic allo- parapatric lineages having a Pleistocene divergence, suggests a scenario of long-term isolation in multiple ice-age refugia across the species distribution range. Multiple lineages were identified within the three Mediterranean peninsulas – Iberia, Italy and the Balkans - where the highest genetic diversity was observed. Such an unprecedented phylogeographic pattern - here called “refugia within all refugia” – compasses the classical scenario of multiple southern refugia. However, unlike the southern refugia model, various distinct lineages were also found in northern regions, suggesting that additional refugia in France, Northern Italy, Eastern Alps and Central Balkans allowed the long-term persistence of this species throughout Pleistocene glaciations.

Conclusions

The phylogeography of Podarcis muralis provides a paradigm of temperate species survival in Mediterranean and extra-Mediterranean glacial refugia. Such refugia acted as independent biogeographic compartments for the long-term persistence of this species, for the differentiation of its genetic lineages, and for the short-distance post-glacial re-colonization of neighbouring areas. This finding echoes previous findings from recent phylogeographic studies on species from temperate ecoregions, thus suggesting the need for a reappraisal of the role of northern refugia for glacial persistence and post-glacial assembly of Holarctic biota.

【 授权许可】

   
2013 Salvi et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Hewitt GM: The genetic legacy of the Quaternary ice ages. Nature 2000, 405:907-913.
• [2]Hewitt GM: The structure of biodiversity – insights from molecular phylogeography. Front Zool 2004, 1:4. BioMed Central Full Text
• [3]Widmer A, Lexer C: Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 2001, 16:267-269.
• [4]Schmitt T: Molecular Biogeography of Europe: pleistocene cycles and postglacial trends. Front Zool 2007, 4:11. BioMed Central Full Text
• [5]Hewitt GM: Some genetic consequences of ice ages and their role in divergence and speciation. Biol J Linn Soc Lond 1996, 58:247-276.
• [6]Hewitt GM: Post-glacial re-colonization of European biota. Biol J Linn Soc Lond 1999, 68:87-112.
• [7]Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF: Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 1998, 7:453-464.
• [8]Habel JC, Schmitt T, Müller P: The fourth paradigm pattern of post-glacial range expansion of European terrestrial species: the phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera). J Biogeogr 2005, 32:1489-1497.
• [9]Stewart JR, Lister AM: Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 2001, 16:608-613.
• [10]Provan J, Bennett KD: Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 2008, 23:564-571.
• [11]Stewart JR, Lister AM, Barnes I, Dalén L: Refugia revisited: individualistic responses of species in space and time. Proc R Soc Lond B Biol Sci 2010, 277:661-671.
• [12]Schmitt T, Varga Z: Extra-Mediterranean refugia: the rule and not the exception? Front Zool 2012, 9:22. BioMed Central Full Text
• [13]Deffontaine V, Libois R, Kotlík P, Sommer R, Nieberding C, Paradis E, Searle JB, Michaux JR: Beyond the Mediterranean peninsulas: evidence of Central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol Ecol 2005, 14:1727-1739.
• [14]Rowe G, Harris DJ, Beebee TJC: Lusitania revisited: a phylogeographic analysis of the natterjack toad Bufo calamita across its entire biogeographical range. Mol Phylogenet Evol 2006, 39:335-346.
• [15]Joger U, Fritz U, Guicking D, Kalyabina-Hauf S, Nagy ZT, Wink M: Phylogeography of western Palaearctic reptiles – Spatial and temporal speciation patterns. Zool Anz 2007, 246:293-313.
• [16]Kotlík P, Deffontaine V, Mascheretti S, Zima J, Michaux JR, Searle JB: A northern glacial refugium for bank voles (Clethrionomys glareolus). Proc Natl Acad Sci USA 2006, 103:14860-14864.
• [17]Varga Z: Extra-Mediterranean refugia, post-glacial vegetation history and area dynamics in Eastern Central Europe. In Relict Species: Phylogeography and Conservation Biology. Edited by Habel JC, Assmann T. Heidelberg: Springer; 2010:57-87.
• [18]Saarma U, Ho SY, Pybus OG, Kaljuste M, Tumanov IL, Kojola I, Vorobiev AA, Markov NI, Saveljev AP, Valdmann H, Lyapunova EA, Abramov AV, Männil P, Korsten M, Vulla E, Pazetnov SV, Pazetnov VS, Putchkovskiy SV, Rõkov AM: Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages. Mol Ecol 2007, 16:401-13.
• [19]Valdiosera CE, Garcia N, Anderlung C, Dalen L, Cregut-Bonnoure E, Kahlke RD, Stiller M, Brandström M, Thomas MG, Arsuaga J-L, Götherström A, Barnes I: Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Mol Ecol 2007, 16:5140-5148.
• [20]Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latałowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, De Beaulieu JL: A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 2006, 171:199-221.
• [21]Magri D: Patterns of post-glacial spread and the extent of glacial refugia of European beech (Fagus sylvatica). J Biogeogr 2008, 35:450-463.
• [22]Gruschwitz M, Böhme W: Podarcis muralis (Laurenti, 1768) – Mauereidechse. In Handbuch der Reptilien und Amphibien Europas, Band 2/II, Echsen (Sauria) III (Lacertidae III: Podarcis). Edited by Böhme W. Wiesbaden: Aula-Verlag; 1986:155–-208.
• [23]Biaggini M, Bombi P, Capula M, Corti C: Podarcis muralis (Laurenti, 1768). In Fauna d’Italia, vol.5, Reptilia. Edited by Corti C, Capula M, Luiselli L, Razzetti E, Sindaco R. Bologna: Calderini; 2011:391-401.
• [24]Schulte U, Veith M, Hochkirch A: Rapid genetic assimilation of native wall lizard populations (Podarcis muralis) through extensive hybridization with introduced lineages. Mol Ecol 2012, 17:4313-4326.
• [25]Harris DJ, Arnold EN: Relationships of Wall Lizards, Podarcis (Reptilia: Lacertidae) based on Mitochondrial DNA sequences. Copeia 1999, 3:749-754.
• [26]Capula M: High genetic variability in insular populations of the lacertid lizard, Podarcis muralis. Biochem Syst Ecol 1997, 25:411-417.
• [27]Giovannotti M, Nisi-Cerioni P, Caputo V: Mitochondrial DNA sequence analysis reveals multiple Pleistocene glacial refugia for Podarcis muralis (Laurenti, 1768) in the Italian Peninsula. Ital J Zool 2010, 77:277-288.
• [28]Bellati A, Pellitteri-Rosa D, Sacchi R, Nistri A, Galimberti A, Casiraghi M, Fasola M, Galeotti P: Molecular survey of morphological subspecies reveals new mitochondrial lineages in Podarcis muralis (Squamata: Lacertidae) from the Tuscan Archipelago (Italy). J Zoolog Syst Evol Res 2011, 49:240-250.
• [29]Salvi D, Harris DJ, Bombi P, Carretero MA, Bologna MA: Mitochondrial phylogeography of the Bedriaga’s rock lizard, Archaeolacerta bedriagae (Reptilia: Lacertidae) endemic to Corsica and Sardinia. Mol Phylogenet Evol 2010, 56:690-697.
• [30]Barata M, Carranza S, Harris DJ: Extreme genetic diversity in the lizard Atlantolacerta andreanskyi (Werner, 1929): a montane cryptic species complex. BMC Evol Biol 2012, 12:167. BioMed Central Full Text
• [31]Harris DJ, Pinho C, Carretero MA, Corti C, Böhme W: Determination of genetic diversity within the insular lizard Podarcis tiliguerta using mtDNA sequence data, with a reassessment of the phylogeny of Podarcis. Amphibia-Reptilia 2005, 26:401-407.
• [32]Pyron RA, Burbrink FT, Wiens JJ: A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 2013, 13:93. BioMed Central Full Text
• [33]Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. 2nd edition. New York: Cold Spring Harbor Press; 1989.
• [34]Harris DJ: Reassessment of comparative genetic distance in reptiles from the mitochondrial cytochrome b gene. Herpetol J 2002, 12:85-86.
• [35]Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-989.
• [36]Bruen T, Phillipe H, Bryant D: A quick and robust statis-tical test to detect the presence of recombination. Genetics 2006, 172:2665-2681.
• [37]Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23:254-267.
• [38]Librado P, Rozas J: DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [39]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [40]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 2005, 1:47-50.
• [41]Jobb G: TREEFINDER version of October 2008. Germany: Munich; 2008. Distributed by the author at http://www.treefinder.de webcite
• [42]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
• [43]Drummond A, Ho S, Phillips M, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biol 2006, 4:699.
• [44]Pinho C, Harris DJ, Ferrand N: Contrasting patterns of population subdivision and historical demography in three western Mediterranean lizard species inferred from mitochondrial DNA variation. Mol Ecol 2007, 16:1191-205.
• [45]Fouquet A, Noonan B, Rodrigues MT, Pech N, Gilles A, Gemmell NJ: Multiple quaternary refugia in the Eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Syst Biol 2012, 61(3):461-489.
• [46]Moritz C: Defining "Evolutionary Significant Units" for conservation. Trends Ecol Evol 1994, 9(10):373-375.
• [47]Dupanloup I, Schneider S, Excoffier L: A simulated annealing approach to define the genetic structure of populations. Mol Ecol 2002, 11:2571-2581.
• [48]Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-45.
• [49]Capula M, Corti C: Genetic variability in mainland and insular populations of Podarcis muralis (Reptilia: Lacertidae). Bonn Zool Bull 2010, 57:189-196.
• [50]Moore WS: Inferring phylogenies from mtDNA variation: mitochondrial-gen trees versus nuclear-gen trees. Evolution 1995, 49:718-726.
• [51]Palumbi SR, Ciprinao F, Hare MP: Predicting nuclear gene coalescence from mitochondrial data: the three time-rule. Evolution 2001, 55:859-868.
• [52]Hudson RR, Turelli M: Stochasticity overrules the ‘three-time rule’: genetic drift, genetic draft and coalescence times for nuclear loci vs. mtDNA. Evolution 2003, 57:182-190.
• [53]Poulakakis N, Lymberakis P, Antoniou A, Chalkia D, Zouros E, Mylonas M, Valakos E: Molecular phylogeny and biogeography of the wall-lizard Podarcis erhardii (Squamata: Lacertidae). Mol Phylogenet Evol 2003, 28:38-46.
• [54]Kaliontzopoulou A, Pinho C, Harris DJ, Carretero MA: When cryptic diversity blurs the picture: a cautionary tale from Iberian and North African Podarcis wall lizards. Biol J Linn Soc Lond 2011, 103:779-800.
• [55]Avise JC: Phylogeography: the history and formation of the species. Harvard: University Press; 2000.
• [56]Gómez A, Lunt DH: Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In Phylogeography in southern European refugia: evolutionary perspectives on the origins and conservation of European biodiversity. Edited by Weiss S, Ferrand N. Dordrecht: Springer Verlag; 2007:155-188.
• [57]Hewitt GM: Mediterranean Peninsulas - the evolution of hotspots. In Biodiversity hotspots. Edited by Zachos FE, Habel JC. Heidelberg: Springer; 2011:123-147.
• [58]García-París M, Alcobendas M, Buckley D, Wake DB: Dispersal of viviparity across contact zones in Iberian populations of fire salamanders (Salamandra) inferred from discordance of genetic and morphological traits. Evolution 2003, 57:129-143.
• [59]Canestrelli D, Salvi D, Maura M, Bologna MA, Nascetti G: One Species, three Pleistocene evolutionary histories: phylogeography of the Italian crested newt. Triturus carnifex. PLoS ONE 2012, 7(7):e41754.
• [60]Böhme MU, Fritz U, Kotenko T, Džukić G, Ljubisavljević K, Tzankov N, Berendonk TU: Phylogeography and cryptic variation within the Lacerta viridis complex. Zool Scr 2007, 36:119-131.
• [61]Gassert F, Schulte U, Husemann M, Ulrich W, Rödder D, Hochkirch A, Engel E, Meyer J, Habel JC: From southern refugia to the northern range margin: genetic population structure of the common wall lizard, Podarcis muralis. J Biogeogr 2013. in press,
• [62]Elenga H, Peyron O, BonneWlle R, Jolly D, Cheddadi R, Guiot J, Andrieu V, Bottema S, Buchet G, De Beaulieu JL, Hamilton AC, Maley J, Marchant R, Perez-Obiol R, Reille M, Riollet G, Scott L, Straka H, Taylor D, Van Campo E, Vincens A, Laarif F, Jon-son H: Pollen-based biome reconstruction for southern Europe and Africa18,000 yr BP. J Biogeogr 2000, 27:621-634.
• [63]Vogel JC, Rumsey FJ, Schneller JJ, Barrett JA, Gibby M: Where are the glacial refugia in Europe? Evidence from pteridophytes. Biol J Linn Soc Lond 1999, 66:23-37.
• [64]Ursenbacher S, Conelli A, Golay P, Monney J-C, Zuffi MAL, Thiery G, Durand T, Fumagalli L: Phylogeography of the asp viper (Vipera aspis) inferred from mitochondrial DNA sequence data: evidence for multiple Mediterranean refugial areas. Mol Phylogenet Evol 2006, 38:546-552.
• [65]Litvinchuk SN, Crottini A, Federici S, De Pous P, Donaire D, Andreone F, Kalezić ML, Džukić G, Lada GA, Borkin LJ, Rosanov JM: Phylogeographic patterns of genetic diversity in the common spadefoot toad, Pelobates fuscus (Anura: Pelobatidae), reveals evolutionary history, postglacial range expansion and secondary contact. Org Divers Evol 2013. in press,
• [66]Willis KJ, Van Andel T: Trees or no trees? The environments of central and eastern Europe during the last glaciation. Quat Sci Rev 2004, 23:2369-2387.
• [67]Hammouti N, Schmitt T, Seitz A, Kosuch J, Veith M: Combining mitochondrial and nuclear evidences: a refined evolutionary history of Erebia medusa (Lepidoptera: Nymphalidae: Satyrinae) in Central Europe based on the CO1 gene. J Zool Syst Evol Res 2010, 48:115-125.
• [68]Ursenbacher S, Schweiger S, Tomovic L, Crnobrnja-Isailovic J, Fumagalli L, Mayer W: Molecular phylogeography of the nose-horned viper (Vipera ammodytes, Linnaeus (1758)): evidence for high genetic diversity and multiple refugia in the Balkan peninsula. Mol Phylogenet Evol 2008, 46:1116-1128.
• [69]Korsten M, Ho SY, Davison J, Pähn B, Vulla E, Roht M, Tumanov IL, Kojola I, Andersone-Lilley Z, Ozolins J, Pilot M, Mertzanis Y, Giannakopoulos A, Vorobiev AA, Markov NI, Saveljev AP, Lyapunova EA, Abramov AV, Männil P, Valdmann H, Pazetnov SV, Pazetnov VS, Rõkov AM, Saarma U: Sudden expansion of a single brown bear maternal lineage across northern continental Eurasia after the last ice age: a general demographic model for mammals? Mol Ecol 2009, 18:1963-1979.
• [70]Jackson ST, Webb RS, Anderson KH, Overpeck JT, Webb T III, Williams JW, Hansen BCS: Vegetation and environment in eastern North America during the last glacial maximum. Quat Sci Rev 2000, 19:489-508.
• [71]Rowe KC, Heske EJ, Brown PW, Paige KN: Surviving the ice: Northern refugia and postglacial colonization. Proc Natl Acad Sci USA 2004, 101:10355-10359.
• [72]Pruett CL, Winker K: Evidence for cryptic northern refugia among high- and temperate-latitude species in Beringia. Clim Change 2008, 86:23-27.
• [73]Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE: Refugia: identifying and understanding safe havens for biodiversity under climate change. Global Ecol Biogeogr 2012, 21:393-404.
• [74]Anderson LL, Hu FS, Nelson DM, Petit RJ, Paige KN: Ice-age endurance: DNA evidence of a white spruce refugium in Alaska. Proc Natl Acad Sci USA 2006, 103:12447-12450.
• [75]Lawing AM, Polly PD: Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species’ response to climate change. PLoS One 2011, 16(12):e28554.
• [76]Willis KJ, Bhagwat SA: Questions of importance to the conservation of global biological diversity: answers from the past. Clim. Past Discuss 2010, 6:1139-1162.
• [77]Willis KJ, Bennett KD, Froyd C, Figueroa-Rangel B: How can a knowledge of the past help to conserve the future? Biodiversity conservation strategies and the relevance of long-term ecological studies. Phil. Trans. R. Soc. B 2007, 362:175-186.