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Homoplastic evolution

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Homoplastic evolution of external colouration in Asian stoutnewts (Pachytriton) inferred from molecular phylogenyYUNKE WU,YUEZHAO WANG,KE JIANG,XIN CHEN &JAMES HANKENSubmitted: 13 January 2009Accepted: 21 June 2009doi:10.1111/j.1463-6409.2009.00400.xWu, Y., Wang, Y., Jiang, K., Chen, X. & Hanken, J. (2009). Homoplastic evolution ofexternal colouration in Asian stout newts (Pachytriton) inferred from molecular phylog-eny.—Zoologica Scripta, **, ***–***.The Asian stout newts of the genus Pachytriton (Salamandridae) inhabit montane streamsin south-eastern China. Despite their abundance in the pet trade, the phylogeny and sys-tematics of this genus are poorly understood. Colouration is often used to delimit speciesunder the assumption that consistent chromatic differences characterize independent evolu-tionary lineages. We present the first phylogenetic study of Pachytriton that incorporates2.35 kb of mitochondrial DNA (ND2, cytb) and 1.2 kb of nuclear sequence data (RAG-1)along with morphometric characters to infer evolutionary relationships and patterns of col-our evolution among the three described species: Pachytriton brevipes, Pachytriton labiatusand Pachytriton archospotus. Our results support the monophyly of Pachytriton and recoverP. archospotus as the sister taxon to P. brevipes. Monophyly of P. labiatus is significantlyrejected: south-western populations are sister to the group of P. brevipes plus P. archospotus,whereas north-eastern populations nest with P. brevipes. The two geographic units are fur-ther separated by multivariate morphological analyses. South-western P. labiatus is the typespecies; misidentification of north-eastern populations as P. labiatus results from their simi-lar colouration. An unspotted, dark brown dorsum is the likely ancestral state for thegenus, whereas black-spotted colouration characterized the common ancestor of P. brevipes,P. archospotus, and north-eastern P. labiatus and was secondarily lost in the latter group.Homoplastic evolution and intraspecific variation render colour pattern in Pachytriton anunreliable character for delimiting species boundaries. North-eastern populations of P. lab-iatus are declining as the result of human collection and habitat destruction and are inurgent need of conservation protection.Corresponding author: Yunke Wu, 26 Oxford St., Museum of Comparative Zoology, HarvardUniversity, Cambridge, MA 02138, USA. E-mail: [email protected] Wang, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan610041, China. E-mail: [email protected] Jiang, College of Life Sciences, China West Normal University, Nanchong, Sichuan 637002,China. E-mail: [email protected] Chen, Key Laboratory of Bio-resources and Eco-environment, Ministry of Education, College ofLife Sciences, Sichuan University, Chengdu, Sichuan 610064, China. E-mail: [email protected] Hanken, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138,USA E-mail: [email protected] booming utilization of molecular techniques andassociated analytical tools has facilitated reassessment ofevolutionary relationships that previously were inferredmainly by analysis of phenotypic variation. Phylogeniesderived from molecular data may confirm, supplement andsometimes reject traditional taxonomic assessments. Thelatter instance often yields new evolutionary hypotheses toexplain the incongruence between molecular data andother phenotypic characters (e.g. Schaeferet al. 2002;Garcı´a-Parı´set al. 2003; Babiket al. 2005). In vertebratephylogenetics, mitochondrial DNA (mtDNA) is a fre-quently used marker for molecular analysis because it gen-erally evolves faster than nuclear genes (Ballard &Whitlock 2004). The typically one-fourth coalescent timeof mtDNA, in comparison with autosomal nuclear genes,offers an advantage for studies of closely related speciesin which lineage sorting of ancestral gene copies mayª 2009 The Authors. Journal compilation ª 2009 The Norwegian Academy of Science and LettersdZoologica Scripta, 2009 1confound the gene tree with the true species tree (Moore1995). However, in most cases, mitochondrial genes are alllinked as a single molecule, which provides only one inde-pendent estimate of the phylogeny and such results maybe misleading if there has been mitochondrial introgres-sion. As advocated by integrative taxonomists, the combi-nation of multiple lines of evidence, including independentmolecular markers, morphology, behaviour, ecology, etc.,yields the most informative and insightful evaluation ofevolutionary relationships among species (Padialet al.2009).The Asian stout newts of the genusPachytritonare pop-ular in the global pet trade. In nature, they inhabit tinyshallow montane streams across south-eastern China, alarge geographical area that is characterized by severalmountain ranges that approach 2500 m in elevation. Thesemountains were uplifted by folding and deformation of theEarth’s crust in polyphasic inherited orogenies from theLate Permian through the Cenozoic (Guo 1998). Betweenadjacent mountain ranges lie lower plains and large riversystems, which constitute zoogeographical barriers tomontane salamanders (Fu & Zeng 2008; Shepard & Bur-brink 2008). Additionally, most areas of East Asia werenot glaciated during the Pleistocene (Williamset al. 1998).In situations such as this, we can expect that the combina-tion of complex topography and long-term persistence ofpopulations on isolated mountain peaks may promotesignificant levels of interspecific and intraspecific geneticdifferentiation, as well as geographically based phenotypicdivergence.For a long time,Pachytritonwas believed to comprisejust two species:Pachytriton brevipesSauvage, the black-spotted stout newt, andPachytriton labiatusUnterstein, theunspotted stout newt. As their common names imply,these two species are distinguished mainly by external col-our pattern. Recently, a third species,Pachytriton archospo-tusShenet al., was described from a population previouslyregarded asP.brevipes, which it resembles in colouration.And while phylogenetic relationships ofPachytritonwithother Asian salamandrids are well resolved, the genusforms a well-supported, monophyletic group withPara-mesotritonandCynops(Titus & Larson 1995; Chanet al.2001; Weisrocket al. 2006; Steinfartzet al. 2007); phylo-genetic relationships withinPachytritonhave not beenassessed in detail, largely because of the difficulty ofobtaining


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