PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
115(3):473-487 . 2002.
Further studies on the chromosomes of Philipmne rodents ^'^/\/
Eric A. Rickart and Lawrence R. Heaney Ns^ , A
(EAR) Utah Museum of Natural History, University of Utah, Salt Lake CTT Utah 84112, U.S.A.; (LRH) Department of Zoology, Field Museum of Natural History, Chicago, Illinois 60605, U.S.A.
Abstract. —Standard karyotypes of ten species of Philippine murine rodents representing seven genera are reported for the first time, and new information
is presented for six additional species. Data now available from 25 species (39% of the total Philippine murine fauna) reveal substantial karyotypic di- versity, but also show differences among subgroups in the degree of interspe- cific variability. Within some genera there are major karyotypic differences between species whereas other groups appear to be highly conservative. These data provide only limited information on phylogenetic relationships, but are very useful in clarifying boundaries between groups. In some genera, speciation events apparently have been accompanied by major chromosomal rearrange-
ments. Only a single case is now known of congeneric species having the same karyotype on a single landmass.
As presently understood, the remarkably and Chrotomys, and additional information diverse murine rodent fauna of the Philip- on species reported previously (Rickart & pines includes 64 species belonging to 23 Musser 1993, Rickart et al. 1998). We dis- genera (Heaney et al. 1998). Of these, 55 cuss the significance of this expanded data species (86%) and 16 genera (70%) are en- set within the context of the alternative phy- demic to the Philippines, a pattern that re- logenetic hypotheses posed by Musser & flects relatively few successful colonization Heaney (1992). events followed by repeated speciation and diversification within this isolated archipel- Methods ago (Heaney & Rickart 1990). An earlier report on karyotypes of several Philippine Specimens were collected directly from murines (Rickart & Musser 1993) revealed wild populations during field studies con- substantial diversity in chromosomal char- ducted in 1988 (on Catanduanes, Luzon, acteristics, and provided some support for and Negros islands), 1993 (Mindanao Is- phylogenetic relationships inferred from land), and 2001 (Luzon Island). Animals morphology. captured in live traps were processed and In this paper, we present new chromo- killed with sodium pentobarbital within 24 somal data from 16 species of Philippine h of capture. Cells were prepared from bone
murines representing 1 1 genera; this brings marrow and/or spleen tissue following in the total to 25 species kairyotyped from the vivo methodology (Patton 1967, as modi-
Philippines. Included are the first reports on fied by Rickart et al. 1989). Material from chromosomes of three endemic genera {Ce- freshly killed animals caught in snap traps
laenomys, Limnomys, and Tarsomys), first was processed in vitro (Rickart et al. 1998). reports for species in the genera Apomys Cells were processed and fixed in the field, — —
474 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON and standard (non-differentially stained) PhilHps, elev. 1,900 m, 8°10'30"N, 124°51'E, karyotypes were prepared from stored cell 1 female (FMNH 147929). suspensions. Giemsa-banded preparations Batomys granti Thomas, 1895.—Luzon were made for some taxa (Seabright 1971). Island, Kalinga Province, Balbalan Munic- Determinations of diploid number were ipality, Balbalasang, Magdallao, elev. 1,600 based on counts from a minimum of 10 m, 17°28'30"N, 12r04'30"E, 1 male cells per individual. Chromosome terminol- (FMNH 169125). ogy follows Rickart & Musser (1993). As Archboldomys luzonensis Musser, used here, fundamental number (FN) refers 1982b. —Luzon Island, Camarines Sur to the number of major chromosome arms Province, Mount Isarog, 4 km N, 21.5 km in the entire complement (excluding very E Naga, elev. 1,350-1,750 m, 13°40'N, minute arms). Because non-differentially 123°22'E, 1 female, 1 male (USNM stained chromosomes seldom reveal the full 573505, 573840). extent of variation (Haiduk et al. 1981), dif- Archboldomys musseri Rickart et al., ferences between standard karyotypes are 1998.—Luzon Island, Kalinga Province, considered minimal reflections of actual Balbalan Municipality, Balbalasang, Am-li- differences, while apparent similarities are cao, 1,900 m, 17°26'30"N, 121°04'15"E, 1 interpreted cautiously. Statements regarding male (FMNH 169122). possible directions of karyotypic change are Crunomys suncoides Rickart et al., based on outgroup comparisons, not on a 1998.—Mindanao Island, Bukidnon Prov- priori assumptions as to the relative fre- ince, Mount Katanglad Range, 18.5 km S, quency of chromosome fusion vs. fission, 4 km E Camp Phillips, elev. 2,250 m, or that common arrangements are primitive 8°9'30"N, 124°5rE, 1 male (FMNH (Qumsiyeh & Baker 1988). 147942). The sampled taxa are in the subfamily Mus musculus castaneus Waterhouse, Murinae of the family Muridae, as defined 1843. —Negros Island, Negros Oriental by Musser & Carleton (1993). Specimens Province, Silliman Farm, Dumaguete, elev. examined were prepared as complete skel- 5 m, 09°18'N, 123°18'E, 1 female, 1 male etons or preserved in fluid and are depos- (USNM 459896, 459897). ited in the Field Museum of Natural His- Celaenomys silaceus (Thomas, 1895). tory, Chicago (FMNH), the National Mu- Luzon Island, Kalinga Province, Balbalan seum of Natural History, Smithsonian In- Municipality, Balbalasang, Am-licao, elev. stitution, Washington (USNM), and the 1,800 m, 17°26'30"N, 121°04'15"E, 1 male Philippine National Museum, Manila (FMNH 169132). (PNM). Microscope slides and photomicro- Chrotomys whiteheadi Thomas, 1895. graph negatives are housed at the Utah Mu- Luzon Island, Kalinga Province, Balbalan seum of Natural History, University of Municipality, Balbalasang, Mapga, 1,050
Utah, Salt Lake City. m, 17°28'30"N, 12r04'30"E, 1 male (FMNH 169139). Specimens Examined Rhynchomys isarogensis Musser & Free- man, 1981.—Luzon Island, Camarines Sur Phloeomys cumingi (Waterhouse, 1839). Province, Mount Isarog, 4 km N, 21.5 km Catanduanes Island, Catanduanes Province, E Naga, elev. 1,350-1,750 m, 13°40'N. vicinity of Barrio Summit, elev. 250 m, 123°22'E, 3 males (USNM 573575.
13°47'N, 124°19'E, 1 female (PNM speci- 573905, 573910). men, EAR field number 1662). Apomys datae (Meyer, 1899). —Luzon Batomys saloinoiiseiu (Sanborn, 1953). Island, Kalinga Province, Balbalan Munic- Mindanao Island, Bukidnon Province, Mount ipality, Balbalasang, Mapga. 1,050 m. Katanglad Range, 16.5 km S, 4 km E Camp 17°28'30"N, 121°04'30"E, 3 males (FMNH —1
VOLUME 115, NUMBER 3 475 H m f i H $a l^d sn '^* il XX u «» S3 «t Ift lg &'> i^ 5S 4^ a Sfi «<)» !*•
Fig. 1. G-banded chromosomes of Phloeomys cuiningi female (EAR 1662), 2N = 44, FN = 66.
169051, 169065, 169066), Am-licao, 1,800 Limnomys sibuanus Mearns, 1905. m, 17°26'30"N, 121°04'15"E, 1 male Mindanao Island, Bukidnon Province, (FMNH 169111). Mount Katanglad Range, 16.5 km S, 4 km Apomys hylocoetes Mearns, 1905.—Min- E Camp Phillips, elev. 1,900 m, 8°10'30"N, danao Island, Bukidnon Province, Mount 124°51'E, 1 female, 1 male (FMNH Katanglad Range, 16.5 km S, 4 km E Camp 147944, 147946). Phillips, elev. 1,900 m, 8°10'30"N, Limnomys sp.—Mindanao Island, Bukid-
124°51'E, 1 female, 1 male (FMNH 147871, non Province, Mount Katanglad Range, 147872), 18.5 km S, 4 km E Camp Phillips, 16.5 km S, 4 km E Camp Phillips, elev. elev. 2,250 m, 8°9'30"N, 124°51'E, 2 fe- 2,250 m, 8°10'30"N, 124°51'E, 2 males males, 2 males (FMNH 147875, 147878, (FMNH 147972, 147975). 147880, 147914). Apomys insignis Mearns, 1905.—Minda- Results nao Island, Bukidnon Province, Mount Ka- tanglad Range, 16.5 km S, 4 km E Camp Phloeomys cumingi. 2N = 44, FN = 66, Phillips, elev. 1,900 m, 8°10'30"N, 124° Fig. 1.—The standard karyotype of this 51'E, 1 female, 3 males (FMNH 147912, species, endemic to Luzon faunal region, 147913, 147915, 147916). was described by Rickart & Musser (1993). Tarsomys apoensis Mearns, 1905.—Min- The autosomal complement includes 8 pairs danao Island, Bukidnon Province, Mount of metacentric or submetacentric and 1 Katanglad Range, 16.5 km S, 4 km E Camp pairs of telocentric chromosomes. The sub- Phillips, elev. 1,900 m, 8°10'30"N, 124° metacentric X chromosome is the largest el- 51'E, 3 males (FMNH 147953, 147955, ement in the karyotype, and the submeta- 147956), 18.5 km S, 4 km E Camp Phillips, centric Y chromosome is only slightly elev. 2,250 m, 8°9'30"N, 124°51'E, 1 female, smaller. In a G-banded preparation, here re- 2 males (FMNH 147957, 147960, 147969). ported for the first time, some band patterns 476 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
)l II il H n il < { - Of It t% u !; X X"
Il )': ft It U II O II 91 •* «l ) II ft 9S tt •• •- X Y it #4 %^ *t» s m
Fig. 2. Chromosomes of: A, Archboldomys liizoiiensis male (USNM 573505), 2N = 26, FN = 43. G-banded preparation, with (inset) sex chromosomes of female (USNM 573840); B, Archboldomys miisseh male (FMNH 169122), 2N = 44(?), in-vitro preparation from a snap-trapped specimen, identity of sex chromosomes tentative.
are seen on all but the smallest chromo- Batomys salomonseni. 2N = 52, FN = somes allowing most pairs to be matched 52, not figured.—The standard karyotype accurately. of a specimen from Mindanao appears to Batomys granti. 2N = 52; FN = 52, not be identical to that reported for specimens figured.—The karyotype of a specimen of of this species from Leyte, and is indistin- this Luzon endemic from Kalinga Province guishable from the standard karyotype of fi. in northern Luzon consists of 52 telocentric granti (Rickart & Musser 1993). chromosomes, and is indistinguishable from Archboldomys luzonensis. 2N = 26, FN that reported for specimens from Mt. Isarog = 43, Fig. 2A.—The standard karyotype of in southern Luzon (Rickart & Musser this species, restricted to Mt. Isarog in 1993). southern Luzon, was described by Rickart VOLUME 115, NUMBER 3 477
& Musser (1993). The autosomes include 8 centric, 1 pair of large submetacentric, 1 biarmed and 4 telocentric chromosome pair of large subtelocentric, and 18 pairs of pairs. The submetacentric X chromosome is small to large-sized telocentric elements. the largest element in the karyotype, and The X and Y chromosomes cannot be dis- the Y is small and telocentric. In the one tinguished from the autosomes, but presum- available female specimen, the X chromo- ably are included within the telocentric se- some is paired with a large telocentric ele- ries. ment. G-banded preparations, here reported Chrotomys whiteheadi. 2N = 38, FN = for the first time, reveal distinct banding 52, Fig. 4B.—The karyotype of this spe- patterns on all autosomes. The long arm of cies, a northern Luzon endemic, is here re- the X chromosome and the large telocentric ported for the first time. It consists of 2 chromosome of the female appear to have pairs of small metacentric, 4 pairs of me- some homologous G-banding. The smaller dium to large-sized submetacentric, 1 pair telocentric Y chromosome also has a dis- of large subtelocentric, and 12 pairs of tinct band pattern. small to large-sized telocentric chromo- Archboldomys musseri. 2N = 44?; FN = somes. The sex chromosomes are telocen-
?, Fig. 2B.—A poor-quality in vitro prepa- tric and cannot be distinguished from the ration from a male specimen yielded pre- autosomes. liminary information on the chromosomes Rhynchomys isarogensis. 2N = 44, FN of this species which is restricted to north- = 52, not figured.—The karyotype of this ern Luzon. A diploid number of 44 is es- species was first described by Rickart & timated for a complement consisting largely Musser (1993). Reexamination of material of telocentric elements. The X chromosome from male specimens reveals that the Y is tentatively identified as the largest ele- chromosome is telocentric rather than sub- ment and the Y chromosome may be a metacentric as reported previously. The small, telocentric element. standard karyotype is indistinguishable Crunomys suncoides. 2N = 36, FN = 36, from that of Celaenomys (Fig. 4A). Fig. 3A.—Rickart et al. (1998) made a pre- Apomys datae. 2N = 44, FN = 54, Fig. liminary report on the karyotype of this 5A.—This is the first report on the karyo- species, which is known only from Mount type of this species which is restricted to Katanglad, Mindanao. Cells from a single northern Luzon Island. The autosomal com- male specimen processed in vitro contain plement includes 5 pairs of small to large- 36 telocentric chromosomes. Based on rel- sized biarmed chromosomes and 16 pairs of ative size, we tentatively identify the X small to medium-sized telocentric elements. chromosome as one of the largest elements The X chromosome is large and telocentric, in the karyotype, and the Y chromosome as and the Y chromosome is small and telo- one of the smallest. centric. Mus musculus castaneus. 2N = 40, FN Apomys hylocoetes. 2N = 48, FN = 56, = 40, Fig. 3B.—Specimens of the non-na- Fig. 5B.—The karyotype of this species, a tive Asian house mouse from Negros Island Mindanao Island endemic, is here reported
have a karyotype of 40 telocentric ele- for the first time. It includes 1 pair of small ments, comparable to those documented for submetacentric, 3 pairs of small subtelocen-
specimens from Thailand (Markvong et al. tric, and 20 pairs of small to large-sized 1973). telocentric chromosomes. Both sex chro- Celaenomys silaceus. 2N = 44, FN = 52, mosomes are telocentric and cannot be dis- Fig. 4A.—The karyotype of this species, tinguished from the autosomal complement. belonging to a monotypic genus restricted Apomys ins ignis. 2N = 36, FN = 72, Fig. to northern Luzon, is here reported for the 5C.—This is the first report on the chro- first time. It includes 2 pairs of small meta- mosomes of this species which is restricted 478 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
U fi» H <8
^^^ ISI Al Al nk
00 ^^ Mk AA
XY
Fig. 3. Chromosomes of: A, Cninomys simcoides male (FMNH 147942), 2N = 36, FN = 36, in vitro preparation from a snap-trapped specimen, identity of sex chromosomes tentative; B, Mus imisciilus male (USNM 459896), 2N = 40, FN = 40.
to the Mindanao faunal region. Available Limnomys sibuanus. 2N = 42, FN = 61/ material was prepared in vitro from snap- 62, Fig. 6A.—This is the first report on the trapped specimens. The karyotype consists chromosomes of this species, which is en- entirely of biarmed chromosomes, includ- demic to Mindanao Island. Available ma- ing 5 pairs of small to large-sized metacen- terial was prepared in vitro from snap-
tric, 3 pairs of large submetacentric, and 10 trapped specimens, and quality is relatively pairs of subtelocentric elements. The sex poor. The autosomal complement includes chromosomes cannot be distinguished from 7 metacentric or submetacentric, 2 subtel-
the autosomes, but presumably aie included ocentric, and 1 1 telocentric pairs. The X within the subtelocentric series. chromosome is medium-sized and subtelo- VOLUME 1 15, NUMBER 3 479 A ft K • n n M n\ »l Art an oA «A n« *• *ft *• <"* B Jinx II
*o Oft in r>fi
Fig. 4. Chromosomes of: A, Celaenomys silaceus male (FMNH 169132), 2N = 44, FN = 52; B, Chrotomys whiteheadi male (FMNH 169139), 2N = 38, FN = 52. The sex chromosomes cannot be distinguished from the autosomes in either karyotype.
centric, and the telocentric Y chromosome is here reported for the first time. The au- is the smallest element in the karyotype. tosomes and the X chromosome appear to Limnomys sp. 2N = 42, FN = 61/62, Fig. be identical to those of Limnomys, but the 6B.—The standard karyotype of an unde- telocentric Y chromosome is substantially scribed species of Limnomys from Mount larger. Katanglad, Mindanao Island, is here report- ed for the first time. It appears to be iden- Discussion tical to that of Limnomys sibuanus. Tarsomys apoensis. 2N = 42, FN = 61/ In a review of morphological character- 62, Fig. 6C.—The standard karyotype of istics of Philippine murines, Musser & Hea- this species, endemic to Mindanao Island, ney (1992) recognized three principal 480 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
ft- At IK AK M M « XY HIV flA
^^ m. Jlk 4^ 1^ 4^ A ^ ^ ^% •^ •^
«» A A A B
(!A ftfi 90 ^^^ oa Aft 00 Ift i^^ 'i'^ ^^ AA A 1^ MA kcnus ID U Aft ft^ ftt A*
Aft AA ^ K AA
Fig. 5. Chromosomes of: A, Aponiys clatae male (FMNH 16905 1 ), 2N = 44, FN = 54; B. Apoiiiys hylacoetes female (FMNH 147880), 2N = 48, FN = 56: C, Apomys iuslgnis male (FMNH 147915), 2N = 36. FN = 72. in vitro preparation from a snap-trapped specimen. The sex chromosomes cannot be distinguished from the autosomes in these karyotypes. VOLUME 1 15, NUMBER 3 481 A KK fC|t 4>l
na AA li t hA AO -^A <\ jk fi ^ X X B 1 a AHA II A
A/\ aA AA <« A • ^ * XY C Xl ^X XK ff % 4ii • K
Fig. 6. Chromosomes of: A, Limnomys sibuamis female (FMNH 147943), 2N = 42, FN = 62, in vitro preparation from a snap-trapped specimen; B, Limnomys sp. male (FMNH 147975), 2N = 42, FN = 61; C, Tarsomys apoensis male (FMNH 147960), 2N = 42, FN = 61. 482 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON groups of genera and formulated alternative Pequignot et al. 1983, 1985). Although this hypotheses regarding their potential phylo- has been accepted as a working hypothesis genetic relationships. Our discussion of (Rickart & Musser 1993), there is no in- chromosomal characteristics is framed dependent evidence to support it. The kar- within this context. yotype of Batomys and those of Phloeomys The genus Phloeomys includes two differ substantially, providing no support named species of large, arboreal, folivorous for a hypothesized close relationship be- rats: P. cumingi from southern Luzon and tween these groups of arboreal rats (Musser adjacent islands of Catanduanes and Marin- & Heaney 1992). Batomys, the shrew rats duque, and P. pallidus from central and (Fig. 4; Rickart & Musser 1993:9, fig. 6), northern Luzon (Heaney et al. 1998). Al- and Apomys musculus (Rickart & Musser though Phloeomys is morphologically dis- 1993:6, fig. 3B), all have FN = 52. How- tinct from other Philippine murines, Musser ever, this resemblance may be entirely co- & Heaney (1992) considered a relationship incidental as there are no morphological with the CrateromyslBatomys group as one characteristics that support a particularly alternative hypothesis. Based on non-differ- close association of Batomys with these entially stained chromosomes, Rickart & taxa (Musser & Heaney 1992). Musser (1993) estimated a minimum of two The genus Archboldomys is endemic to Robertsonian and three non-Robertsonian Luzon Island and includes two named spe- events separating the karyotypes of P. cum- cies, A. luzonensis and A. musseri (Musser ingi (2N = 44, FN = 66) and P. pallidus 1982b, Rickart et al. 1998). Rickart & Mus- (2N = 40, FN = 60). A comparison of the ser (1993) reported the standard karyotype Giemsa-banded preparation from P. cum- of A. luzonensis (2N = 26, FN = 43) and ingi (Fig. 1) with published karyotypes of discussed an aberrant sex chromosome ar- P. pallidus (Jotterand-Bellomo & Schauen- rangement in that species. Three male spec- berg 1988:183-184, figs. 2 & 3) reveal imens all have a karyotype that includes a some additional differences. Although the large submetacentric X chromosome (the preparations differ in the degree of chro- largest element in the complement) and a mosome condensation, the absence of any small telocentric Y chromosome. In Giem- obvious arm homologies suggests that sa-banded preparations (Fig. 2A), the X banding patterns have been altered through chromosome appears similar to that of multiple non-Robertsonian events. The X Phloeomys (Fig. 1). The faint banding on chromosomes of the two species also ap- the long arm is probably the same pattern pear to differ. seen among many murines (Baverstock et The arboreal and scansorial rats of the al. 1983, Gadi & Sharma 1983, Jotterand- folivorous genera Batomys, Carpomys, and Bellomo & Schauenberg 1988). The other Crateromys are united by a suite of derived arm is apparently unhanded and heterochro- morphological features (Musser & Heaney matic, which also is common among mu- 1992, Musser et al. 1998). Within this rines (Baverstock et al. 1977, Gadi & Shar- group, chromosomal data are available only ma 1983). The one available female speci- for Batomys granti and B. salomonseni. men of A. hizonicus (which was phenotyp- Specimens from four population samples ically normal and pregnant when captured)
(two of each species) have indistinguishable is heterozygous for what appears to be an standard karyotypes of 52 telocentric chro- X chromosome deletion involving the loss mosomes (Rickart & Musser 1993:5, fig. 2). of the heterochromatic arm (Fig. 2A, inset). The high diploid number and predominance Information on the chromosomes of of telocentric elements in the Batomys kar- Archboldomys nnisseri is limited to a poor- yotype are characteristics that have been quality in vitro preparation from one male considered primitive for murines (Viegas- specimen (Fig. 2B), but it is sufficient to VOLUME 115, NUMBER 3 483
reveal substantial differences from A. lu- diploid numbers ranging from 26 to 48
zonensis. Although the diploid number of (Rickart & Musser 1993:17, table 1). Fur- 44 is an estimate, chromosome counts from thermore, members of the Asian subgenus multiple cells from this specimen were con- Coelomys also have "shrew-mouse" mor- sistently greater than the 2N = 26 of A. phologies with external, cranial, and dental luzonensis, and there appear to be more similarities to Crunomys (Marshall 1977, telocentric elements. The relative size of the Musser & Newcomb 1983). As with Arch- presumed X chromosome (the largest ele- boldomys, however, Mus {Coelomys) retains ment) is the only clear similarity between a primitive cephalic arterial pattern and has the two karyotypes. morphological specializations that distin-
Archboldomys and Crunomys share fea- guish it from Crunomys and may preclude tures of external, cranial, and dental mor- a close relationship (Musser & Newcomb phology, and have been considered close 1983, Musser & Heaney 1992). relatives (Musser 1982b, Musser & Heaney The endemic genera Chrotomys, Celae- 1992). However, their similarities may rep- nomys, and Rhynchomys include seven spe- resent shared primitive traits or simply re- cies of large-bodied Philippine "shrew- flect ecological convergence as relatively rats". Each has morphological specializa- small, insectivorous "shrew-mice" (Rickart tions that reflect vermivorous habits (Rick- et al. 1998). Chromosomal data do not in- art & Heaney 1991, Rickart et al. 1991, dicate a close relationship. Crunomys sun- Musser & Heaney 1992, Heaney et al. coides (Fig. 3A) resembles A. luzonensis in 1999). The morphological differences be- having a relatively low fundamental num- tween Rhynchomys and the other two gen- ber compared to other endemic Philippine era are so distinct that Thomas (1895, 1898) murines (Rickart & Musser 1993), but the placed them in different murid subfamilies. entirely telocentric complement is consid- However, because they share many derived erably different from the Archboldomys morphological traits, Musser and Heaney karyotypes. (1992) postulated monophyly of the three Aside from Crunomys, relatively few of shrew-rat genera. the Asian murines that have been karyo- Chromosomally, the shrew-rats are a typed have complements that are wholly comparatively uniform group. The standard telocentric (Rickart & Musser 1993:22, fig. karyotype of Celaenomys silaceus (Fig. 8). Batomys is the only other native Phil- 4A) is identical to those of Rhynchomys is-
ippine murine that does, but it has a much arogensis (as reanalyzed in this study) and higher diploid number than does Crunomys. Chrotomys gonzalesi (Rickart & Musser Furthermore, the two genera have very dis- 1993:9, fig. 6). All have 2N = 44, FN = similar morphologies and are not thought to 52, with two pairs of very small metacentric be closely related (Musser & Heaney 1992, chromosomes, one pair of large submeta- Musser et al. 1998, Rickart et al. 1998). The centric, a pair of large subtelocentric, and standard karyotype of Crunomys most 18 pairs of telocentric chromosomes. closely resembles those of Cremnomys Among Philippine murines with known from peninsular India (2N = 36; FN = 36- karyotypes, this particular arrangement is 37; Gadi & Sharma 1983), but this may unique to shrew-rats. The karyotype of only be coincidental since there are no mor- Chrotomys whiteheadi (2N = 38, FN = 52; phological features that link the two genera Fig. 4B) is distinctive within this otherwise
(Wroughton 1912, Rickart et al. 1998). Sev- chromosomally conservative group. It dif- eral species of Mus, including the commen- fers from the 2N = 44 arrangement of Ce- sal M. musculus castaneus (Fig. 3B), also laenomys and the other shrew-rats by three have karyotypes consisting entirely or pre- Robertsonian translocations, involving the dominantly of telocentric elements, with substitution of three submetacentric chro- 484 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WAS GTON mosome pairs for six pairs of telocentric el- ter-species (Steppan et al. in prep.). Al- ements. though closely related, these species exhibit Chromosomal evidence appears to sup- major chromosomal differences. The kar- port monophyly of shrew-rats. Furthermore, yotype of Apomys hylocoetes (2N = 48, FN the distribution of karyotypes among the = 56; Fig. 5B) consists predominantly of four species strongly suggests that the 2N telocentric elements, whereas that of Apo- = 38 karyotype of Chrotomys whiteheadi mys insignis (2N = 36, FN = 72; Fig. 5C) is a novel arrangement derived through cen- is composed entirely of biarmed elements. tric fusion from the 2N = 44 karyotype. These arrangements differ from one another With about 14 species, Apomys is the and from karyotypes of congeners by mul- largest endemic genus of Philippine mu- tiple events, both Robertsonian and non- rines (Heaney et al. 1998). Chromosomally, Robertsonian.
it is also the most variable genus. Karyo- The pattern of chromosomal variation types are available for six species, each of within Apomys provides evidence of a close which is unique (Figs. 5 & 6; Rickart & phylogenetic relationship with the shrew- Musser 1993). Diploid and fundamental rats, as hypothesized by Musser & Heaney numbers range from 30 to 48, and from 50 (1993). In his review of the genus, Musser to 88, respectively, indicating a variety of (1982a) separated Apomys datae from all
chromosomal rearrangements including other Apomys species based on its larger both Robertsonian and non-Robertsonian body size and pattern of cephalic arterial
events. The karyotype of Apomys datae (2N circulation. In both respects, it resembles = 44, FN = 54; Fig. 5A) closely resembles the large shrew-rats (Musser & Heaney that of A. musculus (2N = 42, FN = 52; 1993). Apomys datae also is the most basal Rickart & Musser 1993:6, fig. 3b). Both species in a molecular phylogeny of the ge- have similar diploid and fundamental num- nus (Steppan et al. in prep.). The close sim- bers, include apparently homologous bi- ilarities between the karyotypes of A. datae armed chromosome pairs, and have a pre- (Fig. 5A), A. musculus (Rickart & Musser dominance of telocentric elements. 1993), and the shrew-rats (Fig. 4), suggest Other Apomys species that have been that these arrangements are relatively prim- karyotyped have arrangements that depart itive whereas those of other Apomys rep- significant from those of A. datae and A. resent novel derivations in several different musculus. An undescribed species from directions.
Leyte Island (previously reported as A. lit- Limnomys and Tarsomys, together with toralis) has a karyotype of 2N = 44, FN = Abditomys, Tryphomys and Bullimus, con-
88 (Rickart & Musser 1993:6, fig. 3a). It stitute a group of "new endemic" Philip- differs from A. datae by a series of non- pine genera that share derived moi-pholog- Robertsonian events resulting in an entire ical features with the highly derived genus complement of biarmed chromosomes. In Rattus, and are phylogenetically distinct contrast, the karyotype of an undescribed from other native Philippine murines (Mus- species from Negros Island with 2N = 30, ser & Heaney 1992). Available data dem- FN = 50 (Rickart & Musser 1993:7, fig. 4) onstrate that this assemblage is chromosom- represents a departure in a different direc- ally conservative. Standard karyotypes of tion, involving reduced diploid number and Bullimus and Rattus (Rickart & Musser the loss of some chromosome arms. 1993) and of Limnomys and Tarsomys (Fig. Apomys hylocoetes and A. insignis are 6) have 2N = 42 and show little diversity morphologically similar species that occur in gross chromosome morphology. How-
sympatrically on Mindanao Island (Musser ever, the Y chromosome is variable within
1982a). They have nearly identical cyto- this group. It is by far the smallest element
chrome b sequences, and appear to be sis- in Linmomys (Fig. 6B). but is a substan- VOLUME 1 15, NUMBER 3 485
tially larger telocentric element in both Tar- Archboldomys, Chrotomys, Apomys, and somys (Fig. 6C) and Rattus everetti (Rickart Tarsomys), congeneric species have karyo- & Musser 1993:10, fig. 7B). typic differences in 14 of 16 comparisons. Of the 64 species of murine rodents Of the two cases in which there are no not- known to occur in the Philippines (Heaney ed differences, one {Batomys) involves spe-
et al. 1998), karyotypes are available for 25 cies occurring in different faunal regions. In species in 13 genera (Jotterand-Bellomo & only one case {Limnomys) are species with Schauenberg 1988; Rickart & Musser 1993; similar standard karyotypes found in the this report). These data reveal substantial same faunal region. The geographic pat- chromosomal variation within the entire as- terning of chromosomal variation in mu- semblage, and major differences in the ap- rines resembles the more extensive pattern parent rate of chromosomal evolution with- documented for Philippine bats (Rickart et
in separate genera. Batomys and Crunomys al. 1999). The substantial differences ob- have distinctive yet wholly telocentric kar- served among closely related taxa suggest yotypes, arrangements that have been char- that karyotypic change has been a causal acterized as relatively primitive for murines factor in some speciation events.
(Viegas-Pequignot et al. 1983, 1985; Rick- art & Musser 1993). Phloeomys and Arch- Acknowledgments boldomys are chromosomally distinct from We thank N. Antoque, D. Balete, R. Fer- other murines, and both genera show sub- nandez, G. Gee, S. Goodman, P. Heideman, stantial karyotypic variation at the species J. Klompen, M. Lepiten-Tabao, B. Malaga, level. The chromosomal diversity of Apo- N. Mallari, D. Samson, D. Schmidt, A. Ta- mys is remarkable, and includes major dif- baranza, B. Tabaranza, L. Tag-at, and R. Ut- ferences in the karyotypes of presumed sis- zurrum for assistance in collecting speci- ter-species. mens. E. King assisted with photomicro- The chromosomal data support two of graphs. Permits and logistical support were the major phylogenetic hypotheses posed provided by the Philippine Protected Areas by Musser & Heaney (1992) based on their and Wildlife Bureau and the Philippine Bu- study of comparative morphology: (1) reau of Forest Development. Field work monophyly of the shrew-rat genera Celae- was supported by grants from the National nomys, Chrotomys, and Rhynchomys, and Science Foundation (BSR 8514223), the (2) a close relationship between the Apomys John D. and Catherine T. MacArthur Foun- and the shrew-rats. The data also strongly dation (90-09272A), and the Barbara support clustering of the endemic genera Brown and Ellen Thorne Smith funds of the Bullimus, Limnomys, and Tarsomys with Field Museum. Rattus as a group distinct from other Phil- ippine murines, but they provide no reso- Literature Cited lution within this cluster. Available data are
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been karyotyped {Phloeomys, Batomys, Haiduk, M. W., R. J. Baker, L. V^'. Robbins, & D. A. —
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