Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al.

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Zootaxa 3731 (4): 589–598

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http://dx.doi.org/10.11646/zootaxa.3731.4.10

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Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti?

A reply to Balakirev et al. (2013)

ALICE LATINNE1, YANNICK CHAVAL2, SURACHIT WAENGSOTHORN3, PRATEEP ROJANADILOK4,

KRAIRAT EIAMAMPAI5, KRIANGSAK SRIBUAROD6, VINCENT HERBRETEAU7, SERGE MORAND8,9

& JOHAN R. MICHAUX1, 2

1Conservation Genetics Unit, University of Liege, Liège, Belgium. E-mail: [email protected], UMR1062 CBGP, Campus international de Baillarguet, Montferrier-sur-Lez, France3Environment and Resources Technology Department, Thailand Institute of Scientific and Technological Research, Pathum Thani,

Thailand4Doi Chiangdao Wildlife Research Station, Chiang Mai, Thailand5Bung Boraphet Wildlife Research Station, Nakhon Sawan, Thailand6Khlong Saeng Wildlife Research Station, Surat Thani, Thailand7IRD, UMR ESPACE-DEV (IRD, UM2, UAG, UR), Station SEAS-OI, F-97410 Saint-Pierre, France8Institut des Sciences de l’Evolution, CNRS-IRD-UM2, Université de Montpellier 2, F-34093, Montpellier, France9Walai Rukhavej Botanical Research Institute, Mahasarakham University, Maha Sarakham 44150 Thailand

Abstract

Recently, Balakirev et al. (2013) presented a taxonomic revision of the genus Leopoldamys based on phylogenetic analy-

ses. They identified five main Leopoldamys genetic lineages and suggested to rename several of them. According to these

authors, the genetic lineage previously thought to belong to L. edwardsi (lineage L1) should be assigned to L. revertens

while L. neilli (lineage L2) should be considered as a junior synonym of L. herberti. Using molecular and morphological

data from a large sampling of Leopoldamys specimens, the aim of the present study was to investigate the taxonomic status

of L. herberti and L. neilli. This study reveals that, contrary to Balakirev et al.’s statement, both genetic lineages L1 and

L2 occur in Nakhon Ratchasima Province, close to the type locality of L. herberti. We also show that the external mea-

surements and color pattern of L. herberti are highly similar to those of L1 specimens but are not consistent with the mor-

phology of L2 specimens. Therefore these results strongly suggest that L. herberti should be assigned to the genetic

lineage L1. Consequently L. neilli should not be considered as a junior synonym of L. herberti and this study confirms

that the appropriate name of the genetic lineage L2 is L. neilli. Moreover, as our results show that L. herberti should be

assigned to the lineage L1, this name has nomenclatural priority over L. revertens, the species name suggested by Bala-

kirev et al. (2013) for this lineage.

Key words: Leopoldamys, long-tailed giant rats, Thailand, Indochina, Murinae rodents

Introduction

The genus Leopoldamys Ellerman, 1941 comprises several species of long-tailed giant rats living in forests of

Southeast Asia, and extending into northeast India and southern China. Recent studies of the taxonomy of Murinae

rodents in Thailand based on molecular data recovered three main Leopoldamys phylogenetic lineages that were

assigned to the three Leopoldamys species traditionally recognized in Thailand (Latinne et al. 2012, 2013; Pages et

al. 2010). One of these lineages is distributed in southern Thailand and has been identified as L. sabanus (Thomas,

1887), another one is present in northern Thailand and has been assigned to L. edwardsi (Thomas, 1882) whereas

the last one has been found exclusively in limestone karsts of continental Thailand and was identified as L. neilli

(Marshall, 1977). The last-mentioned identification was supported by Pages et al. (2010) using sequences obtained

from the holotype specimen of this species. Recently, Balakirev et al. (2013) presented a quite different taxonomic

arrangement of the genus. They identified five main Leopoldamys genetic lineages and suggested to rename several

Accepted by P. Velazco: 14 Oct. 2013; published: 1 Nov. 2013 589

https://www.researchgate.net/publication/236217993_Revision_of_the_genus_Leopoldamys_Rodentia_Muridae_as_inferred_from_morphological_and_molecular_data_with_a_special_emphasis_on_the_species_composition_in_continental_Indochina?el=1_x_8&enrichId=rgreq-854628d6-4f6d-443d-bf4f-bd66dc195a6d&enrichSource=Y292ZXJQYWdlOzI1ODI1ODM0MztBUzo5OTAwNzIzMzc4OTk1MkAxNDAwNjE2NTc0Njc4

https://www.researchgate.net/publication/44690329_Revisiting_the_taxonomy_of_the_Rattini_tribe_a_phylogeny-based_delimitation_of_species_boundaries_BMC_Evol_Biol_10184?el=1_x_8&enrichId=rgreq-854628d6-4f6d-443d-bf4f-bd66dc195a6d&enrichSource=Y292ZXJQYWdlOzI1ODI1ODM0MztBUzo5OTAwNzIzMzc4OTk1MkAxNDAwNjE2NTc0Njc4


of them. According to these authors, the Indochinese genetic lineage previously thought to belong to L. edwardsi

(lineage L1) should be assigned to L. revertens (Robinson & Kloss, 1922) while L. neilli (lineage L2) should be

considered as a junior synonym of L. herberti (Kloss, 1916).

Leopoldamys herberti, described from a single specimen from Nakhon Ratchasima Province (central

Thailand), was considered by Musser & Carleton (2005) as a synonym of L. sabanus. However, both Balakirev et

al. (2013) and Latinne et al. (2013) have showed that L. sabanus is a Sundaic species that is restricted in Indochina

to southern Thailand (with a northern range limit in Kanchanaburi Province). According to these results, L. herberti

should therefore not be considered as a synonym of L. sabanus. Furthermore, Balakirev et al. (2013) suggested that

the external characteristics of L. herberti are strongly consistent with the morphological description of L. neilli.

They also claimed that the genetic lineage assigned to L. neilli (lineage L2) was the sole Leopoldamys lineage

occurring in Nakhon Ratchasima Province where the holotype of L. herberti was collected. Accordingly, these

authors speculated that L. neilli was a junior synonym of herberti. However, Balakirev et al. (2013) did not

compare the external morphology of the Leopoldamys lineages occurring in Thailand with the holotype of L.

herberti neither did they check whether other genetic Leopoldamys genetic lineages might exist in Nakhon

Ratchasima Province. For these reasons, the decision of Balakirev et al. (2013) to consider L. neilli as a junior

synonym of L. herberti appears premature.

Using molecular and morphological data from a large sampling of Leopoldamys specimens from Thailand and

Indochina, the aim of the present study was to investigate the taxonomic status of L. herberti and L. neilli by

answering the following questions: Is the lineage L2 the sole Leopoldamys lineage occurring in Nakhon

Ratchasima Province? Is the external morphology of the type specimen of L. herberti consistent with the

morphology of L2 specimens and the holotype of L. neilli specimens?

Material and methods

Sampling. One hundred twenty-one Leopoldamys samples collected by our team in continental Thailand,

Cambodia and Lao PDR were used in this study. Several of them were previously included in the studies of Pages

et al. (2010), Latinne et al. (2012, 2013), and Balakirev et al. (2013). Two museum specimens from Nakhon

Ratchasima Province (Sakaerat, Pak Thong Chai district) belonging to the rodent collection of the Centre for Thai

National Reference Collections (CTNRC) (reference numbers: CTNRC 54-1549 and CTNRC 54-1550) were also

added to our dataset. To allow an accurate morphological comparison with the L. herberti holotype specimen (an

adult male), all samples included in our morphological study were adult males that had reached sexual maturity.

Molecular identification of Leopoldamys specimens. To avoid species misidentifications, all our samples

were unambiguously identified using DNA sequencing and phylogenetic analysis.

Fresh samples (tissues in ethanol): The cytochrome b gene (Cytb) and/or the cytochrome c oxidase subunit I

gene (COI) were amplified for all the fresh samples as described in Pages et al. (2010) and Latinne et al. (2013).

Haplotypes were identified using ARLEQUIN 3.11 (Excoffier et al. 2005). Phylogenetic reconstructions were

performed on the combined dataset using the Maximum Likelihood (ML) and Bayesian inference (BI) approaches.

Maxomys and Niviventer sequences were used as outgroups in our phylogenetic trees. The most suitable model of

DNA substitution for each locus and dataset was determined using MODELTEST 3.0 (Posada & Crandall 1998)

according to the Akaike Information Criterion (AIC). ML analyses were performed using PhyML 3.0 (Guindon et

al. 2010). Robustness of the tree was assessed by 1000 bootstrap replicates. MRBAYES 3.1.1. (Ronquist &

Huelsenbeck 2003) was used to perform Bayesian analyses. Metropolis-coupled Markov chain Monte Carlo

(MCMC) sampling was performed with 5 chains run for 3 million generations with one tree sampled every 1000

generations, using default parameters as starting values. A 50% Majority-rule consensus tree was then generated in

PAUP 4.0b10 with burn-in values of 100,000 generations (Swofford 1998).

Museum samples (dried skins): As museum samples contained only small quantity of degraded DNA, we

amplified a 85 base pairs (bp) fragment of the Cytb gene that proved to be suitable for amplification of ancient

DNA and to allow to discriminate among most vertebrate species (Teletchea et al. 2008) and more specifically

Rattini species (Galan et al. 2012; Latinne et al. 2013; Pages et al. 2010). DNA extraction was performed using the

QIAamp DNA Micro Kit (Qiagen) following the protocol for isolation of genomic DNA from tissues in a

physically remote area in ancient DNA laboratory where Leopoldamys samples were never processed before this

LATINNE ET AL.590 · Zootaxa 3731 (4) © 2013 Magnolia Press

https://www.researchgate.net/publication/24238444_ARLEQUIN_Ver_30_An_integrated_software_package_for_population_genetic_data_analysis?el=1_x_8&enrichId=rgreq-854628d6-4f6d-443d-bf4f-bd66dc195a6d&enrichSource=Y292ZXJQYWdlOzI1ODI1ODM0MztBUzo5OTAwNzIzMzc4OTk1MkAxNDAwNjE2NTc0Njc4

https://www.researchgate.net/publication/256461634_Diversity_and_endemism_of_Murinae_rodents_in_Thai_limestone_karsts?el=1_x_8&enrichId=rgreq-854628d6-4f6d-443d-bf4f-bd66dc195a6d&enrichSource=Y292ZXJQYWdlOzI1ODI1ODM0MztBUzo5OTAwNzIzMzc4OTk1MkAxNDAwNjE2NTc0Njc4









study. The precautions and criteria pertinent for ancient DNA studies were observed during all laboratory

procedures (Gilbert et al. 2005). Amplifications were carried out using the primers LLedw (5’-

GATAAAATTCCATTCCACCC-3’) and HLedw (5’-TAATTGTCTGGGTCTCC-3’) following the protocol

described in Latinne et al. (2013). The 85 bp Cytb fragment obtained from our museum samples was then

compared with other Leopoldamys sequences to identify diagnostically informative attributes allowing

discrimination between Leopoldamys lineages.

Morphological analysis. In order to investigate the morphological differences between the Leopoldamys

lineages L1 and L2, size differences among them were assessed using analyses of variance (one-way ANOVA) on

three linear measurements (head+body length, tail length, hind foot length) of adult males. Our sampling for this

morphological analysis comprises 33 L1 specimens (including the two museum samples from Nakhon Ratchasima)

and 92 L2 specimens (including two paratypes of L. neilli from the United States National Museum of Natural

History [NMNH], catalogue numbers: NMNH 533481, NMNH 533482). The measurements of the L. herberti

holotype specimen (available in Kloss [1916]) and those of the L. neilli holotype specimen (deposited in the

collection of the CTNRC [Waengsothorn et al. 2009]) were then compared with those of L1 and L2 specimens

using box-and-whisker plots.

Results

Phylogenetic analysis. Cytochrome b and COI sequences were obtained for 103 and 119 Leopoldamys samples,

respectively. The final alignment includes 52 combined haplotypes (Cytb + COI) (see Table 1 for GenBank

accession numbers of haplotypes). The ML and BI trees of the combined dataset give congruent results and retrieve

two main lineages, the lineages L1 and L2 already evidenced by Balakirev et al. (2013) (Fig. 1). These well-

supported lineages are subdivided into the sublineages L1a (southern Indochina), L1b (northern Indochina), L2a

(northern and northeastern Thailand), L2b (central Thailand), L2c (central Thailand), L2d (western Thailand) and

L2f (Lao PDR) following the nomenclature of Balakirev et al. (2013).

TABLE 1. Lineage, haplotype ID numbers, and GenBank accession numbers for the Leopoldamys samples used in this

study.

Lineage Haplotype Country Cytb COI Source

L1a C0421 Cambodia / KF577939 This study

C0446 Cambodia / KF577940 This study

L1b R3419 Thailand HM217414 HM217543 Pages et al. 2010

HL65 Thailand KC010034 KC010175 Latinne et al. 2013






R3446 Thailand / KF577944 This study

R3624 Thailand KF577948 KF577934 This study







L0431 Lao PDR / KF577941 This study

......continued on the next page

Zootaxa 3731 (4) © 2013 Magnolia Press · 591TAXONOMIC STATUS OF LEOPOLDAMYS HERBERTI AND L. NEILLI



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Museum samples identification. The sequences of the 85 bp fragment amplified for the two museum samples

from Nakhon Ratchasima Province (CTNRC 54-1549, 54-1550) are similar and identical to one of the four L1

variants of this fragment (L1b-1) (Fig. 2). This variant is distributed in northern and northeastern Thailand. The

other three L1 variants (L1b-2, L1b-3, L1b-4) differ from the museum sequences by only one base pair. The L2

variants are much more divergent and differ from the museum sequences by at least 10 base pairs (Fig. 2). The

sequence from the L. neilli holotype is identical to one of the L2 variants (L2b) distributed in central Thailand.

Three pure characteristic attributes (attributes that exist across all variants of a single clade and never in any other

clade according to the definition of Sarkar et al. [2008]) have been identified between the lineages L1 and L2 and

allow unambiguous discrimination of these lineages (Fig. 2).

TABLE 1. (Continued)

Lineage Haplotype Country Cytb COI Source


L2a HL17 Thailand HM219591 HM219573 Latinne et al. 2013

HL18 Thailand HM219592 HM219573 Latinne et al. 2013







HL29 Thailand JQ081357 HM219578 Latinne et al. 2013


HL57 Thailand HM219593 JQ081314 Latinne et al. 2013


HL59 Thailand JQ081365 JQ081316 Latinne et al. 2013

L2b HL31 Thailand HM219600 HM219580 Latinne et al. 2013


L2c HL35 Thailand HM219603 HM219583 Latinne et al. 2013






L2d HL44 Thailand HM219606 HM219586 Latinne et al. 2013



HL47 Thailand JQ081362 HM219588 Latinne et al. 2013






HL62 Thailand JQ081368 JQ081318 Latinne et al. 2013

L2f LK0222 Lao PDR KF577947 KF577933 This study




FIGURE 1. ML phylogenetic tree (GTR+Γ) of combined haplotypes (Cytb + COI). Numbers above branches indicate ML

bootstrap support values (BS) and numbers below branches indicate Bayesian posterior probabilities (BPP). Well-supported

clades are represented by BS values > 75% and by BPP values ≥ 0.95.



FIGURE 2. Comparison of the 85 bp Cytb fragment obtained from our museum samples (CTNRC 54-1549, 54-1550) with

lineages L1 and L2 and the L. neilli holotype specimen (sequence from Pages et al. [2010], GenBank accession number:

HM235947). Identical positions as those of the sequences from museum samples are indicated by dots. Pure characteristic

attributes allowing discrimination between lineages L1 and L2 are outlined in black.

Morphological analysis. All external measurements of adult males show highly significant differences

between the lineages L1 and L2 according to the ANOVAs of tail length (F = 495.03 – p < 0.0001 – df = 1), hind

foot length (F = 146.43 – p < 0.0001 – df = 1) and head+body length (F = 83.54 – p < 0.0001 – df = 1). For each of

these three measurements, individuals of lineage L1 average significantly larger than those of lineage L2.

Differences in tail length, hind foot length and head+body length distinguish 96.8%, 91.2% and 87.2% of adult

males for the two genetic lineages, respectively. Therefore, these three measurements and especially tail length, can

be used to discriminate the lineages L1 and L2 and assign the holotype L. herberti to one of them.

According to these results, the external measurements of the L. herberti holotype specimen are undoubtedly

consistent with those of the lineage L1 rather than lineage L2 (Fig. 3). Indeed tail length of the L. herberti holotype

clearly falls within the range of L1 specimens and is much larger than observed for L2 specimens. Hind foot length

and head+body length of L. herberti are also highly similar to the median values of L1 specimens and larger than

the median values of L2 specimens. All measurements of the L. neilli holotype specimen are similar to those of L2

specimens.

Discussion

Is the lineage L2 the sole Leopoldamys lineage occurring in Nakhon Ratchasima province?

Balakirev et al. (2013) claimed that genetic lineage L2 (assigned to L. neilli) was the sole Leopoldamys lineage

occurring in Nakhon Ratchasima Province because no other genetic lineages have been recorded in this region

despite the considerable number of localities sampled in Latinne et al. (2011). However, the present study clearly

reveals the presence of L1 specimens in Nakhon Ratchasima Province, based on two museum samples identified

using a small Cytb fragment (Fig. 2). These specimens were captured in Sakaerat area, in the Pak Thong Chai

district of Nakhon Ratchasima Province, about sixty kilometers away from Pak Chong where the holotype of L.

herberti was collected (Kloss 1916). Therefore, our results demonstrate that both lineages L1 and L2 occur in the

vicinity of the L. herberti type locality.

Is the external morphology of Leopoldamys herberti consistent with the morphology of L. neilli specimens

(lineage L2)?

The external measurements of the holotype of Leopoldamys herberti and especially its tail length clearly

demonstrate its morphological similarity to specimens of lineage L1 and distinction from specimens of lineage L2

(Fig. 3). The external description of L. herberti also closely matches the color pattern of our L1 specimens.

According to Kloss (1916), the upperparts of L. herberti are “clay-colour streaked with black by the tips of the

hairs. This grizzling is most pronounced dorsally. The limbs are duller and browner. Top of muzzle and a ring

round the eye are pale clove-brown.” Its underparts are “white, this colour extending over the upper lip to include

the tip of the nose and part of the vibrissae roots, projecting upwards to reach the dark eye-ring.” Its feet are “white

with brown centres” and its tail is bicolored (Kloss 1916). Exactly similar color pattern has been observed on our

L1 specimens while the typical L2 specimens are duller and darker brown and the white fur on their upper lip does

not reach their vibrissae or eye-ring (Fig. 4). Therefore, based on its external measurements and color pattern, it is

clear that the holotype of L. herberti should be associated with lineage L1 rather than with lineage L2.




FIGURE 3. Box-and-whisker plots of tail length (A), hind foot length (B) and head+body length (C) for adult males belonging

to lineages L1 (n=33) and L2 (n=92) represented together with L. herberti and L. neilli holotypes measurements.



FIGURE 4. Pictures of typical L1 specimen (sample R4918, photograph by Vincent Herbreteau) (A) and L2 specimen (sample

L400, photograph by Alice Latinne) (B).

Which names for the lineages L1 and L2?

We demonstrated that both genetic lineages L1 and L2 occur in Nakhon Ratchasima Province, close to the type

locality of Leopoldamys herberti. We also show that in external measurements and color pattern the holotype of L.

herberti is highly similar to specimens of lineage L1 but not consistent with the morphology of lineage L2

specimens. Contrary to the conclusions of Balakirev et al. (2013), we conclude that the name L. herberti should be

assigned to the genetic lineage L1. Consequently, L. neilli is not a junior synonym of L. herberti and the

appropriate name of the genetic lineage L2 is L. neilli, as suggested by Pages et al. (2010) on the basis of Cytb

sequences obtained from the holotype of this species.

In their taxonomic revision, Balakirev et al. (2013) also considered that the lineage L1 should be regarded as a

distinct species from L. edwardsi (lineage L3 according to their nomenclature) and identified L. revertens

(Robinson & Kloss, 1922) as the earliest available name for lineage L1. However, as our results suggest that L.

herberti (Kloss, 1916) should be assigned to the lineage L1, this name is here identified as the earliest available

name for this lineage, with L. revertens as a junior subjective synonym.





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Conclusion

Five main Leopoldamys genetic lineages have been delimitated and named by Balakirev et al. (2013) in their

taxonomic revision of the genus. Based on the results of the present study, we propose to revise their nomenclature

as follows: lineage L1 = L. herberti (instead of L. revertens), L2 = L. neilli (instead of L. herberti), L3 = L.

edwardsi, L4 = L. milleti, and L5 = L. sabanus. Leopoldamys ciliatus and L. siporanus, two additional

Leopoldamys species recognized by Musser & Carleton (2005), were not included in the study of Balakirev et al.

(2013) or in our study. Future taxonomic studies based on independent data (mitochondrial and nuclear markers,

morphology) and geographically broader large sampling will be required to confirm these propositions and further

improve the taxonomy of the Leopoldamys genus.

Acknowledgements

First of all, we warmly thank all our collaborators who made sample collection in the field possible and especially

Boonchai Tontan, Sathaporn Jittapalapong and Kittipong Chaisiri. We also thank Marie Pages for her advices about

extraction and amplification of DNA from museum samples. This work was supported by a Belgian FRS-FNRS

(Fonds de la Recherche Scientifique) fellowship to A. Latinne (“Aspirant”) and to J.R. Michaux (“Maître de

recherches”), and a financial grant from the Belgian FRS-FNRS (“crédits pour brefs séjours à l’étranger” to A.

Latinne and J.R. Michaux and credits from the “Fonds de la Recherche Fondamentale Collective (FRFC)” to J.R.

Michaux), from the University of Liège (Patrimoine) and from the Communauté française de Belgique. A. Latinne

also thanks VOCATIO (Belgian Foundation of Vocation) for its financial support. This study is part of the

“CERoPath project” (Community Ecology of Rodents and their Pathogens in South-East Asia: effects of

biodiversity changes and implications in health ecology, www.ceropath.org), ANR Biodiversity ANR 07 BDIV

012, and the “BiodivHealthSEA project”, ANR CP&ES 11 CPEL 002, both funded by the French National Agency

for Research.

References

Balakirev, A.E., Abramov, A.V. & Rozhnov, V.V. (2013) Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred

from morphological and molecular data, with a special emphasis on the species composition in continental Indochina.

Zootaxa, 3640, 521–549.


Ellerman, J.R. (1941) The families and genera of living rodents. Vol. 2. Family Muridae. British Museum (Natural History),

London, 690 pp.

Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): An integrated software package for population genetics

data analysis. Evolutionary Bioinformatics, 1, 47–50.

Galan, M., Pagès, M. & Cosson, J.-F. (2012) Next-Generation sequencing for rodent barcoding: species identification from

fresh, degraded and environmental samples. PLoS ONE, 7, e48374.

http://dx.doi.org/10.1371/journal.pone.0048374

Gilbert, M.T.P., Bandelt, H.J., Hofreiter, M. & Barnes, I. (2005) Assessing ancient DNA studies. Trends in Ecology &

Evolution, 20, 541–544.

http://dx.doi.org/10.1016/j.tree.2005.07.005

Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to

estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.

Kloss, C.B. (1916) On a collection of mammals from Siam. Journal of the Natural History Society of Siam, 2, 1–32.

Latinne, A., Waengsothorn, S., Herbreteau, V. & Michaux, J.R. (2011) Evidence of complex phylogeographic structure for the

threatened rodent Leopoldamys neilli, in Southeast Asia. Conservation Genetics, 12, 1495–1511.

http://dx.doi.org/10.1007/s10592-011-0248-3

Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. (2012) Combined

mitochondrial and nuclear markers revealed a deep vicariant history for Leopoldamys neilli, a cave-dwelling rodent of

Thailand. PLoS ONE, 7, e47670.


Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. (2013) Diversity and endemism

of Murinae rodents in Thai limestone karsts. Systematics and Biodiversity, 11, 323–344.

http://dx.doi.org/10.1080/14772000.2013.818587







http://dx.doi.org/10.1007/s10592-011-0248-3

http://dx.doi.org/10.1007/s10592-011-0248-3


http://dx.doi.org/10.1080/14772000.2013.818587

http://dx.doi.org/10.1080/14772000.2013.818587


Marshall, J.D. (1977) Rats and mice of Thailand. In: Lekagul, B. & McNeely, J.A. (Eds.), Mammals of Thailand. Saha Karn

Bhaet Bangkok, Thailand, pp. 395–490.

Musser, G.G. & Carleton, M. (2005) Superfamily Muroidea. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal species of the

World: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp. 894–1531.

Pages, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.F., Hugot, J.P., Morand, S. & Michaux, J. (2010) Revisiting

the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evolutionary Biology, 10,

184.

http://dx.doi.org/10.1186/1471-2148-10-184

Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

http://dx.doi.org/10.1093/bioinformatics/14.9.817

Robinson, H.C. & Kloss, C.B. (1922) V.—New mammals from French Indo-China and Siam. Journal of Natural History Series

9, 9, 87–99.

http://dx.doi.org/10.1080/00222932208632642

Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19,

1572–1574.

http://dx.doi.org/10.1093/bioinformatics/btg180

Sarkar, I.N., Planet, P.J. & Desalle, R. (2008) CAOS software for use in character-based DNA barcoding. Molecular Ecology

Resources, 8, 1256–1259.

http://dx.doi.org/10.1111/j.1755-0998.2008.02235.x

Swofford, D.L. (1998) PAUP*. Phylogenetic Analysis Using Parsimony, (*and other methods). Version 4. Sinauer Associates,

Sunderland, Massachusetts.

Teletchea, F., Bernillon, J., Duffraisse, M., Laudet, V. & Hanni, C. (2008) Molecular identification of vertebrate species by

oligonucleotide microarray in food and forensic samples. Journal of Applied Ecology, 45, 967–975.

http://dx.doi.org/10.1111/j.1365-2664.2007.01415.x

Thomas, O. (1882) Description of a new species of rat from China. Proceedings of Zoological Society of London, 50, 587–588.

Thomas, O. (1887) Description of a new rat from North Borneo. Annals and Magazine of Natural History, series 5, 20, 269–

270.

http://dx.doi.org/10.1080/00222938709460053

Waengsothorn, S., Kenthao, A., Latinne, A. & Hugot, J.P. (2009) Rodents within the Centre for Thai National Reference

Collections (CTNRC), past, present and future. Kasetsart Journal Natural Sciences, 43, 118–124.


http://dx.doi.org/10.1186/1471-2148-10-184



http://dx.doi.org/10.1080/00222932208632642

http://dx.doi.org/10.1080/00222932208632642




http://dx.doi.org/10.1111/j.1755-0998.2008.02235.x

http://dx.doi.org/10.1111/j.1755-0998.2008.02235.x

http://dx.doi.org/10.1111/j.1365-2664.2007.01415.x

http://dx.doi.org/10.1111/j.1365-2664.2007.01415.x

http://dx.doi.org/10.1080/00222938709460053

http://dx.doi.org/10.1080/00222938709460053

http://dx.doi.org/10.1080/00222938709460053

Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al.

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