Chromosomes of Philippine mammals (Insectivora, Dermoptera, Primates, Rodentia, Carnivora)

11 Pages·2003·6.3 MB·

by  E A Rickart

PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
116(3):699-709. 2003.
Chromosomes of Philippine mammals (Insectivora, Dermoptera,
Primates, Rodentia, Carnivora)
Eric A. Rickart
Utah Museum of Natural History, 1390 E Presidents Circle, University of Utah, Salt Lake City,
Utah 84112, email: [e-mail]
—
Abstract. Karyotypes of nine species of Philippine mammals representing
five orders are presented. Chromosomes of six species are described for the
first time, including three endemic insectivores (Podogymnura truei, Crocidura
beatus, C. grayi), the endemic dermopteran {Cynocephalus volans), an endemic
squirrel {Sundasciurus philippinensis), and a widespread viverrid {Viverra tan-
galunga). Some species endemic to the oceanic Philippines have unique kar-
yotypes whereas other endemics and widespread Asian species have karyotypes
that are similar, or identical, to those ofrelated species or conspecifics occurring
outside the archipelago. These data corroborate patterns of karyotype variation
previously documented for Philippine bats and murid rodents.
For more than a century, the terrestrial land), and 1993 (Mindanao Island). Live-
mammal fauna of the Philippines has been trapped animals were processed and killed
recognized as a unique assemblage (Thom- with sodium pentobarbital within 24 h of
as 1898). All portions of this remarkable capture, and karyotypes prepared from
fauna, which includes 179 species repre- bone marrow and/or spleen cells following
senting nine orders, are characterized by a in vivo methodology (Patton 1967, Rickart
high proportion of endemic species. More et al. 1989). Material from freshly killed an-
than 60% of the mammal fauna, as a whole, imals caught in snap traps was processed in
is endemic (Heaney et al. 1998). For bats vitro (Rickart et al. 1998). Cells were pro-
and murid rodents, the two largest faunal cessed and fixed in the field, and standard
components, cytogenetic studies have pro- (non-differentially stained) karyotypes were
vided insight into how these groups have prepared from stored cell suspensions.
diversified within the archipelago (Rickart Preparations of silver-stained nucleolus or-
et al. 1989, Rickart & Musser 1993, Rickart ganizer regions (Ag-NORs; Howell &
&
et al. 1999, Rickart Heaney 2002). These Black 1980) and G-banded chromosomes
studies suggest that chromosomal data on (Seabright 1971) were made for some taxa.
other Philippine taxa may help clarify their A minimum of 10 chromosomal spreads
phylogenetic and biogeographic relation- was examined from each preparation. Chro-
ships. Accordingly, this report presents kar- mosome terminology follows Rickart and
yotypes of nine species representing five or- Musser (1993). As used herein, fundamen-
ders (Insectivora, Dermoptera, Primates, tal number (FN) refers to the total number
Rodentia, and Carnivora). of chromosome arms in the female karyo-
type (including those of sex chromosomes).
Methods Species nomenclature follows Heaney et al.
(1998).
Specimens were collected during field Voucher specimens were prepared as
studies conducted in 1987 (on Leyte, Bili- skins with partial skeletons, complete skel-
ran and Negros islands), 1988 (Luzon Is- etons, or preserved in fluid, and are depos-
——
700 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
ited in the Field Museum of Natural His- 459818); Mount Pangasugan, 8.5 km N, 2.5
tory, Chicago, IL (FMNH), the National km E Baybay, elev. 500 m, 10°45'30"N,
Museum of Natural History, Smithsonian 124°49'30"E, 1 male (USNM 458723).
Institution, Washington, DC (USNM), and Sundasciurus philippinensis (Water-
—
the Philippine National Museum, Manila house, 1839). Biliran Island, Leyte Prov-
(PNM). Microscope slides of chromosomal ince, 5 km N, 10 km E Naval, elev. 850 m,
preparations and photomicrograph nega- 11°36'N, 124°29'E, 1 male (USNM
tives cross-referenced to cataloged voucher 459821).
specimens are housed at the Utah Museum Paradoxurus hermaphroditus (Pallas,
—
of Natural History, University of Utah, Salt Mil). Leyte Island, Leyte Province, 7 km
Lake City. N, 1.5 km E Baybay, elev. 50 m, 10°45'N,
124°48'E, 1 male (USNM 458891); Mount
Specimens Examined Pangasugan, 10 km N, 2 km E Baybay,
elev. 300 m, 10°46'N, 124°49'E, 1 male
Podogymnura truei Mearns, 1905. (USNM 459999).
—
Mindanao Island, Bukidnon Province, Viverra tangalunga Gray, 1832. Leyte
Mount Kitanglad Range, 16.5 km S, 4 km Island, Leyte Province, Mount Pangasugan,
E Camp Phillips, elev. 1900 m, 8°10'30"N, 10 km N, 2 km E Baybay, elev. 300 m,
124°5rE, 2 males (FMNH 147793, 10°46'N, 124°49'E, 1 male (USNM
147798). 460000).
—
Crocidura beatus Miller, 1910. Leyte
Island, Leyte Province, Mount Pangasugan, Results
10 km N, 4.5 km E Baybay, elev. 950 m,
10°47'N, 124°50'E, male (USNM Order Insectivora
1
Family Erinaceidae
457984).
—
Crocidura grayi Dobson, 1890. Luzon Podogymnura truei. 2N = 40, FN = 76,
—
Island, Camarines Sur Province, Mount Is- Fig. lA. The karyotype of the Mindanao
arog, 4 km N, 22 km E Naga, elev. 1750 gymnure includes 1 1 pairs of small to large-
m, 13°40'N, 123°22'E, 1 female, 1 male sized metacentric or submetacentric auto-
(USNM
573607, 573617).
— somes, 6 pairs of medium-sized subtelocen-
Suncus murinus (Linnaeus, 1766). Ne- tric autosomes, and 2 pairs of small or me-
gros Island, Negros Oriental Province, Sil- dium-sized telocentric autosomes. The
liman Farm, Dumaguete, elev. 5 m, small X chromosome is submetacentric,
(USNM
09°18'N, 123°18'E, 2 males and the minute Y chromosome appears to
457996, 457997); Mount Guinsayawan, 3
W be telocentric.
km N, 17 km Dumaguete, elev. 1470 m,
9°22'N, 123°9'E, 1 female, 1 male (USNM Family Soricidae
458970, 458972).
Cynocephalus volans (Linnaeus, Crocidura grayi. 2N = 38, FN = 58, Fig.
— —
1758). Leyte Island, Leyte Province, 7 km IB. The karyotype of the Luzon shrew in-
N
Baybay, elev. 10 m, 10°45'N, cludes 4 pairs of small to medium-sized
124°47'30"E, 1 female (USNM 458982). submetacentric autosomes, 5 pairs of small
Tarsius syrichta (Linnaeus, 1758). to large-sized subtelocentric autosomes, and
Leyte Island, Leyte Province, 7 km N, 1.5 9 pairs of small to large-sized telocentric
km E Baybay, elev. 50 m, 10°45'N, autosomes. The X chromosome is medium-
124°48'E, 1 male (PNM specimen, EAR sized and subtelocentric, and the small Y
field number 1441); Mount Pangasugan, chromosome is submetacentric.
10.2 km N, 2.2 km E Baybay, elev. 320 m, Crocidura—beatus. 2N = 38(?), FN = ?,
10°46'N, 124°49'E, 1 male (USNM not figured. A poor quality in-vivo prep-
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A
M
KK jm %n
XX
^j(
»l «ft ^'ift^*
lift ftft
AA
• - ?
Y
B
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/>o
no
aa
Aa AA
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)[y
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iio All
Fig. 1. Karyotypes of: A) Podogymnura truei, male (FMNH 147793) from in vitro preparation, 2N = 40;
B) Crocidura grayi, male (USNM 573617), 2N = 38; C) Suncus murinus, female (USNM 458970), 2N = 40.
702 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
aration yielded preliminary information on Island includes 9 pairs of metacentric or
the chromosomes of this species which is submetacentric autosomes, 7 pairs of sub-
endemic to the Mindanao faunal region. telocentric autosomes, and 2 pairs of small
The modal chromosome count from multi- telocentric autosomes. The medium-sized X
ple spreads was 38, indicating a karyotype chromosome is submetacentric and the mi-
similar to that of C grayi (Fig. IB). nute Y chromosome appears to be telocen-
Suncus murinus. 2N = 40, FN = 60, Fig. tric.
—
IC. Specimens of the Asian house shrew
from Negros Island have a karyotype that Order Carnivora
includes 4 pairs of small to large-sized sub- Family Viverridae
metacentric autosomes, 5 pairs of small to
Paradoxurus hermaphroditus. 2N = 42,
medium-sized subtelocentric autosomes, —
FN = 72, Fig. 4A. Specimens of the com-
and 10 pairs of medium to large-sized telo-
X Y mon palm civet from Leyte Island have a
centric autosomes. Both the and chro-
karyotype that includes 8 pairs of small to
mosomes are submetacentric.
large-sized metacentric or submetacentric
autosomes, 6 pairs of small to large-sized
Order Dermoptera
subtelocentric autosomes, and 6 pairs of
Family Cynocephalidae
small to medium-sized telocentric auto-
Cynocephalus volans. 2N = 38, FN = somes. The medium-sized X chromosome
—
Y
40, Fig. 2. The standard karyotype of a is submetacentric, and the small chro-
mosome
female Philippine flying lemur from Leyte is telocentric.
Island includes 18 pairs of small to large- Viverr—a tangalunga. 2N = 36, FN = 64,
sized telocentric autosomes and a pair of Fig. 4B. The karyotype of a male Malay
medium-sized submetacentric X chromo- civet from Leyte Island includes 7 pairs of
somes. A G-banded preparation reveals G- small to large-sized metacentric or sub-
positive bands on the nine largest auto- metacentric autosomes, 6 pairs of small to
somes. The X chromosome is largely G- large-sized subtelocentric autosomes, and 4
positive. Ag-NORs are located terminally pairs of small telocentric autosomes. The X
on the smallest telocentric autosomes. chromosome is large and submetacentric
and the small Y chromosome is telocentric.
Order Primates
Discussion
Family Tarsiidae
Tarsius syrichta. 2N = 80, FN = 94, Fig. The 2N = 40, FN = 76 karyotype of
—
3A. Karyotypes of male Philippine tarsi- Podogymnura truei (Fig. lA) is the first re-
ported for the gymnure subfamily Hylo-
ers from Leyte Island include 6 pairs of
small to large-sized metacentric or sub- myinae. It differs substantially from those
of hedgehogs (subfamily Erinaceinae)
metacentric autosomes and 33 pairs of
which have relatively uniform karyotypes
small to large-sized telocentric autosomes.
The submetacentric X and minute Y chro- of 2N = 48, FN = 90-96 and X chromo-
mosomes are, respectively, the largest and somes that are substantially larger than that
&
of P. truei (Gropp 1969, Bhatnagar El-
smallest elements in the karyotype.
Azawi 1978, Hubner et al. 1991, Reumer &
Meylan 1986).
Order Rodentia
The widespread genus Crocidura dis-
Family Sciuridae
plays extensive interspecific chromosomal
Sundasciurus philippinensis. 2N = 38, variation (Maddalena & Ruedi 1994, Zima
—
FN = 72, Fig. 3B. The karyotype of a et al. 1998). There are seven species of
&
male Philippine tree squirrel from Biliran Crocidura in the Philippines (Heaney
VOLUME NUMBER
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(JHA fik/ii
(0 tk AA OA AO *>>
X X
B
^alw 4^^ z^
^
as*
Bstf HM St Ik*
S II e*^ ftti A*^
f
SA
9|i it e*
!t;$ ftii
il
X X
Fig. 2. Karyotypes of Cynocephalus volans, female (USNM 458982), 2N = 38: A) standard, inset of Ag-
NOR
sites; B) G-banded.
704 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
9noi AO
Al 0)
Ofi
u M
M
id la Ai
An An «n od
(II
0»
A0
<^0
%l\ ft<^
A^ AO
At ^
ftO »»* ^
h u
u
ft^ ^Jf 5t«
A^ AA
5^
#S^ AJS ii^
X Y
Fig. 3. Karyotypes of: A) Tarsius syrichta, male (EAR 1441), 2N = 80; B) Sundasciurus philippinensis,
male (USNM 459821), 2N = 38.
VOLUME 116, NUMBER 3 705
A
X Y
A# ••
nt% *••
iiA
HA
XX
If XI XX
M X Y
oiiA 16
II
Fig. 4. Karyotypes of: A) Paradoxurus hermaphroditus, male (USNM 458891), 2N = 42; B) Viverra tan-
galunga male (USNM 460000), 2N = 36.
Ruedi 1994) of which two have been kar- limited data available suggest that the di-
yotyped (this study). The 2N = 38, FN = versification of Philippine Crocidura has
C
58 karyotype of grayi (Fig. IB) resem- not involved major chromosomal rearrange-
bles those of several species with 2N = 38, ments of the sort seen for members of the
FN = 54-58 from islands of the Sunda genus in Sulewesi (Ruedi & Vogel 1995),
&
Shelf and from Sulewesi (Ruedi Vogel or for Philippine rodents of the genus Apo-
& &
1995). It also is similar to the presumed an- mys (Rickart Musser 1993, Rickart
cestral arrangement for Crocidura (Mad- Heaney 2002).
&
dalena Ruedi 1994). The apparent simi- Suncus murinus is a chromosomally
larity in the karyotypes of C. grayi and C. polymorphic species (2N = 30-40) found
beatus is consistent with morphometric and throughout much of southeast Asia (Yosh-
allozyme data that place these species as ida 1985, Zima et al. 1998). It occurs
&
sister-taxa (Heaney Ruedi 1994). The throughout the Philippines as a non-native
706 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
commensal (Heaney et al. 1998), and on Leyte Island (Fig. 3A) is identical to those
Negros Island, it also is naturalized and previously reported for specimens from
&
abundant in primary forest habitat (Heaney Mindanao (Boer Boer-Van der Vlist
&
et al. 1989). Both commensal and natural- 1973, Dutrillaux Rumpler 1988). Tarsius
ized animals from Negros have identical bancanus also has 2N = 80, FN = 94
karyotypes of 2N = 40, FN = 60 (Fig. IC). (Klinger 1963), but its karyotype differs
This same arrangement has been reported from that of T. syrichta in the size and rel-
for specimens from much of southeast Asia ative arm lengths of several of the biarmed
(Zima et al. 1998). Medina and Leonard autosomes. Tarsius dianae from central Su-
(1977) reported a karyotype of 2N = 40, lawesi is the only other tarsier that has been
FN = 54 for S. luzoniensis (a synonym of karyotyped. Its arrangement of 2N = 46,
S. murinus) from Luzon Island. The differ- FN = 82 (Niemitz et al. 1991) differs from
ence in FN compared to the Negros speci- those of T. syrichta and T. bancanus by
mens most likely reflects variable assess- multiple Robertsonian and non-Robertso-
ment of minute secondary arms on subtel- nian events. Chromosomal data support
ocentric autosomes. phylogenetic hypotheses based on compar-
The 2N = 38, FN = 40 karyotype of ative morphology and behavior that asso-
Cynocephalus volans (Fig. 2), one of two ciate the Philippine and Sundaic species {T.
members of the mammalian order Dermop- syrichta and T. bancanus) as relatively spe-
tera, is reported here for the first time. This cialized forms separate from the three spe-
also corrects an erroneous report by Hsu cies of Sulawesian tarsiers (Niemitz 1977,
&
and Benirschke (1973). They published Musser Dagosto 1987, Dagosto et al.
identical karyotypes of 2N = 56, FN = 72 2001).
for a specimen of Galeopterus variegatus The 2N = 38, FN = 72 karyotype of
from Malaysia and for an animal at the Lin- Sundasciurus philippinensis (Fig. 3B) is re-
coln Park Zoo, Chicago, originally identi- ported here for the first time. It is identical
fied as C volans. After the latter died, it to that of S. jentinki, the only other member
was sent to the Field Museum where it was of the genus that has been karyotyped (Har-
accessioned and correctly identified as Gal- ada & Kobayashi 1980). Among callosci-
eopterus (FMNH 60308; W. Stanley, pers. urine squirrels, Dremomys rufigenis and
comm.). The two dermopterans have sub- Callosciurus albescens also share this ar-
&
stantially different karyotypes. Cynocephal- rangement (Nadler Hoffmann 1970, Har-
&
us lacks nine pairs of autosomes present in ada Kobayashi 1980), and several other
Galeopterus, including seven pairs of small species of Callosciurus have karyotypes of
to large-sized biarmed chromosomes, and 2N = 40, FN = 70-74 that differ only
the X chromosome of the former is sub- slightly from that of S. philippinensis (Nad-
metacentric whereas that of the latter is ler et al. 1975, Yong Hoi-Sen et al. 1975,
metacentric (Fig. 2; Hsu & Benirschke Oshida & Yoshida 1999). The available
1973). The Ag-NORs of Cynocephalus are data suggest that callosciurines are chro-
located on the smallest autosomal pair (Fig. mosomally conservative.
2). In Galeopterus, this same pair bears sec- A karyotype of 2N = 42, FN = 78 was
&
ondary constrictions (Hsu Benirschke reported previously for Paradoxurus her-
1973). This chromosomal distinctiveness is maphroditus from India (Ray-Chaudhuri et
in accord with the substantial morphologi- al. 1966). The karyotype of Philippine
cal and ecological differences that suggest specimens (Fig. 4A) is similar, but appears
ancient divergence of the two species and to have fewer subtelocentric and more telo-
supports their placement in separate genera centric elements (FN = 72). In other re-
&
(Stafford Szalay 2000). spects, the two karyotypes are identical.
The karyotype of Tarsius syrichta from The 2N = 36, FN = 64 karyotype of
—
VOLUME 116, NUMBER 3 707
Viverra tangalunga (Fig. 4B) is the first re- baranza, L. Tag-at, and R. Utzurrum for as-
ported for this widespread southeast Asian sistance with field work. W. Stanley
species. Viverra zibetha, the only other (FMNH) provided information on the iden-
member of this genus that has been exam- tity and history of the dermopteran speci-
ined has a substantially different karyotype men formerly at Lincoln Park Zoo. Com-
of 2N = 38 and FN = 68 (Pathak 1971). ments from L. Heaney and two anonymous
Among members of the subfamily Viverri- reviewers helped improve the manuscript.
nae that have been examined, Viverricula Permits and logistical support were provid-
indica is the only species with 2N = 36 ed by the Philippine Protected Areas and
&
(Wurster Benirschke 1968). However, Wildlife Bureau and the Philippine Bureau
Viverra tangalunga has more telocentric of Forestry Development. Field work was
and fewer subtelocentric autosomes, and a supported by grants from the National Sci-
significantly smaller Y chromosome than ence Foundation (BSR 8514223), the John
does Viverricula. D. and Catherine T. MacArthur Foundation
Interpretation of these chromosome data (90-09272A), and the Barbara Brown and
is limited, in some cases, by the lack of Ellen Thorne Smith funds of the Field Mu-
comparative information on related taxa. seum.
Nonetheless, some general patterns of var-
iation are apparent. Members of the endem-
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