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Species Distinction and Relationships of the Western Iberian

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Species Distinction and Relationships of the Western Iberian HERPETOLOGICALJOURNAL, Vol. 11,pp. 129-136(2001) SPECIESDISTINCTION AND RELATIONSHIPSOF THE WESTERN IBERIAN PODARCISLIZARDS (REPTILIA, LACERTIDAE) BASED ON MORPHOLOGY AND MITOCHONDRIAL DNA SEQUENCES D. J. HnnnISI ANDP. SA-Sousa, t Centro de Estudos de Ciancia Animal (cECA/uP), campus Agrdrio de vairdo, portugal 2Centro de Ecologia Aplicada, Universidade de Evora, 7002-544, Evora, portugal Wall lizards (Podarcis) arethe dominant reptile group acrossmost of southernEurope. Their taxonomy is complex becausemost speciesexhibit substantialintraspecific morphological polymorphisms.We have estimatedthe phylogeny of the particularlydiverse western Iberian forms using partial cytochrome oxidase and cytochrome b mitochondrial DNA sequencedata and have compared this against morphological variation. Of the two currently recognized speciesin the area- P odarcis hispanica andP. bocagei -neither is monophyletic, and extremely high geneticdiversity betweennewly identifiedforms (up to l5%cytochrome b divergences) indicatesthatbotharespeciescomplexes.Podarcisb bocageiisgeneticallydistinctfromP.(b) carbonelli which appearsto be a separatespecies using both mtDNA andprotein electrophoretic data. The insular form previously assigned to P b. berlengensis, and sometimes argued to deservespecies status is not genetically distinct from P. (b ) carbonelli using the mtDNA sequences P hispanica can be separatedinto at least four highly divergent groups, two in western Iberia, one in easternIberia and one in North Africa. Key words: phylogeny, cytochromeb, cytochromeoxidase, morphology, Iberian lizards INTRODUCTION (S6-Sousa,2000a). P. hispanicatype I has the follow- ing On the Iberian Peninsulathree speciesof insectivo- characteristics:flattened head and body; either reticulated rous wall lizards have been recognized- the Iberian or shiped dark dorsalpatterns; and whitish- pearly (for wall lizard, Podarcis hispanica Steindachner 1870; coloured belly details see Pdrez-Mellado, 1981a,b; Bocage's wall lizard, Podarcis bocagei Seoane1884; Gal6n, 1986; Pdrez-Mellado and Galindo, 1986 Guillaume, 1987 and Podarcis muralis Laurenti 1768. Podarcis bocagei ; ; Sii-Sousa,199 5 a). P. hispanica (SW and P. hispanicalive in sympatry in large areasof NW Ape 2 Iberian form) has been found Iberia (Gal6n,1986;Pdrez-Mellado & Galindo,1986; in Andalusia,in Extremadura,in the Madrid re- gion, and in Sii-Sousa,1995a). Both exhibit pronouncedsexual di- the western and southern parts of Portugal (Sii-Sousa,2000a).In morphism, adult males being larger than females and Portugal, P. hispanica type 2 prefer (<400 having more intense colour patterns (Gal6n, 1986; seemsto lowlands m) with a Mediterra- nean climate (Sd-Sousa, Pdrez-Mellado& Galindo, 1986). 2000a). This form has the following characteristics: Podarcis hispanica is a medium sized (SVL 65-70 head and body moderately robust; green and/or patterns, mm), morphologically variable rock-dwelling lizard, light brown and yellow- orange belly (see Klemmer, which is found in SW France(Langedoc-Rousillon and 1957; Salvador, 1986; Guillaume, 1987; Cdvennes),the Iberian Peninsula(except the northern- GonzLlez de la Vega, 1989; Srl- Sousa,1995a). most corner) and NW Africa (Galdn, 1986;Guillaume, Given severalrecords of P. hispanica vaucheri in SW Iberia (Boulenger, 1987, 1997). Despite taxonomic controversyabout P. 1905; Klemmer, 1957;Salvador, hispanicasubspecies, two forms have beenrecognized 7974, 1986;Busack, 1986; Guillaume, 1987) one might in Portugal (S6-Sousa1995a,2000a). First, there is a hypothesizethat morphologically P. hispanica NW Iberian form (P. hispanica type 1) that resembles type 2 and P. hispanica vaucheri are the same. However, retain the "lusitanica" form of Guillaume (1987).P. hispanica we the P. hispanica type 2 de- 'Submeseta nomination until further type I is found in Galicia, in the Norte' studies confirm whether similarity in phenotype plateau, in the northern half of Portugal and on the corresponds to a common 'Sistema genofype across Central' mountain range (S6-Sousa,2000a). the entire range. So far all allopatric greenishmorphotypes wall lizard In Portugal,P. hispanicatype I seemsto inhabitmainly of found in the south- ern part of Iberia (e.g. Portugal, highlands(>400 m) where eitherAtlantic or continental southern Andalusiaand Levant) have climatic conditions may prevail. It has been found in been considered as P. h. hispanica (P6rez-Mellado,1998). the northern part of Portugal, north of the Tagus river Also P. hispanicatype 2 is of- ten mistakenfor P. b. bocagei,because oftheir greenor light-brown chromatic pattems, although the species Correspondence:D.J. Harris, Centro de Estudosde Ci€ncia Animal (CECA/UP), CampusAgrario de Vair6o, 4480 Vila show severaldifferences and have allopatric distribu- do Conde, Portugal.E-mail:[email protected] tions (S6-Sousa,199 5 a, 1998,2000 a). 130 D. J. HARRIS AND P. SA-SOUSA Podarcisb. bocageiis a medium-sized(adult snout- There,the type of climate- but alsothe balancebe- vent length,SVL:65-70 mm), ground-dwellinglizard, tweenthe numberof frost daysper yearand the degree the malesof which show greendorsal patterns, while of aridity- appearimportant to explainthe distribution femalesare brown with a pair of greenstripes (Gal6n, of P. b. carbonelli(S6-Sousa, in prep.). 2000; Pdrez-Mellado, l98la,b, 1986; S6-Sousa, Morphologicalcharacters and the existenceof 1995a).This speciesis an Iberian-Atlanticendemic oc- parapatriczones of contactbetween different type s (i.e. curring in W Asturias,Cantabria, Galicia and north of without interbreeding)suggested that P. bocageiand P. Portugal(Gal6n, 1986,1997; S6-Sousa, 1998). On a hispanicamight in fact be speciescomplexes (56- coarsescale, the distribution of P. b. bocageican be Sousa,2000a and in prep.).To resolverelationships largely explainedby macroenvironmentalvariables betweenand within these groups, and to determine andtype of climate(S6-Sousa, 2000b). whetherrecognized clades based on morphological It has been suggestedthat P. b. carbonelli P6rez- charactersare geneticallydistinct, a phylogenetic Mellado1981 merits species distinction (S6-Sousa, in analysiswas conductedusing DNA sequencesderived prep.;S6-Sousa et a|.2000).P. b. carbonel/t(SVL:50- from two mitochondrialgenes, cytochrome 6 andcyto- 55 mm) is a small, green ground-dwellinglizard, chromeoxidase 1. Populationsacross the rangeof the initially thoughtto be restrictedto the W SistemaCen- acceptedsubspecies of P. bocageiwere sampled. For tral range(P6rez-Mella do, l98 l a,b, l 986).However, it the cytochromeb datasets previously published se- hasbeen found in othermountain systems as well as quencesof P. hispanica from easternSpain and alongthe Atlantic lowlands,particularly in Portugal Morocco(Castilla et al.,1998;Hanis & Arnold, 1999) (Magraner,1986; S6-Sousa,1995b, 1999, 2000b). wereincluded in the analyses. TABLE L List of lizardsexamined in themtDNA phylogeny.* indicatespreviously published data was included in theanalysis. Sequencesare deposited in Genbank(accession numbers AF372051 to AF372089).Map codesare shown in Fig. l. Species mtDNA Code Locality COl/ Cyt 6 Map Code Gqllotia galloti Gran Canaria U- Lacerta dugesii dugesii Madeira l/* Lacerta perspicillata Mallorca Po darcis his panic a' li olepis' Castell6n,Spain Podarcis hispanica "t rpe l" P.h.r Vila Real, Pt. Ur B P.h.2 Montesinho, Pt. t/- A P.h.3 Montesinho, Pt. l/- A Podarc i s hispanic a "Moroccan" P.h.ml High Atlas, Morocco -11 T P.h.m2 High Atlas, Morocco Ur T P.h.m3 High Atlas, Morocco r/r T Podqrcis hispanica "We 2" P.h.vl Leiria, Pt. 1t- C P.h.v2 Portalegre,Pt. Ul D P.h.v3 Beja, Pt. r/l E P.h.v4 Marvao, Pt. l/- F P.h.v5 Agueda,Pt. U- G Podarcis bocagei bocagei P.b.b1 Montesinho,Pt. U- A P.b.b2 Montesinho, Pt. t/- A P.b.b3 Vila Pouca d Aguiar, Pt. l/- K P.b.b4 Serrado Ger6s,Pt. U- H P.b.b5 Vairdo, Pt. t/- J P.b.b6 Vairdo, Pt. U1 J P.b.b7 Vair6o, Pt. t/l J P.b.b8 Braga,Pt. t/- I P.b.b9 Viana do Castelo,Pt. t/- L P.b.b10 Viana do Castelo,Pt. t/- L P.b.b11 Viana do Castelo,Pt. Ur L P odarcis carbonelli carbonelli P.c.cl Serra da Estrela, Pt. U1 M P.c.c2 Torreira, Aveiro, Pt. l/l N P.c.c3 Monte Cldrigo, Pt. Ul a P.c.c4 Peniche,Pt. t/- P P o darc is c arb onelli b er lengensis P.c.b. Berlengaisle, off Peniche 1/- o PHYLOGENYOF IBERIAN PODARCISLIZARDS l3l amplifiedregions of approximately350 bp and 550 bp respectively.Thermocycling consisted of 30 cyclesof 93"Cfor 30 secs,55"C for I min and 72oCfor I min, followedby a singlecycle at 72"Cfor 5 min. Successful PCR bands were purified using a QIAEX II kit (Quiagen)and sequencedon an Applied Biosystems Model373ADNA SequencingSystem, using a PRISM Ready Reaction DyeDeoxy Terminator Cycle Sequencingkit. Centrisepspin columns(Princeton SeparationsInc.) wereused for excessdye extraction. PHYLOGENETICANALYSES Sequenceswere aligned using Clustal W (Thompson et al., 1994). There were no insertions or deletions. They were then imported into PAUP* (Swofford, 2001) for phylogenetic analyses. When estimating phylogenetic relationshipsamong sequences,one as- sumesa model of evolution regardlessof the optimality criteria employed. Determining which model to use given one's data is a statistical problem (Goldman, 1993). We used the approach outlined by Huelsenbeck and Crandall (1997) to test alternative models of evolu- tion, employing PAUP* and Modeltest (Posada & Crandall, 1998). A starting tree was obtained using neighbour-joining. With this tree, likelihood scores were calculated for various models of evolution and compared using a chi-square test,
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