Mammalian Biology 87 (2017) 62–70
Contents lists available at ScienceDirect
Mammalian Biology
journal homepage: www.elsevier.com/locate/mambio
Original investigation
Javan mongoose or small Indian mongoose–who is where?
a,∗ b
Géraldine Veron , Andrew P. Jennings
a
Institut de Systématique, Evolution, Biodiversité, UMR 7205 ISYEB, CNRS MNHN UPMC EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités,
CP 51, 57 rue Cuvier, 75231 Paris Cedex 05, France
b
SMALL CARNIVORES - Research and Conservation, 83 St. Lawrence Street, Portland, ME, USA
a r t i c l e i n f o a b s t r a c t
Article history: The Javan mongoose Urva javanica and the small Indian mongoose Urva auropunctata have been recently
Received 16 December 2016
shown not to be conspecific. However, the limits of their respective distribution ranges have not been fully
Accepted 31 May 2017
defined. In particular, Chinese populations were not attributed to either species using molecular data.
Handled by Paul Grobler
Furthermore, the small mongooses found on Hong Kong Island (discovered at the end of the 1980s) were
Available online 13 June 2017
not clearly attributed to U. auropunctata or U. javanica, nor their status (native or introduced) established.
The main aims of this study were to: (1) investigate the intraspecific genetic diversity and structure
Keywords:
within these two species; and (2) clarify the distribution limits of U. auropunctata and U. javanica, and
Herpestidae
Asia in particular, to identify Chinese populations, and determine which species occurs on Hong Kong Island
Phylogeography (and whether they are native or introduced). The analyses of one nuclear and three mitochondrial genes
Molecular systematics confirmed the separation of U. javanica and U. auropunctata, and showed that the populations from
China southern China and Hong Kong Island belong to U. javanica. The intraspecific geographical structure of
the two species is clarified, and the taxonomic implications are discussed. In particular, we found a strong
divergence of Javan individuals of U. javanica, which should be considered a separate subspecies.
© 2017 Deutsche Gesellschaft fur¨ Saugetierkunde.¨ Published by Elsevier GmbH. All rights reserved.
Introduction over its range (Simberloff et al., 2000). Veron et al. (2007), using
mitochondrial DNA, found three distinct clades corresponding to
Nine species of mongoose occur in Asia (Patou et al., 2009a; the Javan mongoose, the small Indian mongoose, and the Indian
Gilchrist et al., 2009), and recent molecular studies have shown grey mongoose Urva edwardsii (É. Geoffroy Saint-Hilaire, 1818),
that they form a monophyletic group that should be placed in the with a mean Cytb genetic divergence of 5% between each pair of
genus Urva (Patou et al., 2009a; Egi et al., 2011; Veron et al., 2015). species. The mitochondrial analyses of Veron et al. (2007) sup-
The Javan mongoose Urva javanica (É. Geoffroy Saint-Hilaire, 1818) ported a sister relationship between U. javanica and U. edwardsii,
occurs in Southeast Asia, while the small Indian mongoose Urva whereas Patou et al. (2009a), using nuclear data, found that U.
auropunctata (Hodgson, 1836) is found from the Arabian Peninsula javanica and U. auropunctata were sister species (although the node
across the northern Indian subcontinent to Southeast Asia (Gilchrist supports in the phylogenetic trees were low).
et al., 2009; Jennings and Veron, 2011). The latter was introduced The genetic separation of U. javanica and U. auropunctata into
at the end of the 19th century and during the 20th century to many two species is supported by the morphometric study of Taylor and
different parts of the world (mainly on islands) for biological control Matheson (1999); studies of coat colour variation also concur with
of rats and snakes in plantations (Tvrtkovic and Krystufek,ˇ 1990; these results. U. javanica specimens from Vietnam and Java are red-
Simberloff et al., 2000; Thulin et al., 2006; Barun et al., 2013); it is dish, while U. auropunctata specimens from northwest India and
considered by the IUCN to be among the “100 of the world’s worst Pakistan are paler, and those from Assam and Myanmar are darker
invasive alien species” (Lowe et al., 2000). and greyish (Pocock, 1941; Corbet and Hill, 1991). This is in agree-
These mongooses were considered either as two species, or ment with our personal observation of 341 specimens from nine
as one single species (usually named Herpestes javanicus, see museums (see acknowledgements); those from Thailand, Laos and
Wozencraft, 2005 and Veron et al., 2007), varying in size and colour Java (U. javanica) are dark brown and reddish (particularly on the
head), while those from India, Nepal and Pakistan (U. auropunctata)
are paler or greyish.
∗ Even though there is genetic and morphological evidence for the
Corresponding author.
separation of the Javan mongoose and small Indian mongoose into
E-mail addresses: [email protected] (G. Veron), [email protected] (A.P. Jennings).
http://dx.doi.org/10.1016/j.mambio.2017.05.006
1616-5047/© 2017 Deutsche Gesellschaft fur¨ Saugetierkunde.¨ Published by Elsevier GmbH. All rights reserved.
G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70 63
two species, very little is known about their intraspecific genetic 201 substitution models, and gamma distribution (Lsetnst = mixed
diversity and geographical structure, and their precise distribution rates = gamma option) to sample the posterior distribution of
limits. Defining the distribution limits and the intraspecific genetic trees and to take into account the substitution model uncertainty.
diversity of these two mongooses is needed for assessing the tax- We used default priors for branch lengths and ran the chains
onomic and conservation status of these poorly studied species. for 10,000,000 Metropolis-coupled MCMC generations, with trees
Three subspecies of U. javanica and five subspecies of U. auropunc- sampled every 1000 generations, and a burn-in of 25%.
tata have been mentioned by Gilchrist et al. (2009), but their validity Trees were visualized and edited using FigTree 1.4.0 (Rambaut,
has not been tested using molecular data. Chinese populations were 2012). We compared resulting topologies and their node support;
previously assigned to the small Indian mongoose (Ellerman and nodes were considered as supported when posterior probabilities
Morrison-Scott, 1951; von Michaelis, 1972; Honacki et al., 1982; were ≥0.99 and bootstrap values were ≥70%. Genetic distances and
Taylor and Matheson, 1999), and mongooses from Hainan and Neighbor Joining trees (NJ, Saitou and Nei, 1987) were computed
southern China were grouped in the subspecies U. auropunctata using MEGA6.
rubrifrons (J. Allen, 1909) by Ellerman and Morrison-Scott (1951), We used DNAsp 5.10 (Librado and Rosas, 2009) for defining hap-
but these assertions have not been tested using molecular data. lotypes and to compute genetic diversity (haplotype and nucleotide
Furthermore, the identity and status of mongooses on Hong Kong diversity), and Network 4.6 (http://www.fluxus-engineering.com)
Island were unclear. The first record of a small mongoose on Hong to construct haplotype median-joining networks (Bandelt et al.,
Kong seems to be an individual trapped at Mai Po in 1989 (Corlett, 1999).
2001), but the identity and status (native or introduced) of this
species were uncertain, and it now seems to have largely spread
across Hong Kong (Shek et al., 2007; Lau et al., 2010). Results
The main aims of this study were to: (1) investigate the intraspe-
cific genetic diversity and geographical structure within U. javanica We obtained new sequences of the four markers for 31 indi-
and U. auropunctata; and (2) clarify the distribution limits of the viduals of U. auropunctata, U. edwardsii and U. javanica (GenBank
Javan and small Indian mongooses, and in particular, to assign numbers KY346541 to KY346606); other sequences were from pre-
Chinese populations to one of these two species, and to test vious studies (see Table 1).
which species occurs on Hong Kong Island (and whether native The fragment length, number of variable sites, number of
or introduced). For this purpose, we sequenced three mitochon- parsimony informative sites, and number of individuals used
drial fragments, Cytochrome b (Cytb), Control Region (CR) and in the phylogenetic analyses (including outgroups), were: FGB
NADH dehydrogenase subunit 2 (ND2), and one nuclear gene, Beta- (579/22/7, n = 29; Model T92+G); Cytb (1140/251/137, n = 45;
fibrinogen intron 7 (FGB). Model GTR+G+I); ND2 (276/57/35, n = 36; Model TN93+I); CR
(431/90/68; n = 19, model HKY+G+I); Cytb+ND2 (1416/308/172,
n = 45; model GTR+G+I); Cytb+ND2+FGB (GTR+G+I; 1995/330/179,
Material and methods n = 45). All phylogenetic trees (with all methods), although poorly
resolved, retrieved three main clades corresponding to the three
Both fresh (hairs or tissue) and museum samples were used in species U. javanica, U. auropunctata and U. edwardsii (Fig. 2). The
this study (Table 1, Fig. 1). Sequences of a total of 47 individuals of resolution within these clades was low. However, the individuals
U. auropunctata, U. edwardsii and U. javanica were analysed (from from southern China and Hong Kong clustered with U. javanica.
this study, previous studies, and GenBank; see Table 1). We used U. Within U. javanica (Figs. 2 and 3), the Javan individuals were a
brachyura and U. fusca as outgroups, following the results of Patou sister group to all the remaining individuals; those from north-
et al. (2009a). ern Thailand formed a well-supported group, which was sister to a
Total genomic DNA was isolated from samples following a clade that comprised individuals from China, Hong Kong and Viet-
CTAB-based protocol (Winnepenninckx et al., 1993). For museum nam and a group from central and southern Thailand. Within U.
specimen samples, Dithiothreitol (DTT; 1 M) was added during the auropunctata (Fig. 2), two clades were retrieved: one comprising
tissue lyses and the digestion time was increased (up to 72 h). We Myanmar individuals, and one containing all others (Bangladesh,
used Cytb primers from Veron et al (2004a,b), ND2 primers from Pakistan, and introduced populations that were said to come from
Perez et al. (2006) and Patou et al. (2009a), and CR primers as in India).
Patou et al. (2009b). The nuclear locus FGB was amplified using The Cytb haplotype network for U. javanica (Fig. 4; 737 sites; n:
primers from Yu and Zhang (2005). Polymerase Chain Reactions 12; h: 9; Hd: 0.9091; Pi: 0.01589; S: 47; Eta: 49) showed a hap-
(PCR) were carried out as in Patou et al. (2009a), with hybridisation logroup of three haplotypes (H2, H3, H9) from Vietnam, southern
◦ ◦ ◦
temperatures at 50 C for Cytb and ND2, 61 C for CR, and 59 for China and Hong Kong, each separated by one mutation. Another
FGB. PCR products were then purified and sequenced in both direc- haplotype from Vietnam (H8) was separated by five mutations
tions on an automated DNA sequencer by Genoscope (Evry, France) from this group. Thailand specimens were represented by four
and Eurofins (Ebersberg, France). Sequences obtained from DNA haplotypes; three from southern and central Thailand (H4, H6,
extracted from museum samples were amplified and sequenced H7) separated from the haplotype from northern Thailand (H5) by
twice to ensure their quality and authenticity. Sequences were 13–21 mutations. The haplotype from Java (H1) was separated by
edited, assembled and aligned manually, using Bioedit (version 7; 18 mutations from the closest haplotype (H9).
Hall, 1999). The Cytb haplotype network for U. auropunctata (Fig. 5; 704
Each gene was analysed individually and combined. Phyloge- sites; n: 16; h: 14; Hd: 0.942; Pi: 0.00935; S: 31; Eta: 31) showed
netic analyses were performed via Bayesian Inference (BI), using two main groups: one containing two haplotypes from Myanmar
MrBayes 3.2 (Ronquist et al., 2012) and Maximum Likelihood (H7, H8), and another comprising the haplotypes from Pakistan,
(ML), using MEGA6 (Tamura et al., 2013). For ML, the best-fitting India, Bangladesh, and introduced areas (Croatia, Fiji, Guyana,
model was estimated prior to the analyses using MEGA6, follow- Japan, and the Virgin Islands) that was separated by 28 mutations
ing the Akaike information criterion (AIC). The selected model from the first. The haplotypes from Fiji (H4) and the Virgin Islands
was then implemented in the ML analyses, in which node robust- (H3) were close to the ones from Bangladesh (H9/H10), and the hap-
ness was assessed through 1000 bootstrap replicates. For BI, lotype from Croatia (H11) was close to those from Pakistan (H12,
we used Reversible Jump Markov Chain, to sample across the H13). The haplotypes from Japan (H1, H2) were distant from all the
64 G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70 , Berlin; (1996)
Museum
. Thailand
2015)
Arnason
Prov.,
National
Naturkunde, and
Loei
(2014,
fur
al. Malaysia
Park) Park) Ledje
et
Muang,
Smithsonian
from: Museum
Rai Desert Desert
Thailand Thailand Veron
Sarawak, Bangladesh Bangladesh Bangladesh
Vietnam Ban
Vietnam USNM: SW SW SW
BZM:
Japan Japan
others
Kong
Park) Park)
Kong
Park) Forest, (Sharjah (Sharjah
Park, (2009a), Dao,
Japan Japan Park)
York; Sanctuary, Sanctuary, Village Hong
al.
study;
Hong Desert Desert
Indonesia Tam
et Museum;
Desert Bangladesh Bangladesh Bangladesh Indonesia
Po, Croatia
USA Thailand
New
this Man, Desert
Guyana Guyana
Thailand
Jhikorgacha, Jhikorgacha, Jhikorgacha, Emirates Emirates 107,
National
Tai
Samarakan Wildlife Wildlife for (Captivity) (Zoo) (Zoo) Java,
Nishihara, Nishihara,
Patou
Distr.,
(Sharjah (Sharjah Island, China Mam Dhaka, Dhaka, Dhaka,
Ontario
Gate Arab Arab
Thailand Sumatra,
Islands,
(Sharjah
History, Yen Indonesia
Tsuen,
Market, Province,
(Sharjah Khieo Khieo Po
Phuong
Tatau,
(2009), Royal
produced Locality Okinawa, Okinawa, Amamiohshima,Yamato, Amamiohshima,Yamato, Virgin Fiji Unknown Jamaica Jamaica Georgetown, Georgetown, Myanmar Myanmar Manda, Manda, Manda, Korcula Pakistan Pakistan India Ulu Nepal Teuba, Italy Bahrain Bahrain Dubai United United Iran Payradanga, Payradanga, Payradanga, ND Fiji Cheribon, Java, Vinh Canton, Kapoe, Thailand Loei Phu Phu Loei Muang, Cuc Mai Lam
Natural
ROM:
of
Zenatello
Paris; sequences
and
Museum
new
BFG KY346565 KY346566 KY346567 FJ391195 KY346568 KY346569 KY346570 FJ391194 KY346571 KY346572 KJ438326 FJ391197 KY346573 KY346574 KY346575 KY346576 KY346577 FJ391198 KY346578 FJ391191 FJ391201 FJ391202 KY346579 KY346580 KY346581 KY346582 FJ391203 KY346583 KY346584 Gaubert Naturelle,
American
represent
(2009),
bold
d’Histoire al.
in
(AMNH: et
ND2 AY170051 AY873843 FJ391226 AY974031 KY346541 KY346542 KY346543 KY346544 KY346545 KY346546 KY346547 KY346548 KJ438317 KY346549 AY974029 KY346550 KY346551 KY346552 KY346553 KY346554 KY346555 FJ391230 KY346556 AY170050 FJ391231 KY346557 FJ391233 KY346558 KY346559 FJ391234 KY346560 KY346561 KY346562 KY346563 KY346564 National
number Bennett numbers
,
Muséum
(2007)
accession al.
#
CR FJ411052 FJ411053 KY346591 KY346592 KY346593 KY346594 KY346595 FJ687485 KY346596 KY346597 KY346598 KY346599 KY346600 KY346601 KY346602 KY346603 KY346604 KY346605 KY346606 et
MNHN:
specimen/sample
Veron
GenBank
accession
Kong;
the
Hong (2007),
al. Province). GenBank Cytb AB050128 AB050129 AB050130 AB050131 AY170108 AY873843 FJ391219 AF522338 DQ519065 DQ519064 DQ519072 DQ519069 DQ519071 DQ519068 X94926 KJ438348 KY346585 KY346586 DQ519050 DQ519053 DQ519051 DQ519049 DQ519052 DQ519054 DQ519056 AY170107 DQ391277 KY346587 AY928675 KY346588 DQ519058 DQ519073 DQ519063 DQ519059 DQ519057 DQ519061 DQ519062 DQ519060 KY346589 KY346590
number,
et
Garden,
Prov:
Morley
, Botanic
District; identification
and
(2006)
the
#
al. Distr:
Farm et
report
data;
107489 103585
Perez we no
specimen
Kadoorie or
TC220 TC221TC297 TC298TC299 TC340 TC342 TC343 DQ519070 DQ519067 TC144TC145 TC146 TC147 TC148 TC149 TC294 TC295TC296 AF522336 1999-510/C129 R3406 DQ519055 R3407 TC124 TC258 TC354 TC355 TC472 TC649/KFBGM0067-2004 TC693/KFBGM0005-2012
163188 101655102913 FJ391216 129495 590300
(ND: 293
186570/FC186570 34042 17400
(2006),
sample,
KFBG:
al.
Sample FMNH TC141/ROM TC142/ROM MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN USNM AMNH BZM MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN UVM AMNH AMNH MVZ BZM MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN MNHN et locality
each
For and
Chicago;
Koepfli
study.
number,
History,
(2004), this
#
in al.
UaAB050129 UaAB050131 UaAY873843 UaFJ411052 UaTC142 UaTC221 UaTC298 UaTC342 UbU590300 UeTC144 UeTC295 UjA101655 UjTC124 Id. UaAB050128 UaAB050130 UaAY170 UaF129495 UaFJ411053 UaTC141 UaTC220 UaTC297 UaTC299 UaTC340 UaTC343 UaX94926 UeA163188 UeB34042 UeFJ687485 UeTC145 UeTC146 UeTC147 UeTC148 UeTC149 UeTC294 UeTC296 UeUVM293 UfFiji UjA102913 UjAY928675 UjB17400 UjC129 UjM3406 UjM3407 UjTC258 UjTC354 UjTC355 UjTC472 UjTC649 UjTC693 et
Natural
GenBank
of
the Veron included
Museum
(2003),
samples History),
al.
Field auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata auropunctata brachyura edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii edwardsii fusca javanica javanica javanica javanica javanica javanica javanica javanica javanica javanica javanica javanica javanica javanica
the
et 1
of
Natural Species Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva Urva
Table List of Yoder FMNH:
G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70 65
Fig. 1. Distribution map showing the localities of the samples used in this study (done using DIVA-GIS version 7.5.0). Red: U. javanica, green: U. auropunctata, yellow: U.
edwardsii.
rest, with the closest haplotypes being from Pakistan, from which had not previously been investigated using molecular data. The
they were separated by 15 mutations. The Guyana haplotypes (H5, mongoose population from southern China, which was previously
H6) were also distant to others, with one haplotype (H6) separated attributed to U. auropunctata (based on morphology), should now
by 11 mutations from the closest haplotype (H3, from the Virgin be placed within U. javanica. However, the type locality of the Chi-
Islands), while the second one (H5) was separated from H3 by 21 nese subspecies rubrifrons (Allen, 1909) is on Hainan Island, and
mutations. unfortunately, we were not able to obtain genetic sequences from
Mean genetic distances between the three species can be found Hainan samples. Our observations of Hainan specimens (in FMNH
in Table 2. Within U. javanica, Cytb distances ranged from 0% and and AMNH) showed that they are reddish on the head, and their
2.5% (n = 14), and the most distant individuals were from Java (1.8% body coloration is brownish, which is closer to U. javanica than to
to 2.5%); the samples from northern Thailand were also quite diver- U. auropunctata. This would agree with our genetic results obtained
gent from the others (1.1% to 1.9%), including those from central for southern China and Hong Kong, but further genetic data should
and southern Thailand (1.8% to 1.9%). Within U. auropunctata, Cytb be obtained to confirm the status and distributional range of the
distances ranged from 0.2% to 3.1% (n = 17). Myanmar specimens subspecies rubrifrons.
were the most distant from the others, with distances to them rang- Chinese U. javanica individuals (from both the mainland and
ing from 2.3% to 3.1%; distances ranged from 0.2% to 1.5% between Hong Kong) were closest to those from northern Vietnam, which
the other specimens. In comparison, within U. edwardsii, Cytb dis- geographically is the nearest population. The subspecies U. j. exilis
tances ranged from 0.6% to 1.8% (n = 12); the largest distances were (Gervais, 1841) has been described for Vietnam, but further genetic
for the samples from Sumatra (1 to 1.8%), Nepal (0.2% to 1.8%), and investigations are needed to determine if southern China popula-
Bangladesh (0.8% to 1.6%). tions warrant being placed within this or a separate subspecies.
The northern Thailand specimens of U. javanica were very
divergent from others, including those from southern and central
Discussion
Thailand. This finding is not too surprising as these latter areas cor-
respond to the separation of the Indochinese and Sundaic regions,
Our results, with more comprehensive sampling and markers
near the Isthmus of Kra (Woodruff and Turner, 2009; Meijaard,
than previous studies, confirmed the separation of the Javan mon-
2009). Three subspecies have been described for Thailand: U. j. sia-
goose and small Indian mongoose as two separate species. The
mensis (Kloss, 1917) for northern Thailand, U. j. peninsulae (Schwarz,
structure of the phylogenetic tree obtained with all four mark-
1910) for central and southern Thailand, and U. j. incerta (Kloss,
ers, and the Cytb distances superior to 5% (see Baker and Bradley,
1917) for southern Thailand. Our preliminary results would tend
2006), confirmed the specific status of these taxa. These molecular
to support the recognition of at least two subspecies, one in the
results are consistent with morphometric data (which showed a
north and another in the south (U. j. siamensis and U. j. peninsulae,
smaller size for the small Indian mongoose; Taylor and Matheson,
by anteriority). Furthermore, the subspecies status of U. javanica
1999), and with our coat colour observations (that showed that the
populations from Peninsular Malaysia and Sumatra remains to be
Javan mongoose is reddish brown and the small Indian mongoose
investigated using molecular data. On Sumatra, very few records
is much paler and greyish; pers. obs.; 341 specimens), confirming
(museum specimens) of U. javanica exist on the northern tip of the
the observations of Pocock (1941) and Corbet and Hill (1991). How-
island (Jennings and Veron, 2011), and its status on Sumatra needs
ever, the phylogenetic relationships between these two species and
further investigation.
U. edwardsii remain difficult to resolve, with low node supports
One striking result from our study was the strong genetic diver-
obtained whatever markers and phylogenetic methods were used.
gence of U. javanica specimens from Java. Despite Java having been
Further investigations need to be done with additional markers to
(at least partly) connected to the rest of the Sunda shelf during
clarify the relationships between these three species.
the low sea levels of the Pleistocene, a high level of endemism
Our study found that the mongoose population from southern
has been found on this island (Esselstyn et al., 2013), which sug-
China belongs to U. javanica, and not U. auropunctata, contrary to
gests that some isolation mechanism might have occurred to limit
what was previously thought. On Hong Kong Island, the mongoose
exchanges with nearby islands. Our findings suggest that Javan pop-
species is also U. javanica. Even though individuals from southern
ulations should be considered a separate subspecies, U. j. javanica
China and Hong Kong have different Cytb haplotypes, we were
(É. Geoffroy Saint-Hilaire, 1818), whose type locality is Java.
unable to confirm with our small Chinese sample set whether U.
Within U. auropunctata, we found that Myanmar individuals
javanica was introduced to Hong Kong or it dispersed naturally from
were a sister group to all other individuals, and their quite strong
mainland China.
divergence (up to 3% of Cytb divergence) is likely due to geo-
Our results have clarified the species distribution limits of
graphical barriers (such as major rivers). Similar results have been
U. javanica and U. auropunctata, for which Chinese populations
66 G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70
Fig. 2. ML phylogenetic tree reconstructed from a combined dataset of Cytb + ND2 + FGB (1995 bp). The values are bootstrap proportions (≥ 70%) obtained from ML analysis
(Model: GTR+G+I), and the stars indicate Bayesian posterior probabilities (≥ 0.99). Red: U. javanica, green: U. auropunctata, yellow: U. edwardsii.
G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70 67
Fig. 3. ML phylogenetic tree for Cytb (1140 bp) for Urva javanica. The values are bootstrap proportions obtained from ML analysis (Model: GTR+G+I), and stars indicate
Bayesian posterior probabilities ≥ 0.99.
Fig. 4. Median-joining haplotype network for Urva javanica Cytb haplotypes. The size of each circle is proportional to the haplotype frequency and the length of the link
is proportional to the number of mutations (smallest circle = 1 sample, shortest link = 1 mutation). White: southern China, Hong Kong, northern Vietnam; light grey: north
Thailand; dark grey: central and south Thailand, black: Java.
Table 2
Mean distances computed for FGB, ND2 and Cytb for U. auropunctata, U. edwardsii and U. javanica (highlighted in grey) and the two outgroups, U. brachyura and U. fusca.
found in other groups (e.g. fruit bats, Campbell et al., 2004). Our in Myanmar. Four other subspecies of U. auropunctata have been
findings might support the designation of this group as the sub- recognized (Wozencraft, 2005; Gilchrist et al., 2009), and further
species, U. a. birmanica (Thomas, 1886), whose type locality is Pegu genetic studies are needed to determine their validity. In partic-
68 G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70
Fig. 5. Median-joining haplotype network for Urva auropunctata Cytb haplotypes. The size of each circle is proportional to the haplotype frequency and the length of the
link is proportional to the number of mutations (smallest circle = 1 sample, shortest link = 1 mutation). White: introduced populations; light grey: Myanmar; dark grey:
Bangladesh and India; black: Pakistan.
ular, U. a. palustris (Ghose, 1965) from West Bengal is sometimes Acknowledgements
considered a separate species (Ghose, 1965; Mallick, 2009), and its
status should urgently be checked using molecular data. We thank the following people (and their institutions) for their
The small Indian mongoose has been introduced to many dif- contribution to this study: A. Barun and D. Simberloff (University
ferent parts of the world, and the introduced populations were of Tennessee, USA), Than Aya and Tun Myint (Myanmar), Saw Tun
said to come mainly from India, and also from Bangladesh for the Khaing (WCS Myanmar), A. Khan (Pakistan), M.L. Patou (Biotope,
Japanese islands (Thulin et al., 2006; Barun et al., 2013). We found France), C. G. Thulin (Uppsala University, Sweden), P. Vercam-
that the haplotypes from the Virgin Islands and Fiji were close to men (Sharjah Desert Park, United Arab Emirates), A. Wijesuriya
those from Bangladesh, and that the Croatian haplotype was closer and S.R.B. Dissanayake (Department of Wildlife Conservation, Sri
to Pakistan haplotypes than to those from India. We also found Lanka), R.C. Kendrick, G. Ades and Y. Wong (Kadoorie Farm and
that the Japanese haplotypes were closer to the haplotypes from Botanic Garden, Hong Kong), and S. De A. Goonatilake (IUCN Sri
Pakistan than to those from India or Bangladesh. However, only Lanka). We thank the following curators for access to specimens
one Indian sample was included in our study and its haplotype was and for the permission to sample specimens and/or for the loan
quite close to the ones from Bangladesh, the Virgin Islands, and Fiji. of samples: J. Eger (Royal Ontario Museum, Canada), K. Helgen
As a comparison, within U. edwardsii (Appendix A Fig. A1), con- (Smithsonian, USA), CA. Norris, T. Pacheco, and J. Spence (Amer-
trary to what we found for U. auropunctata, Bangladesh individuals ican Museum of Natural History, USA), F. Mayer (Museum fur
were quite distant from all others. No strong genetic structure was Naturkunde, Germany), M. Goonatilake (Department of National
found for the other regions, except for an individual from Nepal, Museums, Sri Lanka), L. Heaney, J. Phelps and the late W. Stan-
which was quite far apart from the remaining specimens; how- ley (Field Museum of Natural History, Chicago). We also thank
ever, most of the other samples were from the Middle East. Better the following museums and their curators for access to spec-
geographical coverage would be needed to investigate further the imens: Zoological Survey of India, Kolkata; Museum National
genetic structure within this species. d’Histoire Naturelle, Paris; Natural History Museum, London; Natu-
The Javan mongoose and small Indian mongoose are listed as ralis, Leiden; University of Malaya, Kuala Lumpur; Raffles Museum
Least Concern in the IUCN Red List (IUCN, 2016), despite little of Biodiversity Research, Singapore; Bogor Zoology Museum/Lipi,
being known about their populations in the wild. In China, U. Cibinong. We also thank the government of Hong Kong Special
javanica is listed as Vulnerable, and is sometimes found in wildlife Administrative Region for permits.
trade (Lau et al., 2010). It is hunted in some parts of its range Molecular work was undertaken at the ‘Service de Systématique
(IUCN, 2016) and is regularly found in the illegal trade markets Moléculaire’ (UMS CNRS 2700, MNHN), and we thank the staff of the
in Indonesia (Shepherd et al., 2004). Even though the Javan mon- lab for their help, and in particular, C. Bonillo. A part of the sequenc-
goose is found within a wide range of habitats (Jennings and Veron, ing was supported by the network “Bibliothèque du Vivant” funded
2011), the number of records remains low, and its conservation sta- by CNRS, MNHN, INRA and CEA (Genoscope, www.genoscope.fr).
tus urgently needs revaluation. Most of the previously published G.V. received financial support from MNHN, CNRS, and from the
studies on the taxa Herpestes javanicus were, in fact, on U. aurop- “Action Transversale du Museum, Biodiversité actuelle et fossile”
unctata (and most of these were from the introduced parts of its (MNHN, French Ministry of Research) for the molecular work and
range). to visit museums to study and sample specimens.
Appendix A.
G. Veron, A.P. Jennings / Mammalian Biology 87 (2017) 62–70 69
Fig. A1. Median-joining haplotype network for Urva edwardsii Cytb haplotypes. The size of each circle is proportional to the haplotype frequency and the length of the link
is proportional to the number of mutations (smallest circle = 1 sample, shortest link = 1 mutation). Black: Nepal; dark grey: Bangladesh; light grey: Bahrain, UEA, Iran; white:
Sumatra and ND.
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