bs_bs_banner
Zoological Journal of the Linnean Society, 2014, 170, 917–932. With 4 figures
The distribution of the Malay civet Viverra tangalunga
(Carnivora: Viverridae) across Southeast Asia:
natural or human-mediated dispersal?
GERALDINE VERON1*§, MARAIKE WILLSCH2, VICTOR DACOSTA1,
MARIE-LILITH PATOU1†, ADRIAN SEYMOUR3‡, CELINE BONILLO4,
ARNAUD COULOUX5, SIEW TE WONG6, ANDREW P. JENNINGS1, JÖRNS FICKEL2
and ANDREAS WILTING2*§
1
Unité Origine, Structure et Evolution de la Biodiversité, UMR CNRS MNHN 7205, Département
Systématique et Evolution, Muséum National d’Histoire Naturelle, CP 51, 57 rue Cuvier, 75231
Paris Cedex 05, France
2
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany
3
Operation Wallacea, Old Bolingbroke, Lincolnshire PE23 4EX, UK
4
Service de Systématique Moléculaire, UMS 2700, Département Systématique et Evolution, Muséum
National d’Histoire Naturelle, CP 26, 57 rue Cuvier, 75231 Paris Cedex 05, France
5
Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux, CP5706, 91057 Evry Cedex,
France
6
Bornean Sun Bear Conservation Center, PPM 219, Elopura, 90000 Sandakan, Sabah, Malaysia
Received 20 June 2013; revised 24 October 2013; accepted for publication 30 October 2013
The Malay civet Viverra tangalunga Gray, 1832 is a fairly large viverrid that has a wide distribution in both the
Sundaic and Wallacea regions of Southeast Asia. We investigated the genetic diversity of V. tangalunga by
analysing the mitochondrial DNA of 81 individuals throughout its range in order to elucidate the evolutionary
history of this species and to test the hypotheses of natural dispersal and/or potential human introductions to some
islands and regions. Our phylogenetic analyses revealed that V. tangalunga has a low matrilinear genetic diversity
and is poorly structured geographically. Borneo is likely to have served as the ancestral population source from
which animals dispersed during the Pleistocene. Viverra tangalunga could have naturally dispersed to Peninsular
Malaysia, Sumatra, and Belitung, and also to several other Sunda Islands (Bangka, Lingga, and Bintang in the
Rhio Archipelago), and to Palawan, although there is possible evidence that humans introduced V. tangalunga to
the latter islands. Our results strongly suggested that V. tangalunga was transported by humans across Wallace’s
Line to Sulawesi and the Moluccas, but also to the Philippines and the Natuna Islands. Our study has shown that
human-mediated dispersal can be an important factor in understanding the distribution of some species in this
region.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 917–932.
doi: 10.1111/zoj.12110
ADDITIONAL KEYWORDS: biogeography – Carnivora – human introduction – phylogeography – Southeast
Asia – Sunda Shelf.
*Corresponding author. E-mail: [email protected]; [email protected]
†Current address: Biotope, Recherche & Développement, 22 Boulevard Maréchal Foch, 34140 Mèze, France.
‡Current address: University of the West of England, Frenchay Campus, Coldharbour Lane, Bristol, BS16 1QY, UK.
§Contributed equally.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 917–932
917
918
G. VERON ET AL.
INTRODUCTION
Southeast Asia had a complex and dynamic environmental history during the Plio-Pleistocene (from c.
5.3 Mya to 11 700 years ago; Voris, 2000; Hall, 2002).
Within the Sundaic region, climate-induced sea
level changes altered the topography repeatedly,
exposing and flooding land corridors between Peninsular Malaysia, Borneo, Sumatra, Java, and smaller
islands. Faunal distribution patterns across the
Sunda Shelf have typically been ascribed to Pleistocene movements across exposed land connections
(Wallace, 1869; Heaney, 1986; Brandon-Jones, 1996,
2001). However, several recent molecular studies
have challenged the traditional hypothesis that there
were unrestricted movements across the Sunda Shelf
during periods of lower sea levels (Gorog, Sinaga &
Engstrom, 2004; Patou et al., 2010; Wilting et al.,
2011).
An often neglected factor that might have influenced the current distribution of species in Southeast
Asia is the human transportation of animals (De
Vos, Manville & Van Gelder, 1956; Heinsohn,
2001, 2002, 2003; Matisoo-Smith & Robins, 2004;
Larson et al., 2007; Corlett, 2010). In particular, the
presence of some Sundaic species within the Wallacea
region, such as the common palm civet Paradoxurus
hermaphroditus (Pallas, 1777) and the Malay civet
Viverra tangalunga Gray, 1832, has been attributed to
human introductions across Wallace’s Line, a deepsea channel separating these two regions (Voris, 2000;
Heinsohn, 2001; van den Bergh et al., 2009). Although
civets are eaten all over Southeast Asia (G.V., pers.
observ.; Corlett, 2007; Shepherd & Shepherd, 2010),
there is currently no historical evidence that civets
were transported as a food item to the Wallacea
region. Civets are also kept as pets (Shepherd, 2008)
and used as rat-catchers (although their diet mainly
comprises fruit and invertebrates; Jennings & Veron,
2009), which are both plausible reasons why humans
might have translocated civets; however, hypotheses
of natural or human-mediated dispersals across
Southeast Asia have rarely been challenged for
mammals within this region, and have never been
tested for V. tangalunga.
Viverra tangalunga is a fairly large (3–7 kg) terrestrial species that occurs mainly in primary and secondary lowland forests (Jennings & Veron, 2009,
2011). It is the sister species to the other Viverra
civets (occurring on mainland Southeast Asia)
from which it diverged c. 4.6 Mya (Gaubert &
Cordeiro-Estrela, 2006). This species is found on Peninsular Malaysia (including Langkawi Island), Singapore, Sumatra, Borneo, the Philippines, Sulawesi, the
Moluccas, and several small Indonesian islands
(Jennings & Veron, 2011). The wide distribution of
V. tangalunga, both within the Sundaic and Wallacea
regions, makes this species a good model to investigate to what extent natural dispersal during the last
glacial period (c. 110 000–10 000 years ago) and/or
human-mediated translocation shaped the current
distribution of a species within Southeast Asia.
It is generally considered that V. tangalunga dispersed naturally across the emerged Sunda Shelf
during the Pleistocene, but was introduced by
humans to areas east of Wallace’s Line (Sulawesi
and the Moluccas; Weber, 1899; De Vos et al., 1956;
Groves, 1976, 1984; Feiler, 1990; Boitani, 2001;
Heinsohn, 2001; van den Bergh et al., 2009). There is
no historical documentation of introductions of
V. tangalunga, although museum specimens have
been collected within the Wallacea region since the
middle of the 19th century. Some civet species
are farmed for ‘civet oil’ from their perineal glands,
which is used in traditional medicine and in the
perfume industry (Jennings & Veron, 2009). This has
been suggested as a reason for the translocation
of V. tangalunga to the Wallacea region (Groves, 1984;
Heinsohn, 2001; Helgen, 2002), but evidence is
lacking that V. tangalunga has ever been farmed for
this purpose. The hypothesis of human-mediated dispersal of V. tangalunga is supported by the absence of
fossils in the Moluccas (Flannery et al., 1995) and
Sulawesi (Hooijer, 1950), whereas remains from the
Niah Caves on Borneo proved its Pleistocenic and
Holocenic presence on this island (Cranbrook & Piper,
2007; Cranbrook, 2010). For the Philippines, human
introduction has been proposed for P. hermaphroditus
(Patou et al., 2010; Piper et al., 2011), but so far not
for V. tangalunga, even though no Pleistocene or
Holocene remains of this latter species have been
found in this region (Piper et al., 2011).
The aim of our study was to investigate the
genetic diversity and the evolutionary history of
V. tangalunga in order to test the traditional hypothesis that its occurrence across the Sunda Shelf
stemmed from Pleistocene natural dispersal, whereas
the presence of this species beyond Wallace’s Line
resulted from human-mediated introductions.
MATERIAL AND METHODS
MOLECULAR SAMPLING, DNA EXTRACTION,
AND SEQUENCING
We collected 86 samples (33 hairs or tissues; 53 from
museum specimens) of V. tangalunga. Sample selection was aimed at covering all major regions and
islands across the distribution of the species
(Appendix S1; Fig. 1; Table 1). DNA of fresh samples
was extracted following a cetyl-trimethyl-ammonium
bromide (CTAB)-based protocol (Winnepenninckx,
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
EVOLUTIONARY HISTORY OF THE MALAY CIVET
919
Figure 1. The location of Viverra tangalunga samples used in this study. The grey shading indicates the currently known
distribution of V. tangalunga (see Jennings & Veron, 2011). The size of each dot represents the number of samples per
locality.
Backeljau & De Wachter, 1993) at the Muséum
national d’Histoire naturelle (Paris, France). DNA
extractions from museum samples were conducted at
the Leibniz Institute for Zoo and Wildlife Research
(Berlin, Germany) following a modified protocol of
Wisely, Maldonado & Fleischer (2004), as described in
Wilting et al. (2011).
We sequenced two mitochondrial loci: 228 bp (in the
5′ region) of cytochrome b (cyt b) using previously
described primers (Gaubert et al., 2004; Veron et al.,
2004) and 569 bp of the control region (CR), using
primers CR1F (5′-CCACTATCAGCACCCAAAGC-3′)
and CR2R (5′-CCCGGAGCGAGAAGAGG-3′) from
Palomares et al. (2002). To accommodate the fragmented DNA in museum samples, we designed
additional nested primers for cyt b and CR: Cytb2F
(5′-TCATCAGTTACCCACATTTGC-3′) and Cytb2R
(5′-GGACATTTGGCCTCATGGTA-3′); CR0F (5′-TTC
CCTGCAATACCAAAAACT-3′) and CR0R (5′-ATGGG
GACAAGCGGTTAAT-3′); CR3F (5′-TTAATCGCTAGT
CCCCATGAAT-3′) and CR2R; CR4F (5′-CCTCTTCTC
GCTCCGGG-3′) and CR3R (5′-TACCAAATGCATGA
CATCACAG-3′). Polymerase chain reactions (PCRs)
were performed in 20-μL reaction volumes with the
following constituents: 50–100 ng of genomic DNA,
2 μL of 10× Taq polymerase buffer, 2.5 mM of MgCl2,
0.2 mM of dNTP mix, 0.32 μM of each primer, and
0.5–1 unit of TaqPolymerase (QBiogene, Illkirch,
France) or GoTaq polymerase (Promega GmbH, Mannheim Germany). PCR cycles for DNA amplification
were: 94 °C for 4 min, followed by 35–45 cycles of 94 °C
for 30 s (denaturation), 50 °C (cyt b) or 61 °C (CR) for
30–45 s (annealing), and 72 °C for 40 s (extension),
with a final extension step at 72 °C for 7 min. Fragments that had amplified successfully were purified by
ExoSap (GENOSCOPE, Evry, France) or ExoFastAP
(Fermentas GmbH, St. Leon-Rot, Germany) and then
sequenced bidirectionally using BigDye® Terminator
v.3.1 on an automated DNA sequencer A3100xl
(Applied Biosystems). PCR fragments obtained from
the DNA extracted from museum samples were amplified and sequenced twice to ensure the quality and
authenticity of sequences. Sequences obtained independently in the two laboratories were congruent.
PHYLOGENETIC
AND HAPLOTYPIC NETWORK ANALYSES
Sequences were assembled, aligned, and edited using
CLUSTAL X2 (Larkin et al., 2007). Sequences
from both loci were analysed separately and then
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
FMNH 145742
FMNH 146957
FMNH LRH4121
C201
C202
C203
TC430
TC431
TC432
TC433
TC434
TC435
TC442
TC448
TC449
TC450
TC452
TC454
TC474
TC494
TC522
TC523
TC524
TC525
TC529
TC533
TC534
TC556
TC571
TC575
TC576
TC577
TC578
TC593
TC594
TC682
IZW1
IZW7
IZW10
IZW11
IZW12
IZW13
IZW21
IZW22
IZW25
IZW26
IZW27
IZW28
ZS 1908/2748
RMNH 12441
RMNH 34838
RMNH 33980
RMNH 34826
RMNH 2412
RMNH 20729
RMNH 20730
RMNH 34831
RMNH 34832
RMNH 34833
RMNH 34827
Specimen
Sample
Sibuyan Island, Romblon Province
Sibuyan Island, Romblon Province
Mount Isarog, Luzon Island
Lubuk Baung, Krau WR, Pahang
Lubuk Baung, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Buton Island, Sulawesi
Buton Island, Sulawesi
Buton Island, Sulawesi
Buton Island, Sulawesi
Buton Island, Sulawesi
Jenderak, Krau WR, Pahang
Jenderak, Krau WR, Pahang
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Jenderak, Krau WR, Pahang
Sabah, Borneo
Danum Valley, Sabah, Borneo
Danum Valley, Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Sabah, Borneo
Mengans Camp, Danum Valley, Sabah, Borneo
Unknown (likely Palawan)
Buru Island, Moluccas
Sibau River, Poelau, Kalimantan, Borneo
Pleihari, Kalimantan, Borneo
Banka Island
Banka Island
Sulawesi
Hitoe, Ambon Island, Moluccas
Ambon Island, Moluccas
Ambon Island, Moluccas
Ambon Island, Moluccas
Ambon Island, Moluccas
Halmaheira Island, Moluccas
Geographic origin
Philippines
Philippines
Philippines
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Unkown
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Country
Field Museum of Natural History, Chicago
Field Museum of Natural History, Chicago
Field Museum of Natural History, Chicago
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Field
Zoologische Staatssammlung, München
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Naturalis, Leiden
Source
1992
1992
1988–1994
2004
2004
2004
2004
2004
2004
2004
2003
2003
2003
2003
2003
2005
2005
2005
2005
2005
2005
2005
2005
2005
2006
2006
2006
2006
2006
2006
2006
2006
2011
1908
1894
1866
1935
1872
1935
1923
1922
1863
1863
1867
1863
Year of
collection
Table 1. List of the samples included in this study. For each sample, we report the sample identification number, the museum specimen identification number,
the locality, country, source of the sample, and the year of collection
920
G. VERON ET AL.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
AMNH 207581
AMNH 207582
AMNH 152881
AMNH 152882
AMNH 152883
AMNH 29734
AMNH 29735
AMNH 152878
AMNH 152879
AMNH 152880
AMNH 101395
AMNH 226805
19293
19294
19299
19302
19337
P158
SM 89
SM1297 (M 1216)
SM 1298 (M 762)
ZRC 4.1446
ZRC 4.1448
1025604
BZM 1089
BZM 70042
BZM 83476
BZM 83473
BZM 83460
IZW42
IZW43
IZW44
IZW45
IZW46
IZW49
IZW50
IZW51
IZW52
IZW53
IZW54
IZW55
IZW56
IZW57
IZW58
IZW59
IZW60
IZW61
IZW62
IZW63
IZW64
IZW66
IZW68
IZW71
IZW72
IZW74
IZW75
IZW78
IZW80
Halmaheira Island, Moluccas
Halmaheira Island, Moluccas
Tanjung Batu, Belitung Island
Bukit Menguru, Belitung Island
Lingga Island, Lingga Archipelago
Bintang Island, Rhio Archipelago (= Riau Archipelago)
Bintang Island, Rhio Archipelago (= Riau Archipelago)
Bintang Island, Rhio Archipelago (= Riau Archipelago)
Bunguran Island, Natuna Islands
Bunguran Island, Natuna Islands
Bunguran Island, Natuna Islands
San Mariano, Sitio, Sierra Madre Mountains, Isabela
Province, Luzon Island
Curry, Pili, Mount Isaroq, Camarines Sur, Luzon Island
Curry, Pili, Mount Isaroq, Camarines Sur, Luzon Island
Bumbulan, Sulawesi
Bumbulan, Sulawesi
Bumbulan, Sulawesi
Iwahig, San Antonio Bay, Palawan
Iwahig, San Antonio Bay, Palawan
Bumbulan, Sulawesi
Bumbulan, Sulawesi
Bumbulan, Sulawesi
Lampobattang, Lombasang, Sulawesi
Gunung Nokilalaki, Sulawesi
Danum, Sabah, Borneo
km 40 logging road Danum, Sabah, Borneo
km 61, Danum road, Sabah, Borneo
camp 85, Danum, Sabah, Borneo
Danum Road, Sabah, Borneo
Substation Marotai, Tawau Hills Park, Borneo
Tawai Plateau, Telupid, Tall forest, Sabah, Borneo
Kg. Pandasan, Kota Belud, Sabah, Borneo
Mawao, Membakut, Way to Beaufort, Sabah, Borneo
Larut, Perak
Sumatra
Sulawesi
Sumatra
Mindoro Island
Luzon Island
Sintang or Lintang, Kalimantan, Borneo
La Datu, Sabah, Borneo
Philippines
Philippines
Indonesia
Indonesia
Indonesia
Philippines
Philippines
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Malaysia
Indonesia
Indonesia
Indonesia
Philippines
Philippines
Indonesia
Malaysia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Indonesia
Philippines
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
American Museum of Natural History, New York
Sabah Parks
Sabah Parks
Sabah Parks
Sabah Parks
Sabah Parks
Sabah Parks
Museum Sabah, Kota Kinabalu
Museum Sabah, Kota Kinabalu
Museum Sabah, Kota Kinabalu
Raffles Museum of Biodiversity Research, Singapore
Raffles Museum of Biodiversity Research, Singapore
Naturhistorisches Museum Bern
Museum fur Naturkunde, Berlin
Museum fur Naturkunde, Berlin
Museum fur Naturkunde, Berlin
Museum fur Naturkunde, Berlin
Museum fur Naturkunde, Berlin
Naturalis, Leiden
Naturalis, Leiden
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
National Museum of Natural History, Washington
American Museum of Natural History, New York
1961
1961
1939
1939
1939
1901
1901
1939
1939
1939
1931
1975
1999
1999
2000
2000
2001
2000
1990
1971
1971
ND
1931
1892
1905
ND
ND
ND
1907
1863
1863
1904
1904
1901
1902
1902
1902
1900
1900
1900
1961
Samples from museum specimens (IZWxx) were processed at the Leibniz Institute for Zoo and Wildlife Research, Berlin. Tissue and hair samples (Cxx and TCxx) were processed at
the Muséum national d’Histoire naturelle, Paris.
RMNH 34828
RMNH 34829
USNM 124945
USNM 125024
USNM 113067
USNM 115597
USNM 115598
USNM 115599
USNM 104866
USNM 104867
USNM 104869
AMNH 187198
IZW29
IZW30
IZW31
IZW32
IZW33
IZW34
IZW35
IZW36
IZW37
IZW38
IZW39
IZW40
EVOLUTIONARY HISTORY OF THE MALAY CIVET
921
922
G. VERON ET AL.
concatenated, as each separate analysis showed
similar topologies. To select the nucleotide substitution
model that best fitted the data, we used the hierarchical likelihood ratio test approach implemented in
JMODELTEST 0.1.1 (Posada, 2008). The selected
model was the Tamura-Nei model (TN93; Tamura &
Nei, 1993), with an allowance for both invariant sites
(+ I) and a gamma (+ G) distribution shape parameter α for among-site rate variation. Parameter values
for the model selected were: –ln L = 1501.61, I = 0.846,
and α = 0.674. Phylogenetic reconstructions based
on these parameters were subsequently performed,
applying the maximum-likelihood (ML) approach and
the neighbour-joining (NJ) method, both implemented
in MEGA 5.05 (Tamura et al., 2011), as well as the
Bayesian inference (BI), implemented in MrBayes
3.2.1 (Huelsenbeck & Ronquist, 2001; for settings,
see Wilting et al., 2011). As we had neither a proper
out-group criterion nor a molecular clock (Felsenstein,
2004), we constructed unrooted phylogenetic trees.
Tree- and star-like phylogenetic proportions were estimated using likelihood mapping analysis (Strimmer &
von Haeseler, 1997), implemented in TREE-PUZZLE
5.2 (Schmidt et al., 2002). Support for proportions was
assessed by a reliability percentage after 10 000
quartet puzzling steps. Stable (and potentially old)
populations had tree-like phylogeny proportions of
well above 50% (Strimmer & von Haeseler, 1997). In
addition, to display all possible maximum parsimonious relationships among haplotypes, a haplotype
median-joining (MJ) network was constructed using
NETWORK 4.6.1 (Bandelt, Forster & Röhl, 1999).
We computed the genetic diversity for five different island populations (Peninsular Malaysia,
Borneo, Philippines, Sulawesi, and Moluccas) using
ARLEQUIN 3.5 (Excoffier, Laval & Schneider, 2005).
Samples from small islands and from Sumatra were
grouped, as sample sizes from these localities were
small. Belitung samples were excluded, owing to their
very distinct haplotypes. Because we used a concatenated data set with potentially differing selective
pressures acting on the two mitochondrial loci (Lopez
et al., 1997), we applied Tajima’s D-test (Tajima,
1989) implemented in ARLEQUIN to investigate
whether the concatenated data set could be treated as
a selectively neutrally evolving unit or not. The demographic histories of the different island populations
were inferred by mismatch distribution (Li, 1977;
Rogers & Harpending, 1992) and from the Fu’s FS
statistics (Fu, 1997), all implemented in ARLEQUIN.
We used tau (τ), representing units of mutational
time, together with a mutation rate μ = 2.2 × 10–9 per
site and year (Kumar & Subramanian, 2002) in the
equation μ = τ/2t × number of sites (= fragment length
in bp) in order to estimate the age of V. tangalunga
matrilines.
RESULTS
Sequences of CR + cyt b were obtained for 81 individuals; only CR sequences could be obtained for the
remaining five samples (results in Appendix S2). The
CR + cyt b Tajima’s D-test indicated that the concatenated data set used in our study could be treated
as a neutrally evolving unit. The 81 samples analysed
for both loci shared 39 mtDNA haplotypes (HTs;
Appendix S3, with GenBank accession numbers
KF177803–KF177880). The mtDNA nucleotide diversity (π) among all V. tangalunga was very low
(π = 0.006361; Table 2). The highest number of HTs
(16) was found on Borneo, and only two of these were
shared with individuals on other islands. Borneo also
had the highest nucleotide diversity of all island
populations (π = 0.005621; Table 2).
The phylogenetic analysis of mtDNA HTs, using
NJ, ML, and BI approaches, generated weakly
resolved phylogenetic trees (Fig. 2). Likelihood
mapping (Schmidt et al., 2002) estimated an overall
star-like phylogenetic proportion of 45.2%, resulting
in a tree-like phylogeny proportion of 54.8%, indicating that V. tangalunga matrilines had not yet reached
phylogenetic stability (Strimmer & von Haeseler,
1997; Fickel et al., 2008). None of the major island
populations formed a monophyletic HT group, and
only the Belitung samples were clearly distinct
from all other V. tangalunga samples. Haplotypes
from the Moluccas, as well as those from the Philippines, formed two distinct groups each. Generally, the
genetic diversity of the samples was poorly structured
geographically, and Bornean individuals were represented in all major clades.
The centre of the main star-like network (Fig. 3)
consisted of seven HTs, which represented samples
from Borneo, Sulawesi, and the Natuna Islands.
From this centre, branches radiated to HTs from
other regions and islands (including the Moluccas,
Sulawesi, the Philippines, other Borneo populations, and Peninsular Malaysia/Sumatra). The
haplotype network supported the distinct position of
V. tangalunga from Belitung. The Belitung HT27,
shared by the two individuals representing this
population, was separated by at least nine mutations
from all other HTs. The HTs from Peninsular Malaysia were at least two, and up to five, mutational
steps away from their closest relatives, HT28
(Borneo and the Rhio Archipelago), whereas the HT
from Bangka and Lingga Islands was only one mutation step away from HT28. One of the two Sumatran
samples was one mutation step from the Peninsular
Malaysia HT group (and six steps away from
Bornean and Riau Islands HTs), whereas the second
Sumatran sample was one mutation step from two
Bornean HTs.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
Number of individuals N
Fragment length/number of usable
sites (nc)
Diversity indices
Number of haplotypes h
Number of segregating sites S
Transition/transversion ratio
Nucleotide diversity p (SD)
Haplotype diversity Hd (SD)
Ratio R = h/N
Tajima’s test of selective neutrality
Tajima’s D
P(Dsimulated < Dobserved)
(1000 simulations)
Mismatch distribution
Average number of nucleotide
differences k
Variance of k
τ
Test of goodness-of-fit
Sum of squared deviation (SSD)
P(SSDsimulated ≥ SSDobserved)
Harpending’s raggedness index
P(Ragsimulated ≥ Ragobserved)
Age of clade
Based on τ (kyr)
95% CI (kyr)
Sudden population expansion
FS
P(FS)
Parameter
25
797
16
25
24/1
0.005621 (0.003192)
0.9567 (0.0231)
0.64
−1.1926
0.113
17 624
8083
2113
0.00141
0.92
0.00968
0.95
N/A
N/A
−6.555
0.003
39
41
37/4
0.006361 (0.003457)
0.9571 (0.0129)
0.481
−1.2375
0.092
5070
8315
6262
0.00464
0.59
0.01354
0.66
1786
891–2462
−24.665
< 0.0001
Borneo
81
797
All
Table 2. Genetic diversity estimates within Viverra tangalunga
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
0.84067
0.689
N/A
N/A
0.0774
0.26
0.158
0.29
7643
6299
3364
0.3978
0.693
5
9
8/1
0.004231 (0.002648)
0.7818 (0.0926)
0.455
11
797
Philippines
−1.2724
0.182
N/A
N/A
0.03425
0.32
0.1269
0.33
3165
2906
2489
−0.5172
0.322
6
8
7/1
0.003123 (0.002078)
0.8444 (0.1029)
0.6
10
797
Peninsular
Malaysia
−3.0597
0.001
N/A
N/A
0.00122
0.75
0.12
0.84
0.681
1465
0.615
−1.77497
0.02
5
4
3/1
0.000772 (0.000731)
0.5385 (0.1611)
0.3846
13
797
Sulawesi
2.1475
0.843
N/A
N/A
0.1172
0.07
0.16898
0.35
11 378
8510
4222
1.9718
0.986
4
8
7/1
0.005298 (0.00329)
0.8056 (0.0889)
0.444
9
797
Moluccas
1.366
0.772
N/A
N/A
0.077
0.11
0.1365
0.19
7891
6488
4127
−0.3068
0.435
5
13
13/0
0.005179 (0.003148)
0.8364 (0.0702)
0.455
11
797
Natuna, Lingga,
Rhio, Bangka,
Sumatra
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
1
N/A
N/A
N/A
N/A
0.5
2
797
Belitung
EVOLUTIONARY HISTORY OF THE MALAY CIVET
923
924
G. VERON ET AL.
Figure 2. Phylogenetic relationships among Viverra tangalunga inferred from mtDNA haplotypes from the concatenated
797-bp mitochondrial control region and cytochrome b sequences. Trees for each of the three analyses (neighbour joining,
maximum likelihood, and Bayesian inference) had similar topologies. Numbers above the branches represent bootstrap
support, with only values > 60% shown. Numbers in parentheses represent the number of individuals sharing the same
haplotype; haplotype codes are listed in Appendix S3.
The mismatch distribution analysis for V. tangalunga showed a unimodal distribution, indicating
sudden population expansion (Fig. 4), which was supported by a strongly negative significant FS statistic
(Table 2). The mismatch distributions for the different
island populations largely confirmed the phylogenetic analyses. A unimodal pattern with a wide base
was found for Borneo, and the populations from the
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
EVOLUTIONARY HISTORY OF THE MALAY CIVET
925
Figure 3. Haplotype network obtained from the analysis of the concatenated mitochondrial control region and
cytochrome b sequences. Connecting lines represent single mutations, unless indicated otherwise under the lines. The size
of the circles is proportional to the haplotype frequency, and the numbers indicate the haplotype names.
Philippines, the Moluccas, and Peninsular Malaysia
showed a bimodal to multimodal distribution, indicating a bi- to meta-population sample. Viverra
tangalunga from Sulawesi had a unimodal mismatch
distribution with a very small base, indicating a
sudden population expansion. Based on the mismatch
distribution, and using the equation t = τ/2μ, the
approximate age of V. tangalunga was 1.79 Myr (95%
CI: 0.89–2.46 Myr; Table 2).
DISCUSSION
The cyt b and CR diversity among V. tangalunga was
very low compared with other Asian viverrids, such
as the binturong Arctictis binturong (Raffles, 1821)
(Cosson et al., 2007) or P. hermaphroditus (Patou
et al., 2010). In contrast to other carnivores (Cosson
et al., 2007; Tchaicka et al., 2007; Patou et al., 2010;
Wilting et al., 2011), our data showed that
V. tangalunga lacks a pronounced geographic structure, and that some island populations did not form
monophyletic groups.
BORNEO,
THE ANCESTRAL POPULATION CENTRE OF
VIVERRA
TANGALUNGA
The highest genetic diversity of V. tangalunga was
found within the Bornean population. Bornean individuals were present in all major clades, and they
shared haplotypes with most of the individuals from
other parts of the species’ range. In addition, the wide
base of the Borneo haplotypic mismatch distribution
supported an ancient status of the Bornean population. These findings are congruent with the presence
of Pleistocene V. tangalunga fossils from the Niah
Caves on Borneo (Cranbrook & Piper, 2007;
Cranbrook, 2010) and the lack of V. tangalunga fossils
elsewhere (Hooijer, 1962; de Vos, 1983; Tougard,
2001; Louys, 2007), while fossil remains of other
viverrids have been found throughout Southeast Asia
(Hooijer, 1962; Flannery et al., 1995; Tougard, 2001;
Louys, 2007; van den Bergh et al., 2009; A.M. Moigne
pers. comm.). Thus, both genetic and fossil evidence
point towards Borneo as the ancestral origin of the
current populations of V. tangalunga. This indicates
that during the Plio- and Pleistocene there was either
a spatial restriction of V. tangalunga to Borneo, followed by a recent expansion to other parts of its range
(congruent with the low intraspecific genetic variation
within V. tangalunga), or that populations on other
islands became extinct.
The spatial restriction of V. tangalunga within the
Sundaic region, during periods of lower sea levels,
could have been ecologically driven, as this species
depends on forested habitats (Jennings & Veron,
2011). During drier and cooler periods of the Pleistocene, humid tropical forest areas receded on the
Sunda Shelf (Heaney, 1991; Wurster et al., 2010, but
see Cannon, Morley & Bush, 2009), thereby restricting rainforest-dwelling species to forest refugia, and
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
926
G. VERON ET AL.
Figure 4. Mismatch distribution computed for the concatenated mitochondrial sequences for all samples, and for the
different populations (Peninsular Malaysia, Borneo, Philippines, Sulawesi, and Moluccas); solid line, observed distribution
of pairwise differences; dashed line, expected distribution under the model of sudden demographic expansion.
hindering their dispersal across exposed land bridges
lacking rainforest. Climate and vegetation simulations (Cannon et al., 2009), as well as analyses of the
carbon isotope composition of ancient cave guano profiles (Wurster et al., 2010), have suggested that
during glacial periods, forests remained present in
western Sumatra, central Borneo, and other parts of
the emergent Sunda Shelf, and that some of these
forested areas could have functioned as refugia for
forest-dependent species (Lohman et al., 2011). Forest
contractions during glaciations are likely to have had
a more negative impact on V. tangalunga populations
within the forest refugia on Sumatra and Peninsular
Malaysia (than on Borneo), because of their smaller
size during glacial periods (Slik et al., 2011). The size
of forest fragments has been shown to impact the
survival rates of species (Opdam, 1991). In addition,
as rainforest refugia have largely been restricted to
mountains (Lohman et al., 2011), the distribution
range of lowland species, such as V. tangalunga, may
have been more constricted during the last glacial
maximum (LGM).
Another explanation for a possible range restriction
of V. tangalunga to Borneo during the last glacial
period could have been the impact of the Toba supereruption in northern Sumatra in the Late Pleistocene,
c. 73 500 years ago (Ambrose, 1998; Williams et al.,
2009; Wilting et al., 2012), although the severity
of its impact is debated (Louys, 2007). On Sumatra
and Peninsular Malaysia, this eruption might
have resulted in local population extinctions of
V. tangalunga. The lack of ash layers on Borneo suggests that this island was less affected by the consequences of this super-eruption (Oppenheimer, 2002).
DISPERSAL
WITHIN THE
SUNDAIC
REGION
The large genetic distance of Belitung V. tangalunga
to all others suggests that V. tangalunga dispersed
naturally from Borneo to Belitung during Pleistocene
glacial periods, which was possible when the sea
level was at least 40 m lower than at present and
land bridges connected the islands (Voris, 2000).
Despite a postulated savannah corridor through
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
EVOLUTIONARY HISTORY OF THE MALAY CIVET
central Sundaland (Bird, Taylor & Hunt, 2005) that
might have restricted the west–east dispersal of
forest species, gallery forests along the main rivers
that traversed the Sunda Shelf (Voris, 2000) could
have served as travel corridors for forest species
and facilitated the dispersal of V. tangalunga from
Borneo to Belitung. Rising sea levels in the Late
Pleistocene (∼10 000 years ago) may have isolated a
small V. tangalunga population on Belitung (only one
haplotype was found), which since then has diverged
from their Bornean source. In fact, the distinctiveness
of the Belitung V. tangalunga population indicates
that it should be recognized as an evolutionarily significant unit (ESU; Moritz, 1994), and thus it should
be managed separately from all other populations.
Individuals from Peninsular Malaysia were also
distinct from all other populations, albeit not as pronounced as the Belitung population. Despite a sandy
seabed soil barrier, a possible savannah corridor
through central Sundaland, and large rivers crisscrossing this region (which have all been proposed
as limiting the dispersal of forest species between
Borneo and Peninsular Malaysia; Heaney, 1991;
Voris, 2000; Gathorne-Hardy et al., 2002; Meijaard,
2004; Bird et al., 2005; Wurster et al., 2010; Slik et al.,
2011), V. tangalunga could have dispersed naturally
from Borneo to Peninsular Malaysia in a similar way
that it might have reached Belitung (i.e. along gallery
forests). However, one specimen from the Raffles
Museum of Natural History (ZRC 4.1446), labelled
‘Larut, Perak, Peninsular Malaysia’ (HT35), did
not cluster with other Peninsular Malaysia individuals and was only one mutation step from a Bornean
haplotype. This might suggest that V. tangalunga
were also recently introduced by humans to Peninsular Malaysia from Borneo; however, the actual origin
of this specimen could be in doubt (it was deposited
initially in Perak Museum, in Larut district, and this
might have been wrongly indicated as the collection
locality).
Viverra tangalunga from Bintang (Rhio Archipelago), Lingga, and Bangka Islands shared a
common ancestor with civets from Peninsular Malaysia. Despite the early Holocene land connection
between these islands and Peninsular Malaysia and
Sumatra (Meijaard, 2003; Sathiamurthy & Voris,
2006; Corlett, 2009), our results suggest that these
small islands were colonized from Borneo, possibly
along the major rivers that crossed the Sundaland
during the LGM (Meijaard, 2003). However, Viverra
tangalunga from Bintang Island shared a haplotype
with one Bornean individual (BZM 83473), which
could also indicate a human introduction. The locality
of BZM 83473 was recorded as ‘Lintang’ or ‘Sintang’
(supposedly from Borneo), but perhaps it was in
fact from ‘Bintang’, which could explain why it had
927
a similar haplotype to the three individuals from
Bintang Island.
The two Sumatran individuals were very distinct
from each other (18 mutations apart). The first individual clustered together with the Peninsular Malaysian HTs. Faunal affinities and genetic similarities
between populations in Peninsular Malaysia and
Sumatra have been documented for several groups of
vertebrates (Gorog et al., 2004; Ziegler et al., 2007;
Patou et al., 2009; Lohman et al., 2010), possibly as a
result of the low depth of the sea channel between
Peninsular Malaysia and Sumatra, which were connected at sea levels of only 20–30 m below the present
level (Voris, 2000). The other Sumatran individual
grouped together with V. tangalunga from Borneo
(with only one mutation step from a Bornean HT),
which could indicate a human introduction; however,
this specimen (ZRC 4.1448) has no precise collection
locality (it is only labelled ‘Sumatra’), and is indicated
as having been purchased, so its exact origin is
uncertain.
Viverra tangalunga populations on Bunguran
Island, part of the Natuna Islands, shared their HT
with Bornean individuals (and most of the Sulawesi
samples). This island was one of the first to be separated from the mainland and Borneo when sea levels
started to rise c. 13 500 years ago (Meijaard, 2003;
Sathiamurthy & Voris, 2006). Thus, this result suggests a recent human introduction from Borneo.
Viverra tangalunga from the Philippines formed
two separate haplogroups. One was separated by at
least three mutation steps from Bornean HTs,
whereas the second was separated by only one mutation step from a Bornean HT. This indicates that at
least two colonization events occurred in the Philippines. Although a narrow sea channel between
Borneo and Palawan is likely to have existed even
during glacial periods, the fauna on Palawan has
affinities with Borneo (Esselstyn et al., 2010; Piper
et al., 2011), suggesting that V. tangalunga could have
colonized Palawan naturally. Natural dispersal to the
rest of the Philippines is less likely, however, because
of the lack of land connections (Lohman et al., 2011).
Thus, the presence of shared HTs on Palawan,
Sibuyan, and Luzon indicates that some human introductions might have occurred in this region.
CROSSING WALLACE’S LINE
The Sulawesi samples showed no or little divergence
from populations from Borneo (and Natuna Islands),
providing evidence for human introductions to
Sulawesi across Wallace’s Line, as the last possible
connections between Borneo and Sulawesi were
during the Pliocene or even the Miocene (Morales &
Melnick, 1998; Mercer & Roth, 2003; Meijaard, 2004).
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
928
G. VERON ET AL.
This is congruent with previous hypotheses that
V. tangalunga was introduced to Sulawesi in the
Late Holocene or during the protohistoric period
(Heinsohn, 2001; van den Bergh et al., 2009). The
genetic diversity within Sulawesi V. tangalunga was
very low and the extreme narrow base of the mismatch distribution strongly supports a recent population expansion. Although multiple introductions
from Borneo to Sulawesi cannot be excluded, our data
seemed to indicate a single introduction event, with a
subsequent population expansion on Sulawesi.
The nine samples from the Moluccas did not form a
monophyletic group, but instead formed two distinct
groups that were at least six mutations apart. Both
groups were well supported by our analysis, suggesting two independent human introductions. One
haplogroup (all from Ambon) was four steps away from
a Bornean HT; the other haplogroup (Halmahera,
Buru, and Ambon) was one step away from the central
HT (Borneo, Sulawesi, and Natuna). Thus, the latter
group probably originated from Borneo, but this might
have been via Sulawesi. It is conceivable that the
Ambon individual from the second group resulted
from a secondary transfer of V. tangalunga from
Halmahera/Buru. The distinctiveness of the Moluccan
haplogroups suggests that V. tangalunga was introduced several thousand years ago to allow for the
observed degree of diversification. Such early introductions were reported for several species from the Moluccas: Flannery et al. (1995) recovered remains of dogs
and rats from a Late Holocene fossil site in Halmahera
(with dogs dated to 2600–3400 years ago and rats
dated to 1000 years ago), and suggested that pigs
were already present before that time. Similar to
V. tangalunga, the Pacific rat Rattus exulans (Peale,
1848) forms two distinct haplogroups in the Moluccas,
likewise suggesting two human-mediated introductions (Matisoo-Smith & Robins, 2004). Rattus exulans
was probably transported as a food item from the
Philippines to the Wallacea region, and to Near and
Remote Oceania (Matisoo-Smith & Robins, 2004).
Although civets are eaten throughout Southeast Asia,
it has never been suggested that V. tangalunga was
transported as a food item during colonization events
in the Wallacea region. Although the precise reason(s)
for transporting V. tangalunga remains unresolved
(e.g. as a rat-catcher, for civet oil, or for food), its
introduction across Wallace’s Line might have followed
the same routes as other introduced species (see a
review in Heinsohn, 2003).
CONCLUSION
Our study has shown that in addition to possible
natural dispersal scenarios, humans have translocated
V. tangalunga across large parts of Southeast Asia,
and that these translocations may have happened
earlier than was previously thought. This is in line
with the growing body of evidence that humans
have carried species around with them since several
thousand years ago (Heinsohn, 2003). For example,
P. hermaphroditus was brought to Flores by humans
c. 4000 years ago (van den Bergh et al., 2009).
The human transportation of animals was not
restricted to areas east of Wallace’s Line, but has also
occurred within the Sundaic region. This has important implications for understanding the biogeography
within Southeast Asia, as early introductions might
blur the natural occurrence of species. Nevertheless,
it is quite difficult to disentangle natural dispersal
from early anthropogenic introductions, as humans
started to translocate animals across Southeast
Asian islands at the same time as when several small
islands had just become isolated by rising sea levels.
ACKNOWLEDGEMENTS
G.V. thanks: D. Boussarie; C. Colon (Kingsborough
Community College); D. Fernandez (Subic Bay Marine
Exploratorium & Wildlife in Need); S. Goodman,
J. Phelps, and L. Heaney (Field Museum of Natural
History); C. Kern (Berlin Zoo); K. Wells (University of
Ulm); and C. Young (Singapore Zoo). The molecular
work performed by M.L.P., V.D., and G.V. was undertaken at the ‘Service de Systématique Moléculaire’
(UMS CNRS 2700, MNHN), and we thank M.C.
Boisselier, E. Pasquet, and the staff of the SSM.
The sequencing was supported by the ‘Consortium
National de Recherche en Genomique’ (agreement
no. 2005/67, GENOSCOPE-MNHN, ‘Macrophylogeny
of Life’), directed by G. Lecointre. G.V. received
funding from ‘PPF Etat et structure phylogénétique de
la biodiversité actuelle et fossile’ (MNHN/French Ministry of Research), and from UMR 7205 CNRS/MNHN.
G.V. and A.J. thank the EPU, PERHILITAN, and
Z. Akbar (UKM) for supporting our fieldwork in Krau
Wildlife Reserve, Malaysia; funding is acknowledged
at http://www.smallcarnivores.org. A.W. and J.F. thank
F. Mayer (Naturkundemuseum Berlin), K.M. Helgen
(National Museum of Natural History), S. van der Mije
(Naturalis), E. Westwig (American Museum of Natural
History), P. Schmid (Natural History Museum Bern),
R. Kraft (Zoologische Staatssammlung München),
K. Lim (Raffles Museum of Biodiversity Research,
Singapore), M. Lakim (Sabah Parks, Malaysia), and
J. Guntavid (Sabah Museum, Malaysia) for the permission to sample their specimens. The molecular
analysis was funded by the German Research Foundation (DFG grant Fi-698/5-1). S.T.W. thanks Sabah
Wildlife Department, Danum Valley Management
Committee, EPU, and funding agencies (Department
of State USA, Singapore Zoological Gardens, The
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
EVOLUTIONARY HISTORY OF THE MALAY CIVET
Columbus Zoo and Aquarium, Sea World Busch
Gardens, and others acknowledged at http://www
.bsbcc.org.my). We dedicate this paper to our colleague
Annie Tillier.
REFERENCES
Ambrose SH. 1998. Late Pleistocene human population
bottlenecks, volcanic winter, and differentiation of modern
humans. Journal of Human Evolution 34: 623–651.
Bandelt HJ, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular
Biology and Evolution 16: 37–48.
van den Bergh GD, Meijer HJM, Awe RD, Morwood MJ,
Szabo K, Ostende LWV, Sutikna T, Saptomo EW, Piper
PJ, Dobney KM. 2009. The Liang Bua faunal remains: a
95 k.yr. sequence from Flores, East Indonesia. Journal of
Human Evolution 57: 527–537.
Bird MI, Taylor D, Hunt C. 2005. Palaeoenvironments
of insular Southeast Asia during the Last Glacial Period:
a savanna corridor in Sundaland? Quaternary Science
Reviews 24: 2228–2242.
Boitani L. 2001. Carnivore introductions and invasions: their
success and management options. In: Gittleman JL, Funk
SM, Macdonald D, Wayne RK, eds. Carnivore conservation.
Cambridge: Cambridge Univ. Press, Zoological Society of
London, 123–144.
Brandon-Jones D. 1996. The Asian Colobinae (Mammalia,
Cercopithecidae) as indicators of Quaternary climatic
changes. Biological Journal of the Linnean Society 59: 327–
350.
Brandon-Jones D. 2001. Borneo as a biogeographic barrier
to Asian-Australasian migration. In: Metcalfe I, Smith J,
Morwood M, Davidson I, eds. Faunal and floral migrations
and evolution in Se Asia-Australasia. Lisse: A.A. Balkema
Publishers, 365–372.
Cannon CH, Morley RJ, Bush ABG. 2009. The current
refugial rainforests of Sundaland are unrepresentative of
their biogeographic past and highly vulnerable to disturbance. Proceedings of the National Academy of Sciences of the
United States of America 106: 11188–11193.
Corlett RT. 2007. The impact of hunting on the mammalian
fauna of tropical Asian forests. Biotropica 39: 292–
303.
Corlett RT. 2009. The ecology of tropical East Asia. Oxford:
Oxford University Press.
Corlett RT. 2010. Invasive aliens on tropical East Asian
islands. Biodiversity and Conservation 19: 411–423.
Cosson L, Grassman LL Jr, Zubaid A, Vellayan S, Tillier
A, Veron G. 2007. Genetic diversity of captive binturongs
(Arctictis binturong, Viverridae, Carnivora): implications for
conservation. Journal of Zoology 271: 386–395.
Cranbrook E, Piper P. 2007. Sarawak through the ice ages
to present time: environmental change and human impacts
on the past and present distribution of mammals. In:
Stuebing R, Unggang J, Ferner J, Ferner J, Giman B, Ping
KU, eds. Regional conference of biodiversity conservation in
929
tropical planted forest in Southeast Asia. Sarawak: Forest
department Sarawak, 83–106.
Cranbrook EO. 2010. Late quaternary turnover of mammals
in Borneo: the zooarchaeological record. Biodiversity and
Conservation 19: 373–391.
De Vos A, Manville RH, Van Gelder R. 1956. Introduced
mammals and their influence on native biota. Zoologica 41:
163–194.
De Vos J. 1983. The Pongo Faunas from Java and Sumatra
and Their Significance for Biostratigraphical and PaleoEcological Interpretations. Proceedings of the Koninklijke
Nederlandse Akademie Van Wetenschappen Series BPalaeontology Geology Physics Chemistry Anthropology 86:
417–425.
Esselstyn JA, Oliveros CH, Moyle RG, Peterson AT,
McGuire JA, Brown RM. 2010. Integrating phylogenetic
and taxonomic evidence illuminates complex biogeographic
patterns along Huxley’s modification of Wallace’s Line.
Journal of Biogeography 37: 2054–2066.
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.
Feiler A. 1990. [On the mammals of the sangihe and talaud
islands the contribution of a. B. Meyer to its exploration].
Zoologische Abhandlungen 46: 75–94.
Felsenstein J. 2004. Inferring phylogenies. Sunderland, MA:
Sinauer Associates Inc.
Fickel J, Hauffe HC, Pecchioli E, Soriguer R, Vapa L,
Pitra C. 2008. Cladogenesis of the European brown hare
(Lepus europaeus Pallas, 1778). European Journal of Wildlife Research 54: 495–510.
Flannery T, Bellwood P, White P, Moore A, Boeadi,
Nitihaminoto G. 1995. Fossil marsupials (Macropodidae,
Peroryctidae) and other mammals of holocene age from
Halmahera, North Moluccas, Indonesia. Alcheringa 19:
17–25.
Fu YX. 1997. Statistical tests of neutrality of mutations
against population growth, hitchhiking and background
selection. Genetics 147: 915–925.
Gathorne-Hardy FJ, Syaukani, Davies RG, Eggleton P,
Jones DT. 2002. Quaternary rainforest refugia in southeast Asia: using termites (Isoptera) as indicators. Biological
Journal of the Linnean Society 75: 453–466.
Gaubert P, Cordeiro-Estrela P. 2006. Phylogenetics and
tempo of evolution of the Viverrinae (Mammalia, Carnivora,
Viverridae) within feliformians: implications for faunal
exchanges between Asia and Africa. Molecular Phylogenetics
and Evolution 41: 266–278.
Gaubert P, Tranier M, Delmas AS, Colyn M, Veron G.
2004. First molecular evidence for reassessing phylogenetic
affinities between genets (Genetta) and the enigmatic genetlike taxa Osbornictis, Poiana and Prionodon (Carnivora,
Viverridae). Zoologica Scripta 33: 117–129.
Gorog AJ, Sinaga MH, Engstrom MD. 2004. Vicariance
or dispersal? Historical biogeography of three Sunda shelf
murine rodents (Maxomys surifer, Leopoldamys sabanus and
Maxomys whiteheadi). Biological Journal of the Linnean
Society 81: 91–109.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
930
G. VERON ET AL.
Groves CP. 1976. The origin of the mammalian flora of
Sulawesi (Celebes). Zeitschrift fur Saugetierkunde 41: 201–
216.
Groves CP. 1984. Of mice and men and pigs in the IndoAustralian archipelago. Canberra Anthropology 7: 1–18.
Hall R. 2002. Cenozoic geological and plate tectonic evolution
of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences 20: 353–431.
Heaney LR. 1986. Biogeography of mammals in Southeast
Asia: estimates of rates of colonization, extinction, and
speciation. Biological Journal of the Linnean Society 28:
127–165.
Heaney LR. 1991. A synopsis of climatic and vegetational
change in Southeast-Asia. Climatic Change 19: 53–61.
Heinsohn TE. 2001. Human influences on vertebrate zoogeography: animal translocation and biological invasions
across and to the east of Wallace’s Line. In: Metcalfe I,
Smith JMB, Morwood M, Davidson I, eds. Faunal and floral
migrations and evolution in SE Asia-Australasia. Lisse: A.A
Balkema Publishers, 153–170.
Heinsohn TE. 2002. Status of the common spotted cuscus
Spilocuscus maculatus and other wild mammals on Selayar
Island, Indonesia, with notes on Quaternary faunal turnover. Australian Mammalogy 24: 199–207.
Heinsohn TE. 2003. Animal translocation: long-term human
influences on the vertebrate zoogeography of Australasia
(natural dispersal versus ethnophoresy). Australian Zoologist 32: 351–376.
Helgen KM. 2002. Notes on a collection of mammals from
the Moluccas, with new geographic records. Mammalian
Biology 67: 51–54.
Hooijer DA. 1950. Man and other mammals from Toalian
sites in south-western Celebes. Verhandelingen der
Koninklijke Nederlandsche Akademie Van Wetenschappen
Afdeling Natuurkunde 46: 1–158.
Hooijer DA. 1962. Report upon a collection of Pleistocene
Mammals from tin-bearing deposits in a limestone cave
near Ipoh, Kinta valley, Perak. Federation Museums
Journal 7: 1–5.
Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian
inference of phylogenetic trees. Bioinformatics 17: 754–
755.
Jennings AP, Veron G. 2009. Family Viverridae. In: Wilson
D, Mittermeier RA, eds. Handbook of the mammals of the
world, volume 1, Carnivores. Barcelona: Lynx edicions, 174–
223.
Jennings AP, Veron G. 2011. Predicted distributions and
ecological niches of 8 civet and mongoose species in Southeast Asia. Journal of Mammalogy 92: 316–327.
Kumar S, Subramanian S. 2002. Mutation rates in mammalian genomes. Proceedings of the National Academy of
Sciences of the United States of America 99: 803–808.
Larkin MA, Blackshields G, Brown NP, Chenna R,
McGettigan PA, McWilliam H, Valentin F, Wallace IM,
Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins
DG. 2007. Clustal W and Clustal X version 2.0.
Bioinformatics 23: 2947–2948.
Larson G, Cucchi T, Fujita M, Matisoo-Smith E, Robins
J, Anderson A, Rolett B, Spriggs M, Dolman G, Kim
TH, Thuy NTD, Randi E, Doherty M, Due RA, Bollt R,
Djubiantono T, Griffin B, Intoh M, Keane E, Kirch P,
Li KT, Morwood M, Pedrina LM, Piper PJ, Rabett RJ,
Shooter P, Van den Bergh G, West E, Wickler S, Yuan
J, Cooper A, Dobney K. 2007. Phylogeny and ancient
DNA of Sus provides insights into neolithic expansion
in island southeast Asia and Oceania. Proceedings of the
National Academy of Sciences of the United States of
America 104: 4834–4839.
Li WH. 1977. Distribution of nucleotide differences between
two randomly chosen cistrons in a finite population. Genetics 85: 331–337.
Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hal R,
Ng PKL, Shih H-T, Carvalho GR, von Rintelen T.
2011. Biogeography of the Indo-Australian Archipelago.
Annual Review of Ecology, Evolution, and Systematics 42:
205–226.
Lohman DJ, Ingram KK, Prawiradilaga DM, Winker K,
Sheldon FH, Moyle RG, Ng PKL, Ong PS, Wang LK,
Braile TM, Astuti D, Meier R. 2010. Cryptic genetic
diversity in ‘widespread’ Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biological Conservation 143: 1885–1890.
Lopez JV, Culver M, Stephens JC, Johnson WE, O’Brien
SJ. 1997. Rates of nuclear and cytoplasmic mitochondrial
DNA sequence divergence in mammals. Molecular Biology
and Evolution 14: 277–286.
Louys J. 2007. Limited effect of the Quaternary’s largest
super-eruption (Toba) on land mammals from Southeast
Asia. Quaternary Science Reviews 26: 3108–3117.
Matisoo-Smith E, Robins JH. 2004. Origins and dispersals
of Pacific peoples: evidence from mtDNA phylogenies of the
Pacific rat. Proceedings of the National Academy of Sciences
of the United States of America 101: 9167–9172.
Meijaard E. 2003. Mammals of south-east Asian islands and
their Late Pleistocene environments. Journal of Biogeography 30: 1245–1257.
Meijaard E. 2004. Solving mammalian riddles. A reconstruction of the Tertiary and Quaternary distribution of
mammals and their palaeoenvironments in island SouthEast Asia. PhD Thesis, The Australian National University,
Canberra.
Mercer JM, Roth VL. 2003. The effects of Cenozoic global
change on squirrel phylogeny. Science 299: 1568–1572.
Morales JC, Melnick DJ. 1998. Phylogenetic relationships
of the macaques (Cercopithecidae: Macaca), as revealed by
high resolution restriction site mapping of mitochondrial
ribosomal genes. Journal of Human Evolution 34: 1–23.
Moritz C. 1994. Defining ‘Evolutionarily Significant Units’ for
conservation. Trends in Ecology & Evolution 9: 373–375.
Opdam P. 1991. Metapopulation theory and habitat fragmentation – a review of holarctic breeding bird studies. Landscape Ecology 5: 93–106.
Oppenheimer C. 2002. Limited global change due to the
largest known Quaternary eruption, Toba approximate to 74
kyr BP? Quaternary Science Reviews 21: 1593–1609.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
EVOLUTIONARY HISTORY OF THE MALAY CIVET
Palomares F, Godoy J, Piriz A, O’Brien S, Johnson W.
2002. Faecal genetic analysis to determine the presence and
distribution of elusive carnivores: design and feasibility for
the Iberian lynx. Molecular Ecology 11: 2171–2182.
Patou ML, Chen J, Cosson L, Andersen DH, Cruaud C,
Couloux A, Randi E, Zhang S, Veron G. 2009. Low
genetic diversity in the masked palm civet Paguma larvata
(Viverridae). Journal of Zoology 278: 218–230.
Patou ML, Wilting A, Gaubert P, Esselstyn JA, Cruaud
C, Jennings AP, Fickel J, Veron G. 2010. Evolutionary
history of the Paradoxurus palm civets – a new model
for Asian biogeography. Journal of Biogeography 37: 2077–
2097.
Piper PJ, Ochoa J, Robles EC, Lewis H, Paz V. 2011.
Palaeozoology of Palawan Island, Philippines. Quaternary
International 233: 142–158.
Posada D. 2008. jModelTest: phylogenetic model averaging.
Molecular Biology and Evolution 25: 1253–1256.
Rogers AR, Harpending H. 1992. Population growth makes
waves in the distribution of pairwise genetic differences.
Molecular Biology and Evolution 9: 552–569.
Sathiamurthy E, Voris HK. 2006. Maps of Holocene Sea
Level Transgression and Submerged Lakes on the Sunda
Shelf. The Natural History Journal of Chulalongkorn University Suppl. 2: 1–43.
Schmidt HA, Strimmer K, Vingron M, von Haeseler A.
2002. TREE-PUZZLE: maximum likelihood phylogenetic
analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
Shepherd CR. 2008. Civets in trade in Medan, North
Sumatra, Indonesia (1997-2001) with notes on legal protection. Small Carnivore Conservation 38: 34–36.
Shepherd CR, Shepherd LA. 2010. The trade in Viverridae
and Prionodontidae in Peninsular Malaysia with notes on
conservation and legislation. Small Carnivore Conservation
42: 27–29.
Slik JWF, Aiba S-I, Bastian M, Brearley FQ, Cannon CH,
Eichhorn KAO, Fredriksson G, Kartawinata K,
Laumonier Y, Mansor A, Marjokorpi A, Meijaard E,
Morley RJ, Nagamasu H, Nilus R, Nurtjahya E, Payne
J, Permana A, Poulsen AD, Raes N, Riswan S, van
Schaik CP, Sheil D, Sidiyasa K, Suzuki E, van
Valkenburg JLCH, Webb CO, Wich S, Yoneda T,
Zakaria R, Zweifel N. 2011. Soils on exposed Sunda Shelf
shaped biogeographic patterns in the equatorial forests of
Southeast Asia. Proceedings of the National Academy of
Sciences of the United States of America 108: 12343–12347.
Strimmer K, von Haeseler A. 1997. Likelihood-mapping:
a simple method to visualize phylogenetic content of a
sequence alignment. Proceedings of the National Academy of
Sciences of the United States of America 94: 6815–6819.
Tajima F. 1989. Statistical method for testing the neutral
mutation hypothesis by DNA polymorphism. Genetics 123:
585–595.
Tamura K, Nei M. 1993. Estimation of the number
of nucleotide substitutions in the control region of
mitochondrial-DNA in humans and chimpanzees. Molecular
Biology and Evolution 10: 512–526.
931
Tamura K, Peterson D, Peterson N, Stecher G, Nei M,
Kumar S. 2011. MEGA5: molecular evolutionary genetics
analysis using maximum likelihood, evolutionary distance,
and maximum parsimony methods. Molecular Biology and
Evolution 28: 2731–2739.
Tchaicka L, Eizirik E, De Oliveira TG, Candido JF Jr,
Freitas TRO. 2007. Phylogeography and population
history of the crab-eating fox (Cerdocyon thous). Molecular
Ecology 16: 819–838.
Tougard C. 2001. Biogeography and migration routes of
large mammal faunas in South-East Asia during the
late Middle Pleistocene: focus on the fossil and extant
faunas from Thailand. Palaeogeography, Palaeoclimatology,
Palaeoecology 168: 337–358.
Veron G, Heard Rosenthal S, Long B, Roberton S. 2004.
The molecular systematics and conservation of an endangered carnivore, the Owston’s palm civet Chrotogale owstoni
(Thomas, 1912) (Carnivora, Viverridae, Hemigalinae).
Animal Conservation 7: 107–112.
Voris HK. 2000. Maps of Pleistocene sea levels in Southeast
Asia: shorelines, river systems and time durations. Journal
of Biogeography 27: 1153–1167.
Wallace AR. 1869. The Malay Archipelago: the land of the
Orang-utan and the Bird of Paradise. A narrative of travel,
with studies of Man and Nature. London: Macmillan and Co.
Weber M. 1899. On the origin of the fauna of Celebes. Annals
and Magazine of Natural History, London 7: 121–136.
Williams MAJ, Ambrose SH, van der Kaars S,
Ruehlemann C, Chattopadhyaya U, Pal J, Chauhan
PR. 2009. Environmental impact of the 73 ka Toba supereruption in South Asia. Palaeogeography Palaeoclimatology
Palaeoecology 284: 295–314.
Wilting A, Christiansen P, Kitchener AC, Kemp YJM,
Ambu L, Fickel J. 2011. Geographical variation in
and evolutionary history of the Sunda clouded leopard
(Neofelis diardi) (Mammalia: Carnivora: Felidae) with the
description of a new subspecies from Borneo. Molecular
Phylogenetics and Evolution 58: 317–328.
Wilting A, Sollmann R, Meijaard E, Helgen KM, Fickel J.
2012. Mentawai’s endemic, relictual fauna: is it evidence for
Pleistocene extinctions on Sumatra? Journal of Biogeography 39: 1608–1620.
Winnepenninckx B, Backeljau T, De Wachter R. 1993.
Extraction of high molecular weight DNA from molluscs.
Trends in Genetics 9: 407.
Wisely SM, Maldonado JE, Fleischer RC. 2004. A technique for sampling ancient DNA that minimizes damage to
museum specimens. Conservation Genetics 5: 105–107.
Wurster CM, Bird MI, Bull ID, Creed F, Bryant C,
Dungait JAJ, Paz V. 2010. Forest contraction in north
equatorial Southeast Asia during the Last Glacial Period.
Proceedings of the National Academy of Sciences of the
United States of America 107: 15508–15511.
Ziegler T, Abegg A, Meijaard E, Perwitasari-Farajallah
D, Lutz Walter L, Hodges JK, Roos C. 2007. Molecular phylogeny and evolutionary history of Southeast
Asian macaques forming the M. silenus group. Molecular
Phylogenetics and Evolution 42: 807–816.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014
932
G. VERON ET AL.
SUPPORTING INFORMATION
Additional supporting information may be found in the online version of this article at the publisher’s web-site:
Appendix S1. List of regions and islands where Viverra tangalunga has been recorded, grouped by country and
archipelago, with alternative spellings of names (from this study and Jennings & Veron, 2011; in bold, regions
and islands for which we obtained samples).
Appendix S2. Haplotype network obtained from analysis of the 86 control region sequences; connecting lines
represent single mutations, unless indicated otherwise.
Appendix S3. List of Haplotypes and their GenBank accession numbers.
© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014