Phylogenetic relationships between Indian and Burmese hares

Mammalian Biology
Zeitschrift fuÈr SaÈugetierkunde
www.elsevier-deutschland.de/mammbiol
Original investigation
Phylogenetic relationships between Indian and
Burmese hares (Lepus nigricollis and L. peguensis)
inferred from epigenetic dental characters
By F. SUCHENTRUNK
Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Vienna, Austria
Receipt of Ms. 17. 10. 2001
Acceptance of Ms. 10. 01. 2003
Abstract
Systematic relationships among several forms of hares from South and Southeast Asia currently included in the Indian hare, Lepus nigricollis, and the Burmese hare, L. peguensis, are not well understood. In this study, 29 epigenetic occlusal characters (enamel fold patterns) were analyzed quantitatively to infer phylogenetic relationships among the following operational taxonomic units
(OTU): L. n. nigricollis (n = 29), L. n. singhala (n = 9), L. n. simcoxi (n = 18), L. n. mahadeva
(n = 7), L. n. dayanus (n = 29), L. n. ruficaudatus (n = 52), and L. peguensis (L. p. peguensis,
L. p. siamensis, L. p. vassali, combined n = 25). Pairwise epigenetic distances (C. A. B. SMITH's
MMD) among OTUs were calculated from OTU-specific frequencies of character states. All cluster
analyses performed on the distance matrices revealed close relationships among the OTUs of
L. nigricollis, including rufous-tailed hares, L. n. ruficaudatus, and an only slightly separate status
of Burmese hares, but a distinct separation of both Indian and Burmese hares from woolly hares,
L. oiostolus (n = 27), and Chinese hares, L. sinensis (n = 28), that where used as outgroups. The results conformed the current provisional systematic evaluation, positioning rufous-tailed hares
within Indian hares, but rendering the separate species status of L. peguensis still open.
Key words: Lepus, Indian hare, Burmese hare, teeth, meristic characters
Introduction
Phylogenetic relationships among extant
hares of the genus Lepus from the Indomalayan Region are not well understood and
a revision is overdue (Angermann 1983;
Flux 1983; Flux and Angermann 1990).
All forms from the Indian subcontinent including Nepal, Buthan, and Bangladesh, as
well as from Pakistan, Sri Lanka, Myanmar,
Thailand, Laos, Cambodia, Vietnam, Hainan (China), and western Java appear to
1616-5047/04/69/01-028 $ 30.00/0.
be closely allied, in spite of more or less
conspicuous geographic differences in body
size, ear length, and colouration of fur,
nape, and ears (Angermann 1983; Flux
and Angermann 1990).
Amongst the various forms described earlier as separate species, Flux and Angermann (1990) acknowledged provisionally
the following subspecies of Indian hares,
Lepus nigricollis F. Cuvier, 1823: L. n. nigriMamm. biol. 69 (2004) 1 ´ 28±45
Epigenetic relationships between Indian and Burmese hares
collis, L. n. aryabertensis, L. n. cutchensis,
L. n. dayanus, L. n. joongshaiensis, L. n.
macrotus, L. n. mahadeva, L. n. rajput, L. n.
ruficaudatus, L. n. sadiya, L. n. simcoxi,
L. n. singhala Wroughton, 1915, L. n. tytleri,
and the following three subspecies of Burmese hares, L. peguensis Blyth, 1855:
L. p. peguensis, L. p. siamensis, and L. p.
vassali; however, a valid subspecies description is only available for L. n. singhala
Wroughton, 1915 (see Corbet and Hill
1992). Flux and Angermann (1990) considered provisionally the Hainan hare as separate species (L. hainanus) but, contrary
to McNeeley (1981), hares from western
Java as introduced L. nigricollis (see also
Sody 1939). Corbet and Hill (1992) and
Wilson and Reeder (1993) largely accepted this classification but included
L. hainanus in L. peguensis (see also Nowak 1999).
Nevertheless, Angermann (1983), Flux
(1983), and Flux and Angermann (1990)
emphasized the problematic status of some
of the forms from South and Southeast
Asia. While some may represent separate
species, Burmese hares might be included
in L. nigricollis (cf. Flux and Angermann
1990), or rufous-tailed hares, L. n. ruficaudatus, from the north of the Indian subcontinent might go together with L. peguensis.
Petter (1961) included L. peguensis in
L. nigricollis and suggested to include the
African L. crawshayi (i. e., L. victoriae; c. f.,
Flux and Angermann 1990) in L. nigricollis as well, but considered the rufous-tailed
hare as a separate species, closely related
to L. capensis. To date, not a single comprehensive quantitative morphological analysis
is available to substantiate any of these systematic hypotheses.
In this study, I used occlusal variants (i. e.,
enamel folds, conformation patterns of enamel walls) as epigenetic characters to infer
phylogenetic relationships among several
forms provisionally considered as subspecies of the Indian hare by Flux and Angermann (1990) and between Indian and
Burmes hares. As variation of the studied
dental characters apparently has a strong
phylogenetic background (Suchentrunk
29
and Flux 1996; Suchentrunk et al. 2000),
they should aid in understanding specifically the position of rufous-tailed hares,
L. n. ruficaudatus. This form might either
belong to L. nigricollis as suggested by Angermann (1983), or to L. peguensis, or
might be a separate species (Petter 1961).
Insignificant epigenetic differentiation between the various forms of Indian and Burmese hares would conform the null hypothesis of L. nigricollis (including L. n. ruficaudatus) and L. peguensis being conspecific.
Material and methods
Specimens and geographical ranges of taxa
This study is based on 4 861 teeth (incisors and
cheek teeth) in cleaned skulls and mandibles of
224 specimens of the Indian hare, L. nigricollis,
the Burmese hare, L. peguensis, the woolly hare,
L. oiostolus, and the Chinese hare, L. sinensis.
The latter two species were included to calibrate
the degree of epigenetic differentiation between
forms of L. nigricollis and L. peguensis. As for
L. nigricollis I included only those forms provisionally given subspecific status by Flux and Angermann (1990) of which a minimum of seven
specimens with reliable collection information
was available in diverse museum collections (respective sample sizes are in Tab. 1 and Tab. 3). I
considered all these forms as OTUs (operational
taxonomic units). Specimens of L. peguensis originated mainly from Thailand, i. e., from the
range of L. p. siamensis; only few were from the
presumed or vaguely described ranges of L. p. peguensis, and L. p. vassali. I allocated all specimens
referable to one of the three subspecies of L. peguensis to one combined OTU ªL. peguensisº, because of the lack of clear morphological characteristics and very vague descriptions of the
respective ranges. Several other forms of Indian
hares (see list of provisional subspecies above)
certainly deserve a thorough study, but could not
be included in the present analysis because of no
or too little material with useful information on
sampling location.
I allocated specimens currently included in L. nigricollis to one of the following OTUs: L. n. dayanus, L. n. mahadeva, L. n. nigricollis, L. n. ruficaudatus, L. n. simcoxi, L. n. singhala. Because of
the lack of precise range descriptions and no information on differential diagnostic skull and skin
30
F. SUCHENTRUNK
Table 1. Occlusal characters and dichotomized character states (0/1) used for assessing epigenetic differentiation within and among Indian hares (L. nigricollis) (N), Burmese hares (L. peguensis) (P), woolly hares (L. oiostolus) (O), and Chinese hares (L. sinensis) (S). Frequencies of character state one (1) are given for each species including all studied OTUs, respectively. Individual numbers are in parenthesis; they can be sightly lower for some
characters, due to missing teeth. Character numbers with asterisks denote significant (p < 0.00006, = 0.05 for
SBP) variation of character state frequencies between taxa with same lower chase letter in pairwise comparisons.
Charac- tooth
ter
number
Description of characters and dichotomized character states (0/1)
Frequency of character state 1
c1
P3
Mesial re-entrant fold (filled with cement):
present(1)/absent(0)
c2
P3
Additional mesial re-entrant fold (with cement):
present(1)/absent(0)
2.8
c3
P3
Anterior lingual re-entrant fold (with cement):
present(1)/absent(0)
c4
P3
c5
O (27)
S (28)
96.3
89.3
4.0
11.3
0
1.4
16.0
0
0
Margins of posterior external re-entrant fold forming one extra fold in its most lingual section; additional fold extending mesiad: yes(1)/no(0)
49.0
40.0
5.9
25.0
P3
Both margins of posterior external re-entrant fold
approaching considerably or even touching one
another (usually close to their central section):
yes(1)/no(0)
94.4
92.0
77.8
92.9
c6*
P3
Mesial margin of posterior external re-entrant
fold plicate (plication either strong or slight):
yes(1)/no(0)
30.8a
4.0b
85.2abc
10.7c
c7*
P3
Distal margin of posterior external re-entrant
fold plicate: yes(1)/no(0)
90.1a
88.0b
33.3abc
92.9c
c8*
P3
Distal margin of posterior external re-entrant
fold forming one extra fold in its lateral part:
yes(1)/no(0)
63.4a
28.0
7.4a
50.0
c9
P3
Trigonid with at least one enamel lake:
yes(1)/no(0)
0.7
0
7.4
0
c10
P3
cement layer of mesial re-entrant fold stretching
lingually and covering also anterior lingual re-entrant fold (if present): yes(1)/no(0)
3.5
8.0
0
10.7
c11
P3
margin of anterior external re-entrant angle
shows strong plication (three or more fairly
distinctly developed plicae): yes(1)/no(0)
38.0
44.0
3.7
25.9
c12*
P4
distal margin of lateral re-entrant fold (slightly
or distinctly) plicated: yes(1)/no(0)
95.7a
84.0b
7.7abc
85.7c
c13*
P4
distal margin of lateral re-entrant fold with one
extra fold in its lateral section (occasionally a
dopple fold): yes(1)/no(0)
80.9a
76.0b
3.8abc
50.0c
c14
P4
lingual enamel wall connecting trigonid and
talonid: present (1)/absent (0)
97.8
100
100
100
c15
P4
mesio-lateral enamel wall of trigonid with one
fold (filled with cement): yes(1)/no(0)
2.2
0
0
0
c16*
M1
as c12
c17*
M1
as c13
N (144) P (25)
97.9
93.3ab
a
69.9
100
76.0ac
b
52.0
3.8cd
0
ab
60.7bd
35.7
Epigenetic relationships between Indian and Burmese hares
31
Table 1. (continued)
Charac- tooth
ter
number
Description of characters and dichotomized character states (0/1)
Frequency of character state 1
c18
M1
as c15
0.7
c19*
M2
as c12
88.8ab
68.0c
3.8ac
39.3b
c20*
M2
as c13
72.0ab
48.0c
0ac
28.6b
c21
M2
as c14
99.3
c22
M3
trigonid and talonid connected by a dentine
bridge coated with an enamel layer: yes(1)/no(0)
1.5
c23
M3
distal margin of trigonid: plicated (1)/not
plicated (0)
c24
M3
mesial margin of talonid: plicated (1)/not
plicated (0)
c25
P3
c26
N (144) P (25)
0
0
S (28)
0
100
100
8.0
0
0
3.1
0
0
3.6
3.8
0
0
3.6
distal margin of lingual re-entrant fold
(hypostria) plicated or undualting: yes(1)/no(0)
93.4
96.0
96.2
92.8
P3
distal margin of hypostria with a distinct fold in
lingual section (axis of fold in linguo-buccal
direction or slightly inclined): yes(1)/no(0)
21.6
24.0
15.4
7.1
c27
P4
as c25
82.5
c28
P4
as c26
11.7
12.0
0
0
c29
M1
as c25
82.4
92.0
80.8
96.4
c30
M1
as c26
3.7
c31*
M2
as c25
56.6
c32
M2
as c26
0.8
4.0
0
0
c33
M3
with lingual enamel fold or enamel island (1)/
without lingual enamel fold or island(0)
2.4
0
0
0
c34*
P2
three folds or more(1)/less than three folds (0)
c35*
1
I
complex fold: squarish, bifurcated, or more
complex (3 or more arms) (1)/one simple fold
or groove (0)
characters in the literature, I included four specimens labled as ªL. cutchensisº in L. n. dayanus.
This conforms to the range information for
ªL. dayanusº given by Wroughton (1921). Also,
because of vague range information for single
forms, I included all rufous-tailed hares from the
north of the Indian subcontinent in the OTU
ªL. n. ruficaudatusº, even though some specimens
might have been collected in the presumed ranges
of L. n. macrotus, L. n. aryabertensis, or L. n. tytleri. This grouping conforms to Ellerman and
Morrison-Scott (1951) and Petter (1961), albeit
the latter tended to position ªL. tytleriº somewhat
separate from ªL. ruficaudatusº. I selected only
specimens with reliable information on collection
100a
ab
100
100
O (27)
100
0
36.0a
100
cd
100
96.2
0
30.8b
100
0
85.7ab
66.7a
96.3
0ac
0bd
location/region on specimen lables, but omitted
skulls with loose teeth, or whenever I could not
locate the collection location/region on the map
(concerned mainly specimens collected in the
19th century). Whenever skins were available, I
checked coloration for agreement with collection
localion/region.
The maps in figure 1 show the tentative distributional ranges of the currently studied OTUs of
L. nigricollis together with those of L. peguensis,
L. oiostolus, and L. sinensis. Ranges of OTUs of
L. nigricollis and L. peguensis were based on informations by Dr. R. K. Ghose (Zoological Survey of India, Calcutta ± ZSI), the sampling locations on specimen lables of the studied skulls
32
F. SUCHENTRUNK
Fig. 1. Distributional ranges of the studied operational taxonomic units (OTU) of Inidan hares (Lepus nigricollis)
and of Burmese hares (L. peguensis), Chinese hares (L. sinensis), and woolly hares (L. oiostolus). Informations
used to delineate the ranges are given in Material and methods.
(n = 224), on further 50 specimens that I studied
at the ZSI in 1993 by inspection of skins only (because skulls were not available), as well as on the
following literature: Jerdon (1867, 1874), Sterndale (1884), Blanford (1891, 1901), Sclater
(1891), Lydekker (1900), Forsyth Mayor (1898),
Wroughton (1915, 1921), Glover (1938), Tate
(1947), Petter (1961), Angermann (1965, 1966,
1967, 1983), Ghose (1967, 1971, 1978), Siddiqi
(1969), van Peenen et al. (1969), Tiwari et al.
(1971), Lekagul and McNeely (1977), Roberts
(1977), Lord Medway (1978), Prater (1980),
Ghose (1981), Phillips (1981), Chakraborty
(1983), Wilson and Reeder (1983), Ghose and
Ghosal (1984), Jerdan (sic!) (1984), Flux and
Angermann (1990), Corbet and Hill (1992),
Bergmans (1995), and Shrestha (1997), Jayson
(1999), Manakadan and Rahmani (1999), and
Grassman (2000). The ranges of L. oiostolus and
L. sinensis were taken from Flux and Angermann (1990), Corbet and Hill (1992), and
Zhang et al. (1997).
Epigenetic relationships between Indian and Burmese hares
I took information on the sex from specimen
lables and assigned skulls to the following age
classes: (a) ªjuvenile/subadultº, characterized by
clearly small cranial size, delicate processus supraorbitales with quite smooth edges, and almost
no obliteration of skull sutures (sutura frontalis,
s. saggitalis), (b) ªadultsº, with larger p. supraorbitales with more uneven edges, and partial obliteration of s. frontalis and s. saggitalis. Application
of these criteria, however, was associated with
some ambiguity due to many intermediate skulls.
Because of highly variable skull size, the lack of
information of skull growth in different environments and in hares from different birth seasons,
a large fraction of specimens was left unclassified.
In central European brown hares (L. europaeus),
for instance, patterns of ossification of skull sutures overlap greatly in juvenile, subadult, and
adult hares (Suchentrunk et al. 1991) and skull
size may vary considerably in adult age-known
specimens from a breeding station (Suchentrunk, unpubl. data). I measured condylobasal
length (cbl) of undamaged skulls with a digital
calliper to the nearest 0.1 mm.
All specimens were from one of the following collections: Zoological Survey of India, Calcutta
(ZSI), Natural History Museum London (BMNH),
US National Museum of Natural History, Smithsonian Institution, Washinton D. C., U.S.A.
(USNM), Zool. Museum of the University of
Hamburg, Germany (ZMH), Natur-Museum und
Forschungsinstitut Senckenberg, Frankfurt/M.,
Germany (SMF), Zool. Museum f. Naturkunde of
the Humbold University, Berlin, Germany
(ZMB), National Natuur-historich Museum Leiden, The Netherlands (RMNH), and one specimen
of L. sinensis (without catalogue number) was
from the private collection of Dr. J. E. C. Flux
(Lower Hutt, N.Z.); it is now housed at the National Museum of New Zealand, Wellington. The
respective specimen reference numbers are listed
below: L. n. dayanus: BMNH 8.3.9.19, 25.10.3.3,
25.10.3.4,
64.11.99,
12.10.4.84,
12.10.4.87±
12.10.4.90, 13.8.8.132, 13.8.8.134, 13.8.8.136±
13.8.8.139, 13.9.18.36, 13.9.18.93, 13.9.18.95,
15.11.1.121±15.11.1.124, 91.10.7.147, 91.10.7.150,
USNM 353185, 369012±369015; L. n. mahadeva:
BMNH 12.11.29.126, 12.11.89.127, 12.11.29.138,
12.11.29.184,
12.11.29.185,
12.11.29.189,
12.11.29.190; L. n. nigricollis: BMNH 90495,
9.3.13.5, 15.7.3.67± 15.7.3.69, 19.6.3.77, 19.6.3.78,
13.4.10.62, 13.4.10.63, 13.8.22.86, 12.11.28.123,
12.6.29.128, 12.6.29.130, 91.10.7.154, 30.5.24.235±
30.5.24.238, ZMH 5045±5047, ZSI: 337, 1129,
1480, 1874, 7426, 7437, 18760, 18761; L. n. ruficaudatus: BMNH 12.6.19.3±12.6.19.5, 15.7.2.19,
21.5.1.41, 10.12.2.23, 10.12.2.24, 15.4.3.155±
33
15.4.3.159, 15.4.3.161, 21.8.7.129, 23.11.4.51,
23.11.5.54, 45.1.8.228, 45.1.8.266, 58.6.24.85,
85.8.1.341, 85.8.1.343, 14.7.10.230±14.7.10.233,
91.10.7.152, USNM 290067, SMF 9624, 59123, ZSI
1250, 23249, ZMH: 5024±5044; L. n. simcoxi:
BMNH 12.3.8.3, 12.3.8.4, 12.6.28.43, 12.6.28.44,
11.12.21.34,
12.11.29.181,
12.11.29.182,
12.11.29.188, ZSI 15469, 15508, 15703, 15704 plus
six (a±f) specimens with unsecure numbers;
L. n. singhala: BMNH 77.390, 20.2.8.15, 81.4.29.7,
15.3.1.248, RMNH 33749, ZMB 81516, 81520, ZSI
15499, 15500; L. peguensis: BMNH 0.10.7.21,
3.8.5.17, 3.8.5.19±3.8.5.21, 1.11.8.13, 14.6.18.35,
2.6.6.14±2.6.6.16, 38.9.7.54, 55.16.46, 55.16.47,
8.6.20.10,
15.5.5.241,
9.10.11.26,
91.512.1,
1938.9.7.55, USNM 236614±236617, 240520,
320792, 320793; L. oiostolus: BMNH 20.6.17.1,
20.6.17.2, 99.3.1.20, 11.2.1.246±11.2.1.248, USNM
49495, 49496, 62134, 84073, 84075±84077, 84079,
84080, 198671, 239376, 239874, 239876±239878,
240379, 240380, 255952±255955; L. sinensis:
BMNH 7.7.3.23, 90.7.8.4, 93.6.8.2, 2.6.10.51,
2.6.10.53, 2.6.10.55, 6.12.5.12, 78.4.27.2, 8.11.14.7,
78.11.27.1, USNM 219281, 237772, 239587±
239589, 252159, 252160, 294180, 294182, 294185,
310830±310833, 332902, 339903, 380130.
Occlusal variants and statistical analysis
I studied occlusal variants with a dissecting microscope but did not take into account the variable
thickness of enamel walls. Based on all variants
found, I established 42 mutually exclusive dichotomous (0/1) characters for the epigenetic differentiation analyses (Tab. 1 and 2, Fig. 2). Bilateral
(right/left) and inter-character associations of
character states were tested by Pearson's u coefficients; inter-character associations were based on
right side teeth, and significance of associations
were proved by v2- or Fisher's exact tests. Wilcoxon matched-pair signed rank tests (WMPSR tests)
were performed to distinguish between fluctuating and directional asymmetry in bilateral associations of character states (e. g., Palmer and
Strobeck 1986). OTU-specific frequencies of
character states were based on one skull side
(right) per individual, as were Fisher's exact tests
for sex or age dependence of character states of
single characters. But character states on the left
skull side were considered whenever the corresponding right-side tooth was not available. This
procedure was in agreement with moderately to
highly positive right/left associations of character
states. To account for the high number of tests,
I based significance decisions in test series on
sequential Bonferroni procedures (SBP) with
34
F. SUCHENTRUNK
Table 2. Description of additional occlusal characters found in subspecies of L. nigricollis and L. peguensis. Asterisks denote those included in the MMD analysis of OTUs of L. nigricollis and L. peguensis; the others where excluded from MMD calculations because of their mutual dependence with some other characters.
c36*
P2
central mesial fold (slightly or strongly) plicated: yes(1)/no (0)
c37*
P2
mesial fold lingually of central mesial fold plicated: yes(1)/no(0)
c38*
P2
mesial fold buccally of central mesial fold plicated: yes(1)/no(0)
c39*
I1
labial fold (filled with cement): 3-armed or more than 3 arms (1)/slightly or distinctly bifurcated (0)
c40
P3
posterior lateral re-entrant fold breaking through the lingual enamel wall and separating entirely trigonid and talonid: yes (1)/no (1) (see ANGERMANN 1966)
c41
P3
enamel lake filled with cement between posterior lateral re-entrant fold and
lingual margin: yes (1) /no (0) (see ANGERMANN 1966)
c42
P4
isolated enamel island filled with cement instead of lingual fold: yes (1)/no (0)
= 0.05 (Rice 1989), irrespective of dependence
or independence of data sets.
OTU-specific variation of frequencies of character states was tested pairwise by a series of Fisher's exact tests, separately for the OTUs of L. nigricollis and the four nominal species. Epigenetic
differentiation was assessed by pairwise calculation of C. A. B. Smith's ªmean messure of divergenceª (MMD) and associated standard deviation
(SD) from frequencies of character states with
Anscombe's (1948) transformation. To avoid mutual dependence of some characters, these calculations were performed initially for L. nigricollis,
L. peguensis, L. oiostolus, and L. sinensis, and in
a separate analysis for a slightly altered data set
encompassing the OTUs of L. nigricollis and
L. peguensis only. Because of significant intercharacter associations of character states, characters c16, c17, c19, c28, c29, c30, c31, c38 were not
included in any MMD calculation. The following
28 characters were used for the MMD-calculations among species: c1±c15, c18, c20±c27, c32±
c35 (Tab. 1); and the following 29 characters for
MMD calculations among the OTUs of L. nigricollis and L. peguensis: c1±c15, c18, c20±c27, c32,
c33, c36, c37, c39 (Tab. 1 and 2). Significance of
variation of character state frequencies among
OTUs was not a criterion for selecting characters
for MMD calculations (for rationale see Suchentrunk et al. 1994; Suchentrunk and Flux 1996).
Any MMD value above the associated duplex
SD-value was considered significantly differing
form zero (Sjùvold 1977). The generalized epigenetic relationships among OTUs were revealed by
cluster analyses of MMD values, using the following algorithms of the PHYLIP-package (Felsenstein 1985): UPGMA, Fitch-Margoliash (FM),
and Neighbour Joining (NJ). For UPGMA all ne-
gative MMD values were set to zero and for the
FM and NJ ± analyses they were set to 0.0001.
While the further procedure assumes equal rates
of character evolution in all lineages, the latter
two allow for different rates. Cluster results were
evaluated by bootstrapping (100 replicates) based
on frequencies of characters by a Fortran program developed by R. Willing (Vienna).
Results
The epigenetic occlusal characters created
from the encountered variants of the four
hare species are described in tables 1 and 2
and respective frequencies of character
state appear in tables 1 and 3. Some further
occasional variants (c 38, c40±c42), that
were not used for the epigenetic analyses
because of mutual dependence with other
characters, are listed in table 2. Frequencies
of character state 1 of characters used for
the MMD-matrix of L. nigricollis OTUs
and L. peguensis are listed in table 3. While
there were only two significant differences
in character state frequencies between
OTUs of L. nigricollis or between OTUs of
L. nigricollis and L. peguensis (Tab. 3), frequencies of character states of 12 characters
differed significantly between species
(Tab. 1), and an additional twelve Fisher's
exact tests (results not shown) yielded tendencies (p £ 0.005) for differences between
OTUs of L. nigricollis or between single
OTUs of L. nigricollis and L. peguenesis.
Epigenetic relationships between Indian and Burmese hares
35
36
F. SUCHENTRUNK
Table 3. Relative frequencies (%) of character state 1 of occlusal characters of OTUs of L. nigricollis and L. peguensis (scores of right teeth; left tooth scores whenever right tooth was missing). NIG = L. n. nigricollis,
SIN = L. n. singhala, SIM = L. n. simcoxi, MAH = L. n. mahadeva, DAY = L. n. dayanus, RUF = L. n. ruficaudatus. Individual numbers in parentheses. Character number with asterisk denotes significant (p < 0.00006, = 0.05 for
SBP) variation of character state frequencies between taxa with same lower chase letter in pairwise comparisons.
Character number,
tooth
Lepus nigricollis
NIG
(29)
SIN
(9)
SIM
(18)
MAH
(7)
DAY
(29)
100
100
100
100
c1
P3
96.6
c2
P3
0.0
c3
P3
0.0
0.0
0.0
0.0
c4
P3
51.7
77.8
76.5
14.3
c5
P3
96.6
88.9
c6
P3
17.2
33.3
c7
P3
92.9
88.9
c8
P3
71.4
66.7
c9
P3
0.0
0.0
c10
P3
3.6
c11
P3
39.3
c12
P4
93.1
c13
P4
89.3
75.0
c14
P4
93.1
87.5
0.0
0.0
100
100
3.4
96.2
(25)
100
3.8
4.0
0.0
3.8
16.0
44.8
40.4
40.0
89.7
94.2
92.0
0.0
24.1
44.2
4.0
85.7
79.3
92.3
88.0
70.6
57.1
51.7
63.5
28.0
0.0
0.0
3.4
0.0
0.0
11.1
5.9
0.0
3.4
1.9
8.0
22.2
35.3
57.1
27.6
44.2
44.0
85.7
92.9
98.0
84.0
100
35.3
14.3
RUF
(52)
Lepus
peguensis
100
100
93.8
100
71.4
100
78.6
100
75.6
100
76.0
100
c15
P4
3.4
0.0
5.9
0.0
0.0
2.0
c18
M1
0.0
0.0
0.0
0.0
0.0
2.0
0.0
c20
M2
79.3
71.4
88.2
57.1
84.6
56.5
48.0
0.0
c21
M2
c22
M3
3.6
0.0
0.0
0.0
3.6
0.0
8.0
c23
M3
3.6
0.0
0.0
0.0
7.4
2.1
0.0
c24
M3
3.6
0.0
6.3
0.0
7.4
2.1
0.0
c25
P3
96.6
50.0
94.1
92.6
96.1
96.0
c26
P3
20.7
50.0
29.4
14.3
25.9
16.0
c27*
P4
72.4
71.4
47.1ab
85.7
92.6
96.0a
c32
M2
0.0
0.0
0.0
0.0
0.0
2.0
c33
M3
0.0
0.0
0.0
0.0
0.0
6.1
0.0
c36
P2
32.1
50.0
47.1
28.6
31.0
39.2
32.0
c37
P2
25.9
25.0
35.3
14.3
23.1
27.5
28.0
c39
I1
25.0
14.3
25.0
14.3
17.9
33.1
66.7
100
100
100
85.7
100
100
100
100
24.0
100b
4.0
b
Fig. 2. Non-metric occlusal characters used in the epigenetic analyses. Numbers correspond to characters in tables 1 and 2. Thickness of enamel walls not considered. White areas = dentine, stippled areas = cement. I1 nomenclature according to conventional numeration. b = buccal, m = mesial, l = labial.
Epigenetic relationships between Indian and Burmese hares
There were no age class or sex-related differences of frequencies of character states,
when tested separately for each species.
Also, cbl values did not differ significantly
between character states, indicating independence of character states from skull size
(length). But significant (p < 0.0001) positive bilateral (right/left) associations of
character states of single characters with ucoefficients ranging between +0.44 and
+1.0 occcurred in 72.6% of all v2- or Fisher's exact tests (n = 69), when based on
SBP. Additional 18.9% of the tests yielded
a tendency (0.0001 < p < 0.007) for positive
right/left associations (+0.519 < u < +0.692);
and only 8.5% of the tests did not reveal a
significant positive association or such a
tendency. WMPSR tests (results not shown)
revealed fluctuating asymmetry (FA) of
character states of all characters. Significant
inter-character associations and tendencies
37
for such associations were found for twenty
pairs of characters, with u-coefficients ranging between ±0.449 and +0.899.
Pairwise MMD calculations for the four
species L. nigricollis, L. peguensis, L. oiostolus, and L. sinensis were based only on
the statistically independent characters.
The set of characters for MMD calculations
between the four species differed slightly
from that used for the OTUs of L. nigricollis and L. peguensis, to provide mutual independence of characters for the MMD calculations (comp. Tab. 1 and 2). While all
pairwise MMD values between species
were significantly higher than zero (Tab. 4),
only four pairwise MMD values varied significantly between OTUs of L. nigricollis
and L. peguensis (Tab. 5). In all cluster analysis, L. nigricollis and L. peguensis clustered together (see Fig. 3 for the UPGMA
and bootstrap values; NJ and FM dendro-
Table 4. Epigenetic differentiation among hare species from central, southern and south-eastern Asia based on
28 occlusal characters. MMD values above and associated SD values below diagonal. Asterisks denonte significant
MMD values. For characters see Tab. 1 (c16, c17, c19, c28, c29, c30, c31 not used for MMD calculation ± see
text).
(1)
(2)
(3)
(4)
L. nigricollis (1)
±
0.0469*
0.8909*
0.3437*
L. peguensis (2)
0.0126
±
0.7323*
0.2560*
L. oiostolus (3)
0.0120
0.0200
±
0.3723*
L. sinensis (4)
0.0114
0.0194
0.0189
±
Table 5. Pairwise MMD-values for subspecies of L. nigricollis and L. peguensis based on 29 epigenetic dental
characters. MMD-values are given above and associated SD-values below the diagonal. nig = L. n. nigricollis,
sin = L. n. singhala, sim = L. n. simcoxi, mah = L. n. mahadeva, day = L. n. dayanus, ruf = L. n. ruficaudatus,
peg = L. peguensis. Asterisks denote MMD values significantly greater than zero.
nig
sin
sim
mah
day
ruf
peg
nig
±
±0.0516
±0.0466
±0.0717
±0.0270
0.0079
sin
0.0445
±
±0.0429
±0.1160
±0.0631
±0.0142
0.0494
sim
0.0243
0.0504
±
0.0135
0.0126
0.0389
0.1433*
mah
0.0441
0.0701
0.0501
±
±0.0739
±0.0472
day
0.0184
0.0447
0.0244
0.0443
±
0.0010
0.0413*
ruf
0.0143
0.0406
0.0203
0.0402
0.0145
±
0.0504*
peg
0.0196
0.0458
0.0256
0.0455
0.0198
0.0156
±
0.0625*
±0.0559
38
F. SUCHENTRUNK
grams not shown). The UPGMA dendrogram (Fig. 4) revealed epigenetic separation
of L. peguensis from all studied OTUs of
L. nigricollis, and this was confirmed by essentially same topologies of the NJ and
FM-dendrograms (not shown). However,
all bootstrap values were rather low (see
Fig. 5 for a 50% consensus tree), and the divergence between L. peguensis and the
OTUs of L. nigricollis was mainly due to
different character state frequencies of the
first upper incisor (I1). The labial fold of
the I1 was more complex in L. peguensis
than in the OTUs of L. nigricollis (Tab. 6),
but most other character state frequencies
used for MMD-calculations did not differ
much between L. nigricollis and L. peguensis (Tab. 3 and 6). Moreover, frequencies of
plicated margins of the folds of the P2
(Tab. 7) did also not vary significantly.
While all studied specimens of L. peguensis
and 99.3% of L. nigricollis had more or less
distinctly developed labially inclined abrasion areas of the I1 (as described by Flux
and Flux 1983 and Angermann and Feiler
1988 for hares from Africa), only 36% of
woolly hares and none of the Chinese hares
exhibited such bevelled I1.
Fig. 3. UPGMA-dendrogram of epigenetic relationships among the four studied Lepus species and bootstrap values (100 replicates, L. oiostolus was defined as outgroup). Scale gives MMD-values.
Fig. 4. UPGMA-dendrogram of epigenetic relationships among the studied OTUs of Lepus nigricollis and L. peguensis based on MMD-values from 29 characters. Scale gives MMD-values.
Epigenetic relationships between Indian and Burmese hares
39
Fig. 5. 50% consensus tree of OTUs of L. nigricollis, L. peguensis, and L. oiostolus as calculated from pairwise
MMD values based on 29 characters. Bootstrap support is given for each node (L. oiostolus was defined as outgroup).
Table 6. Frequencies (%) of character states of fold of I1 in OTUs of L. nigricollis and L. peguensis. nig = L. n. nigricollis, sin = L. n. singhala, sim = L. n. simcoxi, mah = L. n. mahadeva, day = L. n. dayanus, ruf = L. n. ruficaudatus, L. peg = L. peguensis. Sample sizes are given in parentheses.
character state
nig
(24)
slightly bifurcated
sin
(7)
sim
(16)
mah
(7)
day
(28)
ruf
(52)
L. peg
(24)
4.2
0
12.5
14.3
21.4
5.8
0
distinctly bifurcated
70.8
85.7
62.5
71.4
60.7
67.3
33.3
3-armed
16.7
14.3
18.8
0
14.3
17.3
50.0
8.3
0
6.3
14.3
3.6
9.6
16.7
> 3-armed
Table 7. Frequencies (%) of plication of central fold (CF), lateral fold (LAF), and lingual fold (LIF) of P2 in OTUs
of L. nigricollis, L. peguensis, L. oiostolus, and L. sinensis. nig = L. n. nigricollis, sin = L. n. singhala, sim = L. n.
simcoxi, mah = L. n. mahadeva, day = L. n. dayanus, ruf = L. n. ruficaudatus, L. peg = L. peguensis, L. oio = L. oiostolus, L. sin = L. sinensis. Sample sizes are given in parentheses.
nig
sin
sim
mah
day
ruf
L. peg
L. oio
CF
32.1 (28) 50.0 (8)
plicated
47.1 (17) 28.6 (7)
31.0 (25) 39.2 (51) 32.0 (25)
LAF 25.0 (28) 12.5 (8)
plicated
29.4 (17) 57.1 (7)
20.7 (24) 21.6 (51) 24.0 (25) 11.1 (18)
LIF
25.9 (27) 25.0 (8)
plicated
35.3 (17) 14.3 (7)
23.1 (29) 27.5 (51) 29.2 (24)
L. sin
4.3 (23) 55.6 (27)
7.7 (26)
4.8 (21) 37.0 (27)
40
F. SUCHENTRUNK
Discussion
In Leporids, occlusal traits have traditionally been used for phylogenetic inferences
(e. g., Forsyth Major 1898; Petter 1959;
Hibbard 1963; Palacios and LoÂpez 1980;
Corbet 1983; Miller and Carranza-CastanÄeda 1982; Erbaeva and Angermann
1983). They refer to presence or absence of
enamel folds or notches, enamel islands,
conformation patterns of grooves, filling of
grooves with cement, and the extent of enamel wall plication. Although currently
scored in a binary mode, they can be considered quasi-continuous, quantitative-genetic characters with both genetic and environmental causation (e. g., Berry 1963;
GruÈneberg 1965; Lande 1981, Suchentrunk et al. 1994; and generally Lynch and
Walsh 1998) and have been used earlier to
distinguish extant and fossil Leporid species, to reveal their phylogenetic relationships, as well as in population genetic and
ecological-genetic contexts (e. g., Forsyth
Major 1898; Petter 1959, 1961; Hibbard
1963; Angermann 1965, 1966; Palacios
and LoÂpez 1980; Erbaeva and Angermann
1986; Robinson 1986; Suchentrunk 1993;
Suchentrunk et al. 1994; Suchentrunk
and Flux 1996; Palacios 1996; Suchentrunk 2000; Suchentrunk et al. 2000;
Alves et al. 2001).
The high intraspecific variability of occlusal
characters (e. g., Angermann 1965; Petter
1959, 1961; Suchentrunk et al. 1994) recommends a quantitative (ªepigeneticº) approach for phylogenetic inferences (for general aspects see e. g., Sjùvold 1977). In this
context epigenetic characters are particularly valuable, if environmental factors have
only a minor influence on their variability
(phylogenetic character variability; see
e. g., Thorpe et al. 1991). Information on
hereditary properties and possible selective
factors of variation of the studied traits are
not available, but studies on hares from
Kenya and Israel indicate phylogenetic
rather than ecogenetic causation of character variability (Suchentrunk and Flux
1996; Suchentrunk et al. 2000). Possible
functional morphological constraints to
character variability should produce certain
(coadapted) character patterns of occlusal
variants and could thus reduce the reliability of phylogenetic or population genetic inferences made from these traits. In the present study, however, significant intercharacter associations of character states
were primarily revealed between characters
of different teeth and not within single
teeth, suggesting common underlying genetic backgrounds for respective characters
of different teeth (ªmorphogenetic fieldsº),
rather than functional contraints within single teeth. The generally low level of fluctuating asymmetry (FA) of all characters studied presently complies with findings of
occlusal FA in Israeli hares (Suchentrunk
2000), Iberian hares (L. granatensis) from a
local population in Portugal (Alves et al.
2001), and cape hares (L. capensis) from
different environments in Kenya (Suchentrunk and Flux, unpubl. data). It suggests
high developmental stability (e. g., Mùller
and Swaddle 1997) of these dental characters in different evolutionary lineages of
hares and under varying environmental
conditions. Although a certain allelic component on intra-individual variability of
character states cannot be entirely excluded
(phenetic-genetic correlation; e. g., Schnell
and Selander 1981, see also Suchentrunk
1993), I refrained from basing frequencies
of character states for calculation of epigenetic divergence on both body sides, as
suggested by some authors (e. g., Ossenberg 1981), in order to ensure statistical
independence of character states. Furthermore, because FA is characterized by bilateral deviations from regular development
with equal chances for both body sides,
character states scored on one body side represent already the statistically meaningful
data set.
All currently studied OTUs of Indian hares
are closely related, as implicated by low
pairwise MMD values (statistically not different from zero). Contrary, significant
MMD values for most pairs of OTUs of Indian hares and the Burmese hares indicate
a somewhat separate position of L. peguensis from all studied OTUs of L. nigricollis.
Epigenetic relationships between Indian and Burmese hares
Rufous-tailed hares (L. n. ruficaudatus),
that have been considered or suspected a
separate species (Petter 1961, see also
Flux and Angermann 1990), or where tentatively included in L. peguensis, are closely
associated epigenetically with all other
OTUs of Indian hares. This finding substantiates the provisional systematic evaluation by Angermann (1983), Flux and Angermann (1990), Corbet and Hill (1992)
(see also Wilson and Reeder 1993; Novak
1999). On the other hand, the epigenetic divergence between the OTUs of L. nigricollis and L. peguensis is only marginally
greater than between several pairs of OTUs
within L. nigricollis, when compared to
pairwise epigenetic distances involving
L. sinensis or L. oiostolus. In fact there is
no single epigenetic character that distinctly
seprates L. peguensis from L. n. ruficaudatus. Rather, differences of frequencies of
some character states appear to be merely
gradual.
Apart from the occlusal characters used in
the epigenetic differentiation analyses, all
Indian and Burmese hares share another
dental feature, namely an inclined abrasion
area in the labial part (anterior face) of the
I1. This was also described for L. victoriae
(syn. L. crawshayi, syn. L. whytei) from
Kenya and West Africa (Flux and Flux
1983; Angermann and Feiler 1988). While
this characteristic abrasion pattern was currently present in almost all (99.3%) specimens of L. nigricollis and in all L. peguensis
specimens, it occurred in only 36% of
L. oiostolus and in no specimen of L. sinensis. But I also found it, to varying degrees,
in several Lepus species from the New
World, in one specimen of L. mandshuricus
from northeast China, and in one specimen
of Korean hares, L. coreanus (unpubl.
data). In L. nigricollis it appears to be produced by specific chewing movements already very early in ontogeny, because I
found slightly bevelled I1 in a neonate or
very young skull from Nepal. Bevelled I1
were also always present in L. n. dayanus,
despite some of the skulls of this taxon resembled very much those of L. capensis.
Only one skull (cbl = 77.0 mm) of all stu-
41
died L. n. dayanus had only slightly bevelled I1. While frequencies of plication of
the central, lateral, and lingual folds of first
upper cheek teeth (P2) did not vary significantly between L. peguensis and OTUs of
Indian hares, the labial fold of the I1 appeard to have the highest complexity in
L. peguensis (see also Forsyth Major
1898), possibly indicating clinal variation
among Indian and Burmese hares. Robinson (1986) mentioned a clinal trend for the
complexity of I1 patterns in L. saxatilis from
southern Africa. Apart from only gradually
changing patterns of the I1 fold and of other
teeth, the presence of bevelled I1 in almost
all individuals of L. nigricollis and L. peguensis might stress their close relationship.
Indeed, both rufous-tailed hares from the
north of the Indian subcontinent and Burmese hares are very similar in external appearence. The only striking coat difference
concerns the dorsal face of the tail which is
rufous-brown in the further and black in
the latter hares. Variation of nape, tail, and
general coat coloration is clearly greater
among the epigenetically closely related
OTUs of Indian hares than between rufous-tailed and Burmese hares: Indian hares
from Sri Lanka, south, and south-central India have black or dark brown napes and a
black upper face of the tail; napes are
smoke-grey or ash-brown in L. n. simcoxi,
grey with buffy suffusions in L. n. mahadeva, sandy-grey in the generally paler
L. n. dayanus from the arid regions of
north-west India and Pakistan, and rufousbrown or ochraceous in the rufous-tailed
hares from northern India, Nepal, Buthan,
and Bangladesh. The colour of the upper
face of the tail varies also among the OTUs
of L. nigricollis from black to dusty grey or
rufous brown. In the face of this colouration
variation within L. nigricollis and the present epigenetic results, Indian and Burmese
hares might indeed be conspecific with a
somewhat increased gene pool separation
of L. peguensis. Alternatively, L. nigricollis
and L. peguensis could represent a tightly
connected pair of very young species. Basically, this conforms the current systematic
view (Angermann and Flux 1990; see also
42
F. SUCHENTRUNK
Wilson and Reeder 1993). The present epigenetic results, however, are more in favour
of the hypothesis of conspecificity of L. nigricollis and L. peguensis, rather than a
separate species status of each taxon. Considering the emerging complexity of evolutionary patterns in the genus Lepus, with
the possibility of introgressive hybridization
in natural populations of phylogenetically
well separated species (Alves et al. 2003;
see also Thulin and TegelstroÈm 2002), a
comprehensive assessment of relationships
among hares from South and Southeast
Asia deserves molecular studies with emphasis on gene flow patterns in the contact
zones of the diverse forms.
Acknowledgements
I thank Dr. R. K. Ghose (Zoological Survey of
India, Calcutta ± ZSI) for informations and discussions on ranges and systematics of the hares
from India and for the allowance to study the material at the ZSI, as well as Mrs. Linda Gordon,
Mr. R. Fisher (Smithsonian Institution, Washington D. C.), Mrs. Paula Jenkins (British Museum
of Natural History, London), Prof. H. Schliemann (Zool. Museum, University of Hamburg),
Dr. Renate Angermann (Zoological Museum of
the Humboldt University, Berlin), Dr. G. Storch
(Senckenberg Museum, Frankfurt/M.), Dr.
Ch. Smeenk (Rijksmuseum Leiden, The Nether-
lands) for the agreement to study the specimens
in the collections under their care. Dr. Friederike
Spitzenberger (Natural History Museum Vienna,
Austria) provided access to the rich library of the
mammals collection, and Dr. J. E. C. Flux (Lower Hutt, New Zealand) encouraged me to study
Asian hares and supplied literature. DI R. Willing (Vienna) developed the Fortran program
for bootstrapping MMD-cluster analyses. Dr.
F. Frey-Roos (Vienna) helped with French translations and Mr. A. KoÈrber (Vienna) assisted with
graphical work.
Zusammenfassung
Phylogenetische Beziehungen zwischen indischen Hasen und burmesischen Hasen (Lepus
nigricollis und L. peguensis) anhand epigenetischer Zahnmerkmale
Die Hasen (Genus Lepus) des suÈd- und suÈdostasiatischen Festlandes werden ± abgesehen von L. capensis, L. comus, L. oiostolus und L. sinensis ± provisorisch zu zwei Arten zusammengefaût; zu den
indischen Hasen (L. nigricollis) und den burmesischen Hasen (L. peguensis). Innerhalb der ersteren
Art werden provisorisch 13 und innerhalb der letzteren Art drei Subspecies unterschieden. Einzelne
Formen von L. nigricollis koÈnnten eigene Arten darstellen, zu L. peguensis oder auch zu L. capensis
gehoÈren. L. nigricollis und L. peguensis koÈnnten auch Vertreter einer Art sein. Quantitative morphologische Analysen fehlen, um die einzelnen Hypothesen zu stuÈtzen. In dieser Untersuchung wurden
die Frequenzen von 29 non-metrischen Merkmalen der ZahnoberflaÈchen indischer und burmesischer
Hasen zur Berechnung ¹epigenetischer Distanzenº (C.A.B: SMITH's MMD ± ¹Mean Measure of Divergenceº) zwischen folgenden ¹operationalen taxonomischen Einheitenº (OTU) herangezogen:
L. n. dayanus (n = 29), L. n. mahadeva (n = 7), L. n. nigricollis (n = 29), L. n. simcoxi (n = 18),
L. n. singhala (n = 9), L. n. ruficaudatus (n = 52), und L. peguensis (n = 25). Verschiedene ClusterAnalysen der paarweisen MMD-Werte ergaben unter Einbeziehung von L. oiostolus (n = 27) und
L. sinensis (n = 28) eine sehr enge Beziehung zwischen den OTUs von L. nigricollis und L. peguensis.
Dies spricht fuÈr die ZugehoÈrigkeit aller untersuchter OTUs zu L. nigricollis und stuÈtzt die Ansicht,
daû L. nigricollis und L. peguensis konspezifisch seien.
Epigenetic relationships between Indian and Burmese hares
43
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Author's address: Franz Suchentrunk, Research
Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Savoyenstrasse 1, A-1160
Vienna, Austria
(e-mail: [email protected])