sign in sign up
<<
Home , Monitor lizard, Varanus (Hapturosaurus)

eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 1

herPetoZoA 30 (1/2): 9 - 20 9 Wien, 30. Juli 2017

New findings on the relationships among tree monitor of the prasinus (S chleGel , 1839) complex (: Sauria: )

Neue erkenntnisse zur Verwandtschaft innerhalb der neuguineischen Baumwarane aus dem Varanus prasinus (S chleGel , 1839) - Komplex (Squamata: Sauria: Varanidae)

BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

KurZfASSuNG

Gewebeproben von 36 Waranen neun unterschiedlicher Arten aus dem Varanus prasinus (S chleGel , 1839) - Komplex wurden hinsichtlich eines 519 bp fragments des mitochondrialen 16S Gens zur erhellung ihrer Verwandtschaftsbeziehungen untersucht. der datensatz, der die ersten Sequenzdaten von V. reisingeri eideN - müller & W icKer , 2005 und V. bogerti merteNS , 1950 enthält, wurde mit publizierten Sequenzdaten ( ZieGler et al. 2007) verglichen. die vorliegenden ergebnisse bestätigten frühere Studien und deuten darüber hinaus auf eine unerwartet nahe phylogenetische Verwandtschaft von V. bogerti mit V. kordensis hin. obwohl sichtbare unter- schiede in färbung, Pholidose und den meßwerten zwischen V. reisingeri und V. prasinus vorhanden sind, war ein genetischer unterschied in den mitochondrialen Sequenzen zwischen diesen beiden taxa nicht feststellbar. die neuen erkenntnisse werden hinsichtlich der Biogeographie der Neuguinea-region diskutiert. ABStrAct

tissue samples of 36 monitor lizards of nine species of the Varanus prasinus (S chleGel , 1839) complex were investigated regarding a 519 bp fragment of the mitochondrial 16S gene to elucidate their systematic rela - tionships. the dataset, which contains the first sequence data for V. reisingeri eideNmüller & W icKer , 2005, and V. bogerti merteNS , 1950, was aligned to published sequence data (ZieGler et al. 2007). the present results gen - erally support the findings of an older study, and furthermore propose an unexpected close phylogenetic relation - ship of V. bogerti to V. kordensis (A. B. m eyer , 1874) . despite of obvious differences in coloration, pholidosis, and morphometrics, no sign of molecular differentiation in the studied mitochondrial sequence data was detected between V. reisingeri and V. prasinus. the new findings are discussed in the light of the biogeography of the New Guinea region. Key WordS reptilia: Squamata: Sauria: Varanidae; Hapturosaurus , Varanus prasinus complex, Varanus bogerti , Varanus reisingeri , mitochondrial 16S gene, systematics, New Guinea region

iNtroductioN

Within the varanid subgenus Hapturo- which does not occur in any other species of saurus BucKlitSch ,Böhme & K och , 2016 , monitor . the curved claws are very the mem bers of the highly arboreal Varanus sharp. in the palmar, plantar, and subdigi - prasinus (S chleGel , 1839) group share a tal regions, several scales form cushion-like set of characteristic and synapormorphic arrangements that are somewhat adhesive. morphological features, clearly separating All these morphological features are eco - them from their more terrestrial sister group logical adaptations to a highly specialized of the V. indicus (dAudiN , 1802) complex arboreal life style, enabling these monitor of the subgenus Euprepiosaurus fitZiNGer , lizards to venture out on the thin, outer tree 1843 ( BucKlitSch et al. 2016). the body is branches in the rainforest canopy, inacces - al ways fairly long and slender with consid - sible to other congeneric species ( GreeNe erably long legs, and a prehensile , 1986). eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 2

10 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

the geographical distribution of the & J AcoBS , 2001, from Batanta island, the members of the V. prasinus complex is re- black and yellow V. boehmei JAcoBS , 2003, stricted to New Guinea and several offshore from Waigeo island, and the yellow-green V. islands. one species, V. keithhornei (WellS reisingeri eideNmüller & W icKer 2005, & W elliNGtoN , 1985), inhabits the cape from misol island. other species, such as V. york Peninsula of (fig. 1). Among telenesetes SPrAcKlANd , 1991 from rossel the members of the complex, V. prasinus island or V. bogerti merteNS , 1950, inhabit - has by far the widest distribution; it covers ing the trobriand, d’entrecasteaux and the entire land mass of New Guinea and the louisiade islands off southeastern New small islands of the torres Strait separating Guinea are known only from a single or a northern Australia from New Guinea. few historical voucher specimens, respec - Notably, there exist unconfirmed but trust - tively ( Koch et al. 2014). the phylogenet - worthy observations and reports of green ic relationships between the various mem - tree monitor lizards from the cape york bers of the V. prasinus group were first in- Peninsula (see references in lemm 2014), vestigated by ZieGler et al. (2007), but in substantiating the possibility of a sympatric this initial study not all taxa involved were occurrence of two tree spe - available. hence, samples of V. telenesetes , cies. V. bogerti and the recently de scribed V. despite their partly colorful appear - reisingeri were lacking. the present study ance and up to 120 cm total length, several aims to remedy this lack of information in species of tree monitor lizards were order to elucidate the systematic relation - described only in recent years. these are ships of the New Guinea tree monitor liz- the light blue and black V. macraei Böhme ards.

mAteriAlS ANd methodS

the authors obtained blood samples of 2014). Varanus caerulivirens ZieGler , 23 monitor lizards of the V. prasinus com - Böhme & P hiliPP , 1999, of the V. indicus plex from dr. markus Baur, head of the rep - (d AudiN , 1802) species group, the sister tile sanctuary at munich, including six sam - of the tree monitor lizards, was chosen ples of specimens that were identified as V. as outgroup sample. reisingeri , based on their distinctive black Andreas SchmitZ (Geneva ) provided a and yellow coloration. All these specimens sequence of the mitochondrial 16S gene of a were confiscated by German customs at specimen of V. bogerti (Bishop museum, frankfurt Airport, a major hub in europe for honolulu, hawaii, uSA - BPBm 16053) the international trade with exotic obtained using the same primers as given (VAlAorAS 1998; AuliyA 2003). in addi - below . the newly gen erated sequences tion, blood samples were obtained from ten were aligned to 20 16S sequences of moni - specimens held in private collections in tor lizards of the V. prasinus complex that Germany. the taxonomic allocations of all were found in the NcBi (National center specimens were based on their external for Biotechnology information) database appearance as compared with an illustrated Genbank ®. they all were published by identification key ( Koch et al. 2013) and the ZieGler et al. (2007), who applied the same respective original species descriptions. primers used for this study (see below). tissue samples of V. telenesetes (QmJ1190) for analysis of the mitochondrial 16S and V. keithhornei (QmJ65052) were kindly gene, dNA extractions were carried out, by provided by Patrick couPer (Queensland vacuum extraction, using a vacuum extrac - museum Brisbane, Queensland, Australia). tion kit (Pall Gmbh, dreieich, Germany), A sequence from the sample of V. telene - following the instructions of the manufac - setes was not obtained, probably due to the turer. dNA concentration was checked long-time preservation of the specimen col - elektrophoretically. A 532 bp fragment of lected about 100 years ago ( Koch et al. the mitochondrial 16S gene was amplified eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 3

New findings on the relationships within the Varanus prasinus complex 11

by Pcr, using primers as published by pairwise distances was computed (table 1). VeNceS et al. 2005 (forward: 16SA-l, maximum likelihood analyses were run in 5’-cGcctGtttAtcAAAAAcAt-3’; re - PAuP 4.01 ( SWofford 2001), performing a verse: 16SB-h, 5’-ccGGtctGA ActcA heuristic search, applying tBr (tree-Bisec - GAtcAcGt-3’). Pcr reactions were run tion-reconnection) branch swapping and with 1 μl dNA template, 2.5 μl reaction computing 1000 bootstrap replicates. Just Buffer (PeqGold), 2.5 μl 2.5 mm dNtPs, as for Bayesian analyses (fig. 2), evolution - 0.5 μl taq Polymerase (Peqlab), 16.5 μl ary models were used, which were found h2o, and 10 pmol of each primer. reaction using jmodeltest ( PoSAdA 2008) under mixes were processed by the following pro - assumptions of Aic (Akaike’s information tocol: initial denaturation: 180 s at 94 °c; criterion). denaturation: 15 s at 94 °c; hy bridization: Bayesian analyses were run in 60 s at 51 °c; elongation: 60 s at 72 °c; mrBayes v3.1.2. ( roNQuiSt & h uelSeN- repeated for 39 cycles; final elongation: 120 BecK 2003). four markov chains were run s at 72 °c. Sequencing the Pcr products twice for 2,000,000 generations, sampling was done at the laboratories of the Bio - every 100th generation. the increase in diversität und Klima - forschungs zentrum likelihoods was checked by visualizing the (BiK-f), frankfurt am main. p-files provided by the program in an Sequences were automatically aligned, eXcel spreadsheet. the first 1,000 gener - applying the clustalW Algorithm ( lArKiN ations were discarded as “burn in”. the et al. 2007) as implanted in meGA.5 soft - Genbank ® accession numbers of the newly ware ( tAmurA et al. 2011); alignments were acquired sequences are provided in table 1. checked manually. A matrix of uncorrected,

reSultS

the results obtained are generally in from the other specimens of the V. kordensis accordance with the findings of earlier clade. Six of the seven samples assigned to authors ( ZieGler et al. 2007) regarding the V. kordensis share a common haplotype, molecular phylogenetic relationships be- from which specimen Kor6 differs by only tween the different species of the V. prasi - 0.2 % uncorrected sequence distance (p-dis - nus complex. As in the previous study by tance). from this common haplotype, the ZieGler et al. (2007), all samples of V. kor - sequence of V. bogerti differs by a p-dis - densis form a well-supported clade, the sis - tance value of 1.2 % and the sequence of ter group to all other taxa in the phylogram ZfmK 70604 by 1.0 %. the p-distance (fig. 2). however, the sample of V. bogerti value between the sequences of V. bogerti lies embedded in this clade, separated from and ZfmK 70604 is 1.7 %, which explains the other specimens only by a quite long the problems of the Bayesian analysis to branch length. in the maximum likelihood resolve the relationships within this clade. Analysis, and a preliminary Neighbor Join- Another well-defined but weakly re- ing Analysis, V. bogerti was positioned as solved clade contains the samples assigned sister group to V. kordensis . Since this gene- to V. macraei , V. boehmei , V. prasinus and V. alogical grouping was supported by very reisingeri . Within this clade, the three sam - weak bootstrap values only, the V. bogerti ples of V. boehmei (two from ZieGler et al. clade collapsed. Another puzzling peculiar - 2007: ZfmK 77837, ZfmK 79122 and a ity regarding this clade is caused by a sam - new sample: Boe1) are grouped together as ple of the Zoologisches forschungsmuseum a distinct subclade. they all share a com - Alexander Koenig, Bonn (ZfmK 70604) mon haplotype. Similarly, the samples as - from ZieGler et al. (2007) which these signed to V. prasinus and V. reisingeri form authors had labeled V. cf. prasinus . in the a separate sub clade. the samples assigned heat map graphic (not shown), these two to V. macraei that all share the same haplo - aforementioned samples are well separated type, form a basal polytomy, from which eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 4

12 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

fig. 1: Geographical distributions of the members of the Varanus prasinus complex in the region of New Guinea and northern Australia. Abb. 1: Geographische Verbreitung der Arten des Varanus prasinus -Komplexes im Gebiet von Neuguinea und dem nördlichen Australien.

these two groupings arise. however, in a are considered the sister clade to the clade less conservative phylogenetic analysis, V. of V. macraei / V. prasinus / V. reisingeri , boehmei might well be considered a sister although this grouping is not well-support - clade to V. macraei , V. prasinus , and V. ed. however, three samples that were as- reisingeri (see mP and NJ trees in ZieGler signed to V. prasinus (cf. PrA 7, PrA 3) et al. 2007). the p-distance values between and V. reisingeri (rei 3) are positioned V. boehmei and the V. prasinus / V. reisingeri within this clade, as a basal polytomy to V. clade are 1.6 – 1.9 % (on average 1.6 ± beccarii . these samples sharing a common 0.001 %), those between V. boehmei and V. haplotype are separated from the rest of the macraei are 1.4 ± 0 %. the specimens col - V. prasinus / V. reisingeri samples by p-dis - orwise assigned to V. reisingeri are not tances of 2.3 – 2.7 % (on average 2.4 ± delimitable from most of the V. prasinus 0.0014 %), whereas the p-distances to V. samples. ten of the 14 samples within this beccarii are merely 0.4 – 0.6 % (on average clade share a common haplotype. this hap - 0.4 ± 0.0007 %). to verify this unexpected lotype was found in four samples of V. pras - finding, i.e., to rule out the possibility that inus and six of V. reisingeri . Average p-dis - this is an artifact caused by cross contami - tances between the V. prasinus / V. reisingeri nation, these three samples were run again clade and the single haplotype found in V. in an independent trial (from dNA extrac - macraei are only 0.2 – 0.6 % (on average tion on). however, the authors ob tained the 0.3 ± 0.001 %). same result in the second run and thus are in accordance to ZieGler et al. (2007), confident, that the results are correct (but V. keithhornei and V. beccarii doriA , 1874, see discussion). eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 5

New findings on the relationships within the Varanus prasinus complex 13

fig. 2: Bayesian phylogram of the combined datasets. Numbers above branches are posterior probability values from Bayesian analysis, numbers below branches are bootstrap values from maximum likelihood analysis, inferred from 1,000 pseudoreplicates. Abb. 2: Phylogramm der kombinierten datensätze nach Bayesianischer Analyse. Zahlen über den Ästen sind Posterior Probability-Werte der Bayesianischen Analyse. Zahlen unter den Ästen sind Bootstrapwerte (1000 Pseudoreplikationen) der maximum likelihood Analyse.

diScuSSioN

Within monitor lizards , the V. indicus monitor lizard groups broadly co-exist on complex is regarded to be the sister group New Guinea and its surrounding islands, of the V. prasinus group ( Böhme 1988; where they sympatrically inhabit evergreen SPrAcKlANd 1991; ASt 2001; ZieG ler et al. tropical rainforests. hypothetically, once 2007). Genetically, this split was dated at the evolutionary split between the V. indicus the early about 20 million years group and the V. prasinus group had oc- ago (mya) by VidAl et al. (2012). Both curred (possibly through sympatric specia - eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 6

14 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

table 1 (this and opposite page): matrix of uncorrected, pairwise distances. the table reads from the left page to the right page, its upper portion being continued in the lower portion.

tion resulting from ecological divergence), bright markings representing the last com - greater New Guinea was probably inhabited mon ancestor of all modern tree monitor by a predominantly black colored, tree dwel - lizards. With increasing global tempera - ling, prehensile tailed monitor lizard with tures and consequently rising sea levels dur - eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 7

New findings on the relationships within the Varanus prasinus complex 15

tab. 1 (diese und gegenüberliegende Seite): matrix der unkorrigierten, paarweisen Abstände. leserichtung von der linken zur rechten Seite, wobei der untere tabellenblock die fortsetzung des oberen darstellt.

ing the Pliocene (with a maximum about 3.5 various local tree monitor populations mya), some areas of this formerly contigu - became geographically and genetically iso - ous landmass around New Guinea were lated, giving rise to divergent evolutionary divided into distinct smaller islands and the lineages and disjunctive insular distribution eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 8

16 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

patterns as was the case in many other the northern hemisphere during the Pliocene Australo-Papuan vertebrates (see e.g., and particularly during the following Plei - heAdS 2002; r AWliNGS & d oNNellAN stocene, global sea levels repeatedly drop- 2003; o utlAW & V oelKer 2008). ped substantially ( JoNGSmA 1970; c hAPPell it can be assumed that the last com - & S hAcKletoN 1986). from the mon ancestor of the members of the sub - to the early Pliocene (ca. 33.8 to 2.5 mya) genera Euprepiosaurus and Hapturosaurus sea levels changed by an altitude of about was a generalist, as is the case in most indo- 30 to 60 meters, while greater changes only Australian varanids ( horN & V iSSer 1991; began during the ( miller et al. BeNNett 1998; KiNG & G reeN 1999). the 2005). Associated with the glaciation evolutionary split into the strictly tree events during this period, the sea level in the dwelling taxa of the V. prasinus complex area lowered and rose substantially and re- and the more terrestrial taxa of the V. indicus peatedly ( heAtWole 1987; VoriS 2000) de - complex could be explained by specializing pending on cold and warm periods during in certain food preferences and availability. glacification. for instance, about 130,000 most likely, the green background col - years ago, sea levels off the north-eastern oration of some members of the V. prasinus coast of New Guinea were 60 to 80 meters complex evolved as an adaption to their life lower than today ( mcculloch et al. 1999). in the foliage of the canopy. in this special As a consequence of falling sea levels, Aus- environment, being of green color repre - tralia, New Guinea, and the associated off - sents a selective advantage since it provides shore islands, many of which are under camouflage. thus, GreeNe (1986) regarded water today, were united in a contiguous the green coloration in V. prasinus as a landmass connected by the currently sub - derived character state and an adaptation to merged continental Sahul shelf. strongly arboreal habits. members of the V. Accordingly, land bridges between the prasinus comple x mostly feed in the upper islands formed and disappeared, connecting tree canopies ( irWiN 1994), and accordingly, and disconnecting repeatedly during each stomach content studies mainly detected glacial and interglacial period, enabling katydid s and other arthropods ( GreeNe populations of animals to segregate and mix 1986), whereas members of the V. indicus genetically. the longer the forested land complex mainly forage in the lower vegeta - bridges existed, the longer animals could tion and on the ground (but see Koch et al. migrate in both directions and the exchange 2009), and often also near the shoreline. of genetic information was increased. Ac- consequently, PhiliPP et al. (2007) revealed cording to heAtWole (1987), about 14,000 that a high percentage of prey items found years ago, as large amounts of water were in stomachs of their V. indicus study group bound through the glaciation in the northern consisted of crusta ceans, and hemisphere, the sea level in the area was vertebrates (especially skinks). only in the about 120 m below its present level and examined specimens of V. jobiensis the food Australia, New Guinea, and most of their consisted of a large proportion of offshore islands were united in a contiguous (PhiliPP et al. 2007). landmass, which was probably inhabited by the area of New Guinea, northern tree dwelling, prehensile-tailed monitor Australia, and the neighboring islands expe - lizards, in areas where suitable habitats rienced a very dynamic geological and cli - occurred. matological history ( heANey 1991; hAll & the authors of this paper are con - holloWAy 1998; lohmAN et al. 2011) that vinced that the aforementioned climatologi - most likely played an important role in the cal, ecological, and zoogeographic factors diversification of tree monitor lizards induced the radiation and distribution of the (ZieGler et al. 2007). their dispersion V. prasinus subgroup and, thus interpret the began at the miocene-Pliocene transition results of their molecular investigation in about five to six mya ( VidAl et al. 2012), an the light of these repeated events. epoch characterized by a global sea level under these past conditions which minimum ( outlAW & V oelKer 2008). also affected the raya Ampat Archipelago Associated with cyclical glaciation events in (west of New Guinea), Batanta island, the eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 9

New findings on the relationships within the Varanus prasinus complex 17

distribution range of V. macraei , was repeat - a plausible explanation why V. boehmei is edly connected to New Guinea. these two well differentiated from its closest con - islands’ tight geographical connection and geners in the data set studied (fig. 2). the close genetic affiliation of V. macraei to According to VoriS (2000), the sea level V. prasinus as discovered by ZieGler et al. would have to be more than 120 m below (2007) and supported by the present study, the present conditions to connect Waigeo suggest that introgression and hybridization island to New Guinea which was only the during glacial periods with overland con - case during Pleistocene glacial maxima, that nections between former island territories is, less than 10 % of the time during the last are probably responsible for the presented 250,000 years before present ( VoriS 2000). phylogenetic findings. the relatively pronounced genetic differ - When global sea levels were 30 meters ences between V. beccarii and V. prasinus below present levels, also misol island, the correspond well to the greater spatial dis - range of V. reisingeri , was connected to tance between those islands of the Aru Archi- mainland New Guinea ( VoriS 2000). Be - pelago (southwest of New Guinea) and New cause of the pronounced differences in col - Guinea, although both land masses were oration, scalation and overall appearance it connected by a land bridge, when the sea may be intuitively assumed that V. reisingeri level was just 40 m below the present level was geographically isolated from V. prasi - (VoriS 2000). nus for a longer period of time than V. mac - the close genetic affiliation of three raei . Such an assumption, however, is not samples of V. prasinus and V. reisingeri supported by the phylogenetic estimates pre - (PrA 3, cf. PrA 7, and rei 3), respective - sented here. Whether or not these external ly, to the V. beccarii clade (fig. 2), suggests morphological differences strictly corre - a paraphyletic status V. prasinus , which is spond to the geographical range, with yellow hard to interpret in the absence of reliable specimens being restricted to misol island, locality data, in particular since the voucher while emerald green being exclusive to New specimen of cf. PrA 7 (Smf99805) has the Guinea, awaits confirmation by comparison typical coloration of V. prasinus . one pos - of voucher s pecimens with detailed locality sible, however very theoretical, explanation data or observations from the field. State- would require a common south-central New ments of local reptile dealers are not reliable Guinean origin of the specimens PrA 3, cf. since they often obscure the exact origin of PrA 7, and rei 3, while the rest of the V. traded specimens. in this regard, it is worth prasinus samples stem from Western , mentioning that captive specimens of V. rei - where most specimens are collected for the singeri changed their coloration from yel - pet trade ( luX moore 1988; luX moore & low to green, possibly depending on nutri - GroomBridGe 1990; JeNKiNS & B roAd tion or artificial lighting (d. KielmANN pers. 1994). According to VoriS ’ (2000) pale - comm.) WeiJolA (pers. comm.) mentioned, omaps, the land bridge persisted longest that V. reisingeri was clearly distinguished between the islands of the Aru Archipelago from V. prasinus when a different mitochon - and the central southern coast of New drial dNA sequence (e.g., Nd4) was ana - Guinea. A population level study incorpo - lyzed. rating a larger number of specimens of V. the present results regarding V. prasinus from many different localities boehmei are in accordance with those of across the huge land mass of New Guinea is ZieGler et al. (2007) in that this species is a needed to clarify this biogeographic as- close relative of V. macraei and V. prasinus . sumption. however, despite the abundance Varanus boehmei is restricted to Waigeo of tree monitor lizards in the pet trade island, located just about 50 km north of (ShePherd et al. 2005; PerNettA 2009; New Guinea’s Vogelkop Peninsula. how- Koch et al. 2013), there are few voucher ever, the sea between Waigeo island and specimens with detailed locality data in Western Papua is comparatively deep and international museum collections (A. Koch , thus, Waigeo island was separated from the pers. observ.). main island for a considerably longer time the V. kordensis / V. bogerti clade is than Batanta or misol islands, which offers well separated from the other members of eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 10

18 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

the V. prasinus complex, which accords well one can assume, that V. prasinus specimens with the assumption, that Biak island from easily accessible and regul arly visited (northwest of New Guinea), the range of V. localities on New Guinea are overrepresent - kordensis , was not connected to mainland ed, so that the entire genetic diversity within New Guinea, even when sea levels in the V. prasinus is not fully reflected by the data - region were as much as 120 m below the set under study. Varanus prasinus shows present level ( VoriS 2000). Although, there some variation in color pattern across the are clear genetic differences between these entire distribution range that may correlate two species in the investigated gene frag - with geographic distance ( Koch et al. 2014). ment, these differences seem rather subtle, obviously, the V. prasinus group given the huge geographic distance of more experienced a higher diversification rate in than 1,800 km between their respective dis - the western parts of its distribution range tribution ranges ( V. bogerti: d’entre - than in the east with V. beccarii , V. boehmei , casteaux and trobriand Archipelagos, east - V. kordensis , V. macraei and V. reisingeri ern ). Since both species being restricted to islands off the indonesian occur on islands only 50 km (for V. korden - part of New Guinea (the province called sis on Biak island) and less than 10 km (for Papua, formerly known as irian Jaya), while V. bogerti on fergusson island) away from merely V. bogerti and V. keithhornei (and the the next populations of V. prasinus (Koch et dubious taxon telenesetes ) occur on islands al. 2014), one would expect that each off the coast of Papua New Guinea and on species is more closely related to the neigh - the Australian mainland (fig. 1). on the boring populations of V. prasinus than with other hand, the islands off southeastern New each other. the authors could, however, Guinea, namely the trobriand, d’entre - only compare with sequences of V. prasinus casteaux and louisiade archipelagos, are collected for the pet trade and, consequent - severely underexplored as to their (herpeto) ly, lack exact and reliable locality data. A faunas ( BouleNGer 1895a, 1895b; heAt - dataset incorporating V. prasinus specimens Wole 1975; KrAuS & S heA 2005). there - from the neighborhood of V. kordensis and fore, future field work may reveal further V. bogerti may result in a better understand - undescribed tree monitor taxa from these ing of the phylogeographic relationships. remote island groups.

AcKNoWledGmeNtS

the authors would like say thank you to markus (A. Koch) and Sam Sweet (university of california, Baur (münchen), frank mohr (Würzburg), claudia Santa Barbara, uSA) contributed his observation of richter (mannheim), and Steffen Vökler (coburg), cape york tree monitor lizards. Arne Schulze (hes- who gave permission to take blood samples from the sisches landesmuseum darmstadt, formerly at Sen- animals. tissue samples of V. telenesetes and V. keith - ckenberg museum, frankfurt, Germany) and Andreas hornei were kindly provided by Patrick couper Schmitz (muséum d’histoire Naturelle, Genève, (Queensland museum, Brisbane, Qld., Australia). Switzerland) assisted in obtaining sequence data of the Also, the support by markus Schmidbauer (munich, V. bogerti sample that was kindly provided by Germany), Gunther Schmida (lower Beechmont, Aus- Pumehana imada, lydia Garetano, and Allen Allison tralia), and manfred reisinger (essenbach, Germany) (all Bishop museum, hawaii, uSA). Special thanks for providing photographs of tree monitor lizards is are due to Paul horner (cannonvale, Qld., Australia) acknowledged. dietmar Kielmann (overath, Ger - and robert Neal (Brisbane, Qld., Australia), who made many) kindly shared his observations about color helpful comments on earlier drafts. change in tree monitor lizards with one of the authors

refereNceS

ASt , J. c. (2001): mitochondrial dNA evidence in the 1990s with a focus on Germany. Brussels (traffic and evolution in (Squamata).- cladistics, europe), pp. 107. Westport etc.; 17: 211-226. BAVerStocK , P. r. & K iNG , d. & K iNG , m. & AuliyA , m. (2003): hot trade in cool creatures - Birrell , J. & K rieG , m . (1993): the evolution of spe - A review of the live reptile trade in the european union cies of the Varanidae: microcomplement fixation analy - eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 11

New findings on the relationships within the Varanus prasinus complex 19

sis of serum albumins.- Australian Journal of Zoology, tralia, Vol. 1A. canberra (Australian Government Pub - collingwood; 41: 621-638. lication Service). BeNNett , d. (1998): monitor lizards: Natural horN , h.-G. & V iSSer , G. J. (1991): Basic data history, biology & husbandry. frankfurt a. m. (edition on the biology of monitors; pp. 176-187. in: Böhme , W. chimaira), pp. 352. & horN , h. G. (eds.): Advances in monitor re search.- Böhme , W. (1988): Zur Genitalmorphologie der mertensiella, Bonn; Vol. 2. Sauria: funktionelle und stammesgeschichtliche As pekte.- icZN [international commission on Zoological Bonner Zoologische monographien, Bonn; 27: 1-176. Nomenclature] (2001): opinion 1970: Odatria keith - Böhme W. & J AcoBS , h. J . (2001): Varanus hornei WellS & W elliNGtoN , 1985 (reptilia: Squa - macraei sp. n., eine neue Waranart der V. prasinus -Grup - mata): specific name placed on the official list.– Bulletin pe aus West irian, indonesien.- herpetofauna, Weinstadt; of Zoological Nomenclature, london; 58 (1): 74-75. 23: 5-10. irWiN , S. (1994): Notes on behaviour and diet of BouleNGer , G. A. ( 1895a): on a collection of Varanus teriae SPrAcKlANd , 1991.- memoirs of the and batrachians from ferguson island, d’entre - Queensland museum, Brisbane; 35 (1):128. casteaux Group, British New Guinea.- Annals and maga- JAcoBS h. J. (2003): A further new emerald tree zine of Natural history, london; 16: 28-32. monitor lizard of the Varanus prasinus species group BouleNGer , G. A. (1895b): descriptions of two from Waigeo, West irian (Squamata: Sauria: Varani - new reptiles obtained by mr. A. S. meek in the tro briand dae).- Salamandra, rheinbach; 39: 65-74. islands, British New Guinea.- Annals and magazine of JeNKiNS , m. & B roAd , S. (199 4): international Natural history, london; 6: 408-409. trade in reptile skins: A review and analysis of the main BucKlitSch , y. & B öhme , W. & K och , A. (2016): consumer markets. 1983-91. cambridge (traffic inter - Scale morphology and micro-structure of monitor national), pp. 68. lizards (Squamata: Varanidae: Varanus spp.) and their JoNGSmA , d. (1970): eustatic sea level changes allies: implications for systematics, ecology, and conser - in the Arafura Sea.- Nature, london; 228: 150-151 . vation.- Zootaxa, Auckland; 4153: 1-192. KiNG , d. & G reeN , B. (1999): monitors: the chAPPell , J. & S hAcKletoN , N. J . (1986): biology of varanid lizards. malabar (Krieger), pp. 116. oxygen isotopes and sea level.- Nature, london; 324: Koch , A. & A ridA , e. & S chmitZ , A. & B öhme , 137-140. W. & Z ieGler , t. (2009): refining the polytypic species collAr , d. c. & S chulte , ii J. A. & l oSoS , J. B. concept of mangrove monitors (Squamata: Varanus indi - (2011): evolution of extreme body size disparity in mon - cus group): a new cryptic species from the talaud itor lizards ( Varanus ).- evolution, hamburg; 65 (9): islands, , reveals the underestimated diversity 2664-2680. of indo-Australian monitor lizards.- Australian Journal coNrAd , J. l. & A St , J. c. & m oNtANAri , S. & of Zoology, collingwood; 57: 29-40. Norell , m. A. (2011): A combined evidence phyloge - Koch , A. & e rNSt , N. & e ideNmüller , B. & netic analysis of (reptilia: Squamata).- KrAuS , f . (2014): New data on the rare Varanus bo- cladistics, Westport etc.; 27 (3): 230-277. gerti merteNS , 1950 and V. telenesetes SPrAcKlANd , dAudiN , f. m. (1802): histoire naturelle, 1991 (Squamata: Varanidae), two locally endemic générale et particulière des reptiles. tome troisième. monitor lizards from island groups off southeastern Paris (f. dufart), pp. 384. New Guinea.- herpetological Journal, london; 24: del cANto , r. (2013): field observations on Va - 111-122. ranus macraei .- Biawak, rockville centre; 7 (1): 18-20. Koch , A. & Z ieGler , t. & B öhme , W. & A ridA , eideNmüller , B. & W icKer , r. (2005): eine e. & A uliyA , m. ( 2013): Pressing problems: distribution, weitere neue Waranart aus dem Varanus prasinus -Kom - threats, and conservation status of the monitor lizards plex von der insel misol, indonesien.- Sauria, Berlin; 27 (Varanidae: Varanus spp.) of and the (1):3-8. indo-Australian Archipelago.- herpetological conserv- fuller , S. & B AVerStocK , P. & K iNG , d. (1998): ation and Biology, [WWW internet ressource]; 8: 1-62. Biogeographic origins of (Varanidae): a molec - KrAuS , f. & S heA , G. (2005): Additional reptile ular perspective.- molecular Phylogenetics and and range extensions for milne Bay evolution, San diego; 9 (2): 294-307. Province, Papua New Guinea.- herpetological review, GordoN , A. l. (2005): oceanography of the New york; 36: 471-473. indo nesian seas and their throughflow.- oceanography, lArKiN , m. A. & B lAcKShieldS , G. & B roWN , Virginia Beach; 18: 14–27. N. P. & c heNNA , r. & m cGettiGAN , P. A. & m c- GreeNe , h. W. (1986): diet and arboreality in the WilliAm , h. & V AleNtiN , f. & W AllAce , i. m. & W ilm , emerald monitor, Varanus prasinus , with comments on A. & l oPeZ , r. & t homPSoN , J. d. & G iBSoN , t. J. & the study of adaptation.- fieldiana: Zoology (New hiGGiNS , d. G. (2007): clustal W and clustal X version Series), chicago; 31: 1-12. 2.0.- Bioinformatics, oxford; 23 (21): 2947-2948. hAll , r. & h olloWAy , J. d . (eds.) (1998): Bio - lemm , J. ( 2014): Keen on green: Natural history geography and geological evolution of Se Asia. leiden and captive breeding of Green tree monitors ( Varanus (Backhuys Publishers), pp. 417. pra sinus ).- herp Nation magazine, Sacramento; 16: 32- heAdS , m. (2002): of paradise, vicariance 39. biogeography and terrane tectonics in New Guinea.– lohmAN , d. J. & de BruyN , m. & P AGe , t. & Journal of Biogeography, oxford; 29: 261-283. VoN riNteleN , K. & h All , r. & N G, P. K. l. & S hih , h.- heANey , l. r. (1991): A synopsis of climatic and t. & c ArVAlho , G. r. & VoN riNteleN , t. (2011): vegetational change in Southeast Asia.- climatic Biogeography of the indo-Australian Archipelago.- change, dordrecht; 19: 53-61. Annual review of ecology, evolution, and Systematics, heAtWole , h. (1987): major components and Palo Alto; 42: 205-226. distribution of the terrestrial fauna; pp. 101-135. in: luXmoore , r. ( 1988): Significant trade in wild - dyNe , G. r. & WAltoN , d. W. (eds.): fauna of Aus - life: A review of selected species in citeS Appendix ii. eidenmueller_Koch_Koehler_Wicker_Varanus_prasinus_systematics:herPetoZoA.qxd 07.08.2017 18:05 Seite 12

20 BerNd eideNmüller & A Ndré Koch & J ohANNeS Köhler & r udolf WicKer

Volume 2. reptiles and invertebrates. lausanne (citeS ShePherd , c. & K ecSe -N AGy , K. & P APP , d. Secretariat), pp. 306. (2005): emerald monitor lizards.- traffic Bulletin, luXmoore , r. & G roomBridGe , B. ( 1990): cambridge; 20: 113. Asian monitor lizards - A review of distribution, status, SPrAcKlANd , r. (1991): taxonomic review of exploitation and trade in four selected species. lausanne the Varanus prasinus group with description of two new (citeS Secretariat), pp. 195. species.- memoirs of the Queensland museum, mcculloch , m. t. & t udhoPe , A. W. & e SAt , t. Brisbane; 30 (3):561-576. m. & m ortimer , G. e. & c hAPPell , J. & P illANS , B. & SWofford , d. l. (2001): Phylogenetic Analysis chiVAS , A. r. & o murA , A. (1999): coral record of using Parsimony (*and other methods). Version 4. equatorial sea-surface temperatures during the pen - Sunderland (Sinauer Associates) [software package]. ultimate deglaciation at huon Peninsula.- Science, tAmurA , K. & P eterSoN , d. & P eterSoN , N. & Washington; 283: 202-204. Stecher , G. & N ei , m. & K umAr , S. (2011) : meGA5: merteNS , r. (1950): Notes on some indo-Aus - molecular evolutionary genetics analysis using maxi - tralian monitors.- American museum Novitates, New mum likelihood, evolutionary distance, and maximum york; 1456:1-7. parsimony methods.- molecular Biology and evol ution, miller , K. G. & K omiNZ , m. A. & B roWNiNG , J. oxford; 28 (10):2731-2739. V. & W riGht , J. d. & m ouNtAiN , G. S. & K AtZ , m. e. & VAlAorAS , G. (1998): monitoring of wildlife SuGArmAN , P. J. & c rAmer , B. S. & c hriStie -B licK , N. trade in the european union: Assessing the effectiveness & P eKAr , S. f. (2005 ): the Phanerozoic record of glob - of eu citeS import policies. Brussels (traffic europe), al sea-level change.- Science, Washington; 310: 1293- pp. 112. 1298. VeNceS , m. & t homAS , m. & VAN der meiJdeN , muNdheNK , K. (2008): two observations of cap - A. & c hiAri , y. & V ieiteS , d. r. (2005): comparative tured Green tree monitors ( Varanus prasinus ) in the performance of the 16S rrNA gene in dNA barcoding western province of Papua New Guinea.- Biawak, of .- frontiers in Zoology, london; 2: 5. rockville centre; 2 (3):119-120. VidAl , N. & m AriN , J. & S ASSi , J. & B Atti - outlAW , d. c. & V oelKer , G. (2008): Pliocene StuZZi , f. u. & d oNNellAN , S. & f itch , A. J. & f ry , B. climatic change in insular Southeast Asia as an engine of G. & V oNK , f. J. & r odriGueZ de lA VeGA , r. c. & diversification in Ficedula flycatchers.- Journal of coulouX , A. & h edGeS , S. B. (2012): molecular evi - Biogeography, oxford; 35: 739-752. dence for an Asian origin of monitor lizards followed by PerNettA , A. P. (2009): monitoring the trade: tertiary dispersals to Africa and .- Biology using the citeS database to examine the global trade in letters, london; 8: 853-855. live monitor lizards ( Varanus spp.).- Biawak, rockville VoriS , h. K. (2000): maps of Pleistocene sea centre; 3: 37-45. levels in Southeast Asia - shorelines, river systems and PhiliPP , K. m. & Z ieGler , t. & B öhme , W . time durations.- Journal of Biogeography, oxford; 27: (2007): Preliminary investigations on the natural diet of 1153-1167. six monitor lizard species of the Varanus (Euprepio - ZieGler , t. & B öhme , W. (1997): Genitalstruk - saurus ) indicus group.- mertensiella, rheinbach; 16: turen und Paarungsbiologie bei squamaten reptilien, 336-345. speziell den , mit Bemerkungen zur Systema - PoSAdA , d. (2008): jmodeltest 0.1.1: Phylo - tik.- mertensiella, rheinbach; 8: 1-207 genetic model Averaging. WWW ressource available at ZieGler , t. & B öhme , W. & P hiliPP , K. m. < https://github.com/ddarriba/jmodeltest2 > [last ac- (1999 ): Varanus caerulivirens sp. n., a new monitor liz - cessed: december 10, 2016 ard of the V. indicus group from halmahera, moluccas, rAWliNGS , l. h. & d oNNellAN , S. (2003): Phy - indonesia.- herpetozoa, Wien; 12: 45-56. logeographic analysis of the green python, Morelia ZieGler , t. & S chmitZ , A. & K och , A. & B öh - viridis , reveals cryptic diversity.- molecular Phylo - me , W. (2007): A review of the subgenus Euprepiosau - genetics and evolution, San diego; 27: 36-44. rus of Varanus : morphological and molecular phyloge - roNQuiSt , f. & h uelSeNBecK , J. P. (2003): ny, distribution and zoogeography, with an identification mrBayes 3: Bayesian phylogenetic inference under key for the members of the V. indicus and V. prasinus mixed models.- Bioinformatics, oxford; 19: 1572-1574. species groups.- Zootaxa, Auckland; 1472:1-28.

dAte of SuBmiSSioN: may 30, 2016 corresponding editor: heinz Grillitsch

AuthorS: Bernd eideNmüller (corresponding author < [email protected] >) 1) , André Koch 2) , Johannes Köhler 3) & rudolf WicKer 4) 1) Griesheimer ufer 53, 65933 frankfurt a. m., Germany; 2) Zoologisches forschungsmuseum Alexander Koenig, leibniz institute for Biodiversity, Adenauer - allee 160, d-53113 Bonn, Germany; 3) Zoological Garden frankfurt a. m., Alfred-Brehm-Platz 16, 60316 frankfurt a. m., Germany; 4) An der Schwarzbachmühle 55, 60529 frankfurt a. m., Germany.