zoological Journal of !he Linnean SocieQ (1994), I l l : 161-178. With 9 figures
A cladistic analysis of Hydrophis subgenus
Chitulia (McDowell, 1972) (Serpentes,
Hydrophiidae)
ARNE REDSTED RASMUSSEN
zoological Museum, Universip of Copenhagen, Universitetsparken 15, D X 2100
Copenhagen, Denmark
Receiued March 1993, accepted f o r publzcoltorr Au@~rl1993
The Hydrophis subgenus Chitulia was analysed using the computer program Hennig86 (version I .5).
T h r character data set comprises 22 two-state charactrrs, giving a minimum of 22 steps. Four trees
with a length of 37 steps and a consistency index of 0.59 werr found using the “ie*” option. The
results indicate that the subgenus Chitulia is paraphyletie, and that the group has been based solely
on plesiomorphic character states. The order of taxa input, the display of the root, and the effect of
unknown character states using Hennig86 are commented on.
ADDITIONAL KEY WORDS:
22 morphological charartrr
-
Hennig86 Paraphyletir subgenus.
CONTENTS
Introduction . . . . .
. . .
Material and methods
. . . . .
Construction of the data matrix . .
.
Choice ofoutgroup . .
. . .
Character description
. . . .
Chararters not used in the analysis
.
Results .
. . . . . . . .
Evaluation of the cladograms . . .
Evaluation of tree I .
.
. . .
Consensus tree . .
. . . .
Outgroup
. . . . . . .
Evaluation ofcharacters . .
. .
Test of McDowell’s (1972) hypothesis
Remarks concerning the use of Hrnnig86
Discussion
. . . . . . . .
Phylogeny and taxonomy
. . .
Biogeography
. . . . . .
Acknowledgements . . .
. . .
References
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INTRODUCTION
The genus Hydrophis is a major component of the sea snake fauna and
comprises about 28 species (Rasmussen, 1992). However, the phylogeny and
biology of this genus remain poorly known, especially compared to information
on, e.g. terrestrial elapid and viperid groups.
0024-4082/94/06961+ 18 $08.00/0
161
0 1994 ‘I’hr Linncan
Society of‘ London
I62
A. R. RASMUSSEN
T h e most recent comprehensive monograph which treats the genus Hydrophis
was published by Smith (1926). However, in 1972 McDowell proposed to divide
the genus Hydrophis into three subgenera: Hydrophis, I,eioselasma, and Chilulia
(formerly Aturia (see Williams & Wallach, 1989)). ‘lwo years later, the genus
ljisteira sensu McDowell was included in Hydrophis as an additional subgenus by
Burger & Natsuno (1974). Cogger (1975) adopted Smith’s (1926) classification;
however, he also considered McDowell’s subgeneric assignmcnts within Hydrophi.$
to be a natural one. Neither Cogger (1975) nor Voris (1977) included Disleirn in
the genus Hydrophis, nor did they accept Disteira as redefined by McDowell.
Based on immuriological evidence, Cadle & Gorman ( 198 1 ) concluded that all
available data indicated that the diversification of the Hydrophis group is
relatively recent, and that the genus Hydrophis is paraphyletic. Tn 1984 Kharin
proposed that the three subgenera created by McDowell bc raised to the generic
level. McDowell’s classification was also questioned by Young (1987), on the
grounds that functional morphological criteria had not bccn 11tilized.
The purpose of the present study is to clarify whether or not the subgenus
Chilulia is a monophyletic group within the genus Hydrophis, as suggested by
McDowell ( 1972).
MAIERIAI, A N D METHODS
Unless otherwise mentioned, all skulls, as well as the bodics (in alcohol) from
which the skulls were taken, are deposited in the collection of Zoological
Museum, University of Copenhagen ( Z M U C ) .
T h e outgroup taxa consist of the following species; NoLechis scutatus (Peters,
1861), one skull from Australia, without precise locality. Psezidonnja textilis
(Dumeril, Bibron & Dumeril, 1854),one skull from Victoria, Australia. ilipysurus
eydouxi (Gray, 1849), two skulls from Samut Sakhon, Thailand.
‘lhe following ingroup taxa consist of all the species included in McDowcll’s
(1972) subgenus Chitulia, except H. inornalus (Gray, 1849) as material was not
available, together with two species from the subgenus Leioselnsrna, two specics
from the subgenus Hydrophis, and H. lamberh resurrected by Rasmusscn (1989);
the names in parentheses indicate McDowell’s ( 1972) subgeneric assignmcnts:
H . (Hydrophis) brookii Ciinther, 1872, one skull from Satun, west coast of
peninsular Thailand. H. ( H . ) fascialus (Schneider, 1979), four skulls from Phukct
Port, Phuket Island, west coast of peninsular Thailand. H . (Leioselasrna)
yanocinclus Daudin, 1803, four skulls from Phuket Port, and one skull from
Samut Sakhon, Gulf of Thailand. H. ( L . ) spiralis (Shaw, 1802), six skulls from
Phuket Port. H. (Chitulia) befcheri (Gray, 1849), four skulls from Samut Sakhon.
H. (C.) bihdwculnlus Peters, 1872, two skulls from Phuket Port. H. (C.)
caerulescens (Shaw, 1802), one skull from Phuket Port, one skull from about
1.5 km off the coast 5 km north of Chittagong, Bangladesh. H . (C.) lamberli
Smith, 1917, two skulls from Samut Sakhon. H. (C.) lapernoides (Gray, 1849),
seven skulls from Phuket Port, five skulls from the Persian Gulf, about 100 km
north northeast of Bahrain. H . (C.) mamilluris (Daudin, 1803), one skull from
British Museum (Natural History) (from the collection of M. Smith, without
locality). H. (C.) ornalus (Gray, 1842), six skulls from Phuket Port and two skulls
from Bahrain. H. (C.) striclicollzs Gunther, 1864, five skulls from Chittagong. H.
(C.) lorpalus Gunther, 1864, one skull from T h e Gulf of Thailand. Data
AN ANALYSIS OF SUBGENUS CHITULIA
163
TABLE1. Character matrix for outgroups (marked by *) and
Hydrophis spp. Unknown character states indicated by ?
1
Character nos.
0. Notechis scuta1u.r
*
I . Pseudonaja textilis *
2. Aipysurus ydouxi *
3. H. (Hydrophis) brookit
4. H. ( H . ) farciatus
5. H. (Leioselasma) vanocinctus
6. H. (I,.) spiralis
7. H. (Chitulia) belcheri
8. H. (C.) bituberculatus
9. H. ( C . ) caerulesren~
10. H. (C.) lamberti
II. H . (C.) lapemoides
12. H. (C.) mamillaris
13. H. ( C ) . ornatus
14. H. (C.) striclicollis
15. H. (C.) lorquatus
0
5
0
00000
00000
00000
00000
0000 I
01 100
0000 1
00 100
10010
11110
11110
11111
11111
11110
11110
11110
11110
11110
IIII?
11110
11110
11111
1
5
10000
01100
00000 00000
11110 11110
0 1000 11111 11110
11111
1 I100 11110
11111
11100 11110
I 1000 11100 11110
I 1000 11100 11110
11110 1 1 100 00100
11110 11100 00001
I1100 I 1 100 00100
I1??0 1?100 10100
11100 1 1 100 00001
I I100 11110 11100
11111 11110 11110
2
0
00
00
01
11
I1
01
01
00
00
01
00
00
00
00
01
01
concerning external characters have been taken from Cogger ( 1986), Rasmussen
(1989, 1992, 1993) and Smith (1926).
The only species for which all characters could not be scored in the data
matrix (Table 1 ) was H. mamillaris; the four characters concerned have been
scored with a question mark. T h e character data set comprises 22 two-state
characters, ideally giving a minimum of 22 steps.
The data set was analysed using the computer program Hennig86 (version
1.5) (Farris, 1988). Trees were initially calculated using the ‘ie*’ option (implicit
enumeration; the program retains all the equally most parsimonious solutions)
with outgroup = taxa 0-2 (note that the numbering of both taxa and characters
starts with 0 in Hennig86). The tree editor ‘DOSEquis’ (which displays a tree,
including the states of its nodes, and provides facilities for interactively modifying
the tree and characters coding), was used to modify the cladograms and to test
the relationships proposed by McDowell (1972). ‘xsteps h’ (which lists possible
states for hypothetical ancestors) was applied for each of the trees. By alternately
using the ‘xsteps w’ (which sets character weights from 0 to 10 according to fits)
and Ye*’, successive character weighting was applied to the cladograms until no
changes occurred in the weights assigned. Finally, the option ‘nelsen’ was
applied to obtain a consensus tree.
CONSTRUCTION OF THE DATA MATRIX
Choice of outgroup
In this study, the character polarization has been based on an outgroup
comparison (Maddison et al., 1984). T h e outgroup is composed of two terrestrial
Australian elapids, Notechis scutatus and Pseudonaja textilis together with the sea
snake Aipysurus eydouxi. This outgroup has been selected on immunological
evidence, indicating that Hydrophis evolved relatively recently from Australian
terrestrial elapids (Cadle & Gorman, 1981; Schwaner et al., 1985). T h e
I64
A. R. RASMUSSEN
relationships within the outgroup are treated as uncertain, as it is still doubtful
whether Aipysurus and Hydrophis have an independent common origin among the
elapids (Voris, 1977; Cadle & Gorman, 1981). For a further discussion of
outgroup analysis and parsimony, see Maddison et al. (1984).
Character description
This analysis is based primarily on skull characters because many of the more
widely used characters in ophidian taxonomy (e.g. scale count) exhibit great
s . 22 characters used in this
intraspecific variation in the genus ~ y ~ r # p h i The
analysis are described below and a polarization of each state on the basis of
outgroup comparison is proposed. When the character transformation is
ambiguous an apomorphic condition is suggested.
0. Internasal scales: presence (state 0 ) , absence (state 1). State 0 occurs in
N . scutatus and P. textilis, state 1 occurs in A . eydouxi. Based on the outgroup i t is
not certain which condition is derived, but state 1 is here considered apomorphic
following Marx & Rabb (1972) and McCarthy (1986).
1. Ventral scaleslvertebrae relationships: correspondence ( 1 : 1 ) (state 0), no
correspondence (state 1). State 0 is found in all three species of the outgroup;
state 1 is therefore considered to be the apomorphic condition.
2. Number qf scale rows on body: 22 or fewer (state 0), more than 22 (state 1 ) . As
state 0 is found in all three species of the outgroup, state 1 is taken as an
apomorphic condition, in accordance with Marx & Rabb (19721, McCarthy
(1986), and Voris ( 1977).
3. Tail shape: round (state 0 ) , flat (state 1). State 0 is found in N . scutatus, arid
P. textilis, state 1 is found in A . eydouxi. Based on the outgroup it is uncertain
which is the apomorphic state; however, state 1 is considered to be the
apornorphic condition, which is in accordance with McCarthy (1986).
4 . Ratio between maximum length and maximum width of parietal bone: length less than
1.5 times the width (state 0), length more than 1.5 times the width (state I ) .
State 0 occurs in all three species of the outgroup, indicating that state 1 is the
apomorphic condition.
5. Dorsal parietal crest (midline) (Fig. 1): without a distinct crest (state 0), with a
distinct crest (state 1 ) . State 0 is seen in all three species of the outgroup; state 1
is probably the apomorphic condition, which is in accordance with McCarthy
( 1986).
6. Anterolateral process of parietal (Fig. 1): without process (state 0), with process
(state 1 ) . State 0 can be seen in all three species of the outgroup; state 1 thus
considered the apomorphic condition, which is in accordance with Marx &
Rabb (1972) and Rasmussen (1979).
AN ANALYSIS OF SUBGENUS CHITULZA
I65
5mm
Figure 1. Dorsal aspect o f parietal. Characters 5 and 6; state 0: A . eydouxi (ZMUC R 661 125) (left),
in which parietal is without a distinct dorsal crest and without anterolateral process; state I ;
H . spiralis ( Z M U C R 661 132) (right), in which parietal has a distinct dorsal crest and anterolatpral
process.
7. Vomer ring: (the vomers have an inferior posterior process or lamina, which can
form a bony ring) ring complete (state 0), ring incomplete (state 1). State 0 is
found in all three species of the outgroup; therefore state 1 is regarded as an
apomorphic condition, which is in accordance with Marx & R a b b (1972).
However, Rasmussen (1979) mentioned that the posterior part of the ring is very
easily broken without any obvious injury. If so, the character is doubtful, as the
apparently apomorphic state could be the result of misinterpretation because of
a broken ring.
8. Nasals (Fig. 2): with ventral extension at medial articulation (state 0), without
ventral extension (state 1). State 1 appears to be a n apomorphic condition since
it is not present in the outgroup.
9. Optic fenestra (Fig. 3 ) : parasphenoid entering broadly into margin of optic
fenestra (state 0), parasphenoid nearly or completely excluded from margin of
optic fenestra (state 1). Both state 0 (N. scukztus, and P. lextilis) and state 1
( A . eydouxi) are found in the outgroup, based on the outgroup, it is unclear which
is the apomorphic state. Underwood (1967) suggested that a large optic fenestra
is derived. If this is correct, then state 0 is apomorphic; however, I believe that a
character reversal may have taken place leading to a n optic fenestra in which the
parasphenoid is nearly or completely excluded from the margin. Therefore I
regard state 1 as apomorphic, in accordance with McCarthy (1986).
IO. Mediouenlral ridge of basisphenoid absent (state 0 ) , present (state 1). T h e
outgroup lacks a ridge, which indicates state 1 to be apomorphic.
Ii. Anlerior Vidiun foramen: terminating on dorsal margin of basisphenoid
(state 0), terminating on ventral side of basisphenoid (state 1 ) . State 0 is found
in all three species of the outgroup, indicating state 1 as the apomorphic
A. R. RASMUSSEN
I66
I
I
5 mm
Figure 2. Ventral aspect of nasals. Character 8; state 0: H. bclcheri (ZMUC R 661 126) (left), in
which nasals have a ventral extension at medial articulation; state 1: H. lorqualus (ZMUC R
661 133) (right), in which nasals are without a ventral extension at medial aniculation.
condition, which is in accordance with McCarthy (1986), Rasmussen (1979),
and Underwood ( 1967).
12. Basioccipital medial process: absent (state O ) , present (in most species pointing
posteriorly) (state 1). State 0 is found in N . scuIatus, and A . eydouxi and state 1 is
found in P. textilis. The derived state of this character is uncertain, but state 1 is
here considered apomorphic.
Figure 3. Lateral aspect of anterior braincase. Character 9; state 0: H. nrnalus ( Z M U C K 661 131)
(top), in which parasphenoid enter broadly into margin of optic fenestra; state I: H. CyanoczncluJ
(ZMUC R 661127) (bottom), in which parasphenoid is nearly excluded from margin of optic
fenestra.
AN ANALYSIS OF SUBGENUS CHITCILIA
167
13. Lateral process of palatine approaching maxilla: absent (state 0 ) , present (state 1).
The lateral process is absent in all three species of the outgroup, indicating that
the presence of the lateral process is a derived state, which is in disagreement
with Marx & Rabb (1972), who consider that the presence of a palatine process
is correlated with maximal mobility of the maxilla, palatine, or both.
14. Maxilla-eclopterygoid length ratio: maxilla longer than or of equal length of
ectopterygoid (state 0), maxilla shorter than ectopterygoid (state 1). State 0 is
found in P. textilis and A . eydouxi, and state 1 is found in JV. scutatus. It is
uncertain which condition is derived, but maxilla shorter than ectopterygoid is
here considered apomorphic.
1.5. Number of solid maxillar_y teeth: at least 9 (state 0), less than 9 (state 1). State 0
is present in P. textilis and A . eydouxi; this state is regarded as plesiomorphic by
Marx & Rabb (1972), who proposed that a reduction in the number of teeth on
maxilla, pterygoid, and dental in connection with a poisonous injection is a
derived condition. I agree and regard state 1 to be the derived state, which is
contrary to Voris (1977).
26. Number of pterygoid teeth: at least 21 (state 0), less than 21 (state 1). State 0 is
found in N . scutatus, and A . eydouxi, state 1 in P. textilis. It is uncertain which
state is the apomorphic one, but state 1 is here considered to be derived, which is
in accordance with Marx & Rabb (1972).
17. Number o f pterygoid teeth posterior lo articulation with ectopterygoid (Fig. 4): at least
5 mm
Figure 4. Ventral aspect olpterygoid. Charartrr 17; state 0: H. lamherti ( Z M U C K 661 129) (left),in
which at lrast seven teeth are posterior t o articulation with cctopterygoid; state I: / I . y n o c z n c l u j
(ZMUC R 661 127) (right), in wliich lrwer than seven tceth arc posterior to artirulatioii with
ectopterygoid.
A. R. RASMUSSEN
I68
7 (state 0), less than 7 (state 1). State 0 is found in N. scutatus and A . eydouxi,
state I in P. textilis. It is unclear which state is derived, but state 1 is considered
here to be apomorphic.
28. Number of dentary teeth: at least 21 (state 0), less than 21 (state 1). State 0 is
found in all three species of the outgroup, and state 1 is therefore considered
apomorphic, which is in accordance with Marx & Rabb (1972) but in
disagreement with Voris (1977).
19. Dorso-venlral ridge on posterior edge o f quadrule (Fig. 5): absent (state 0), present
(state 1). State 1 appears to be an apomorphic condition as only state 0 is found
in the outgroup.
20. Dentary branches (Fig. 6 ) : (posteriorly the dentary is separated into a dorsal
branch (with teeth) and a ventral branch) dorsal branch obviously longer than
ventral branch (state 0), dorsal branch almost as long as or shorter than ventral
branch (state 1). State 1 is not found in the outgroup and is probably the
apomorphic condition, which is in accordance with McCarthy ( 1986).
21. Dentary foramen (Fig. 6):--dentary foramen anterior to gap between dorsal
and ventral branch (state 0), closest to or partly overlapping gap on ventral
branch of dentary (state 1). State 0 is found in N . sculatus and P. textilis, state 1
in A . eydouxi. It is uncertain which state is derived, but state 1 is considered here
to be apomorphic.
Characters not used in the analysis
T h e position of the fang tip in relation to the solid maxillary teeth, as well as
the presence or absence of a backward inclination on the quadrate, which were
1
I
5 mm
Figurc 5. Latrral aspect ofquadrate. Charartrr 19: state 0: H . Inpernoidel (ZMUC: K 661 130) (Irli),
in which quadrate is without a dorsoventral ridgc on posterior rdgr: stair I : H. I n m h ~ t / i
( Z U M C K 661 129) (right), in which quadratc has a dorsovmtral ridgr on postcrior rdgr.
A N ANALYSIS OF S U B G E N U S CHITU1,IA
L
169
I
S mm
5 mm
Figure 6. Lateral aspect of drntary. Characters 20 and 21; state 0: H. ornalus ( Z M U C R 661131)
(top), in which dorsal branch is obviously longrr than ventral branch, and dentary foramen (dQ is
anterior to gap between dorsal and ventral branch; staw I : H.,/ascintus (ZMUC K 661 128)
(bottom), in which dorsal branch is almost as long as ventral branch. and dentary fbramen is close
to or partly overlapping gap on ventral branch.
among the characters used by McDowell (1972) to distinguish between the three
subgenera, are not included in the analysis because I found the intraspecific
variation to be too great, and because there are difficulties in separating the
characters into well defined states.
Mid-throat scalation (character 14 in the analysis of Marx & Rabb, 1972) is
recognized as having two states within the genus Hydrophis. However, I could
recognize only one state (Marx & Rabb’s state 1 ) in the species examined. T h e
number of ventrals (character 20 in the analysis of Marx & Rabb) is not
included here as there are difficulties in finding a natural separation of the
character into states and because the intraspecific variation is considerable in the
examined species. All types of keeling are also excluded as I find the intraspecific
variation to be too great. The dorsal processes of the prefrontal (character 33 in
the analysis of Marx & Rabb) have been described as having three states in
Hydrophis;however, I could recognize only one state (Marx & Rabb’s state 3) in
the species examined.
Of the 43 characters used by Voris (1977) (of a total of 153 characters
collected), 20 show variation among the ingroup taxa examined here. Character
nos. 3, 5, 17, 22, 23, 83, 84, 87, 90, 92, 93 (all related to the scales) 30 and 138
(Voris, 1977), are not included in the analysis because I found the intraspecific
variation to be too great in the species examined, and because there are
difficulties in separating the characters into well defined states. Character nos.
34, 35, 52, and 82 (Voris, 1977) have been described as having two states in
I70
A. R. RASMUSSEN
Hydrophis; however, 1 could recognize only one state (Voris’s state 1, 1, 3 and 6,
respectively) in the species examined. Character 46 (Voris, 1977) was impossible
to score, as only fragmented skulls were available to me.
RESULI‘S
Euatuation of the dadograms
Four trees with a length of 37 steps and a consistency index of 0.59 were found
with the outgroup = taxa 0-2 (Fig. 7). The commands ‘xsteps h’ and ‘xsteps w’
were applied to the four trees (character weights from 0 to 10 according to fits,
and steps for each character are listed in Table 2). When using successive
character weighting the topology of the four cladograms did not change.
The character state polarizations given in the section ‘Character description’
are compared to those predicted by Hennig86. Alternative polarizations of some
of’ the characters in the preferred cladogram will also be mentioned. The clade
numbers refer to the preferred cladogram in Fig. 7.
All four cladograms were evaluated using ‘DOSEquis’. Trees 2 and 3 were
immediately rejected, in favour of trees 1 and 4.This is due to the presence of an
extra trichotomy, which gives less phylogenetic information than a dichotomy
(Fig. 7: clade 19 in tree 2 and clade 17 in tree 3). Trees 1 and 4 are both weakly
supported concerning H . (C.) striclicollis. However, I prefer tree 1, where clade
19 is supported by character 18 (number of dentary teeth, evolved convergently
in clade 22) rather than tree 4 in which this clade is supported by character
13(1) (lateral process of the palatine, subsequently reversed in the ancestor to
H. ( l , . )cyanocinctus and H . ( L . ) spiralis in both tree 1 and tree 4).I believe that
TABLE
2. T h e number of steps required for each
character to evolve, and character weights
according to fits using ‘successive weights’
-~
~-
Steps required for
each character
Character weights
according to fits
0
I
I
2
3
I
1
10
10
Character
number
4
S
6
7
1
1
10
10
10
2
I
10
3
3
2
8
9
10
3
2
I
3
1
II
I
2
2
2
10
10
0
12
13
14
IS
I6
3
0
2
2
4
4
17
IR
2
3
2
19
20
21
1
I
4
10
10
3
2
AN ANALYSIS OF SUBGENUS CHITULIA
171
H. (C.) stricticollis is the sister group to clade 19 (tree l ) , being less specialized
than any of the species in this group.
Evaluation of tree 1
(Fig. 7)
Clade 26: the ingroup is supported by the synapomorphies 1 ( l ) , 2( l ) , 5( I ) ,
6(1), 7(1), 10(1), l l ( 1 ) and 12(1). Clade 25: the sister relationship between
H. (C.) lamberti and H. (C.) ornatus is supported by 19(l ) , a ridge running dorsoventrally on the posterior edge of the quadrate. This ridge has not been found in
any other species examined. Clade 24: the monophyly is supported by the
synapomorphy 1 7 ( 1 ) (number of pterygoid teeth posterior to the articulation
with the ectopterygoid). The only trichotomy in the ingroup is found here and
involves H. (C.) caerulescens, H . ( C . ) lapemoides, and clade 23. Clade 23: the
monophyly is supported by 15(1) (number of maxillary teeth). Clade 22: the
monophyly is supported by 16(1) (number of pterygoid teeth). Clade20: the
sister-taxon relationship between H. (C.) belcheri and H . (C.) bituberculatus is
supported by 7(0) (vomer ring), which is a character reversal also found in
H. ( H . ) fasciatus, and by 18(1) (number of dentary teeth), which is predicted to
have evolved convergently in the ancestor of clade 19. Clade 21: the monophyly is
supported by 13(1) (lateral process of the palatine); this state is subsequently
reversed at clade 16, and by 21 ( 1 ) (dentary foramen), which appears to have
evolved convergently in H. ( C . ) caerulescens.
Clade 19: this clade is supported only by character 18(1), a convergence
predicted to have taken place in the ancestor of clade 20. However, an
alternative hypothesis exists in which state 1 of character 18 is a defining
character of clade 22, entailing a subsequent reversal in H. (C.) stricticollis. This
would not add extra steps to the ciadogram; however, clade 19 would then be
unsupported by synapomorphies, resulting in a trichotomy involving H. (C.)
stricticollis, clade 17 and clade 18. The resulting display is identical to that in tree
2 (Fig. 7). Clade 17 the monophyly of H. ( H . ) brookii and H. (H.) fasciatus is
supported by the character reversal 5(0) (dorsal parietal crest) and by 20( 1)
(dentary branch). Clade I 8 the monophyly of the clade which includes H. (C.)
torquatus, H. (L.) cyanocinctus, and H. ( L . ) spiralis is strongly supported by 4(1 )
(parietal length relative to width), and 9( 1 ) (optic fenestra), together with
character 8(1) (nasals). Clade 16: the relationship between H. ( L . ) cyanocinctus
and H. (L.) spiralis is supported only by 13(0),a reversal mentioned above for
clade 2 1.
Consensus tree
The consensus tree (Fig. 8) shows that the four cladograms differ only in the
presence of a trichotomy at clade 18 (see discussion of clade 19 above) and in
clade 17 due to character 13 (lateral process of the palatine).
0utgroup
Only in nine of the 22 characters used in the analysis did the states differ
within the outgroup. In character 0 (internasal scales) and character 3 (tail
A. R. RASMUSSEN
I72
Tree 1
0 N.scutatus
= Z E 1~ P-textilis
ll-
Tree 2
b261
p24c
13 H. C. orn tus
10 H.:C.ilderti
9 H.(C.)caerulescene
11 H.(C.)laDemoides
IF 12 H.(C.)mamillaris
L2zil
8 H.(C.)bituberculatus
7 H.(C.)belcheri
shape), A . eydouxi shares state 1 with the ingroup. An alternative hypothesis
exists in which state 0 in characters 0 and 3 could be taken as the apomorphic
condition, indicating that the Australian terrestrial elapids have a marine origin.
In character 12 (basioccipital medial process), P. lexlilis shares state 1 with the
ingroup. In the remaining six characters, the states differ both in the outgroup
and the ingroup.
AN ANALYSIS OF SUBGENUS CHITULIA
0
173
Tree 3
N.scutatus
13 H. C. orna us
24E 10 H. IC. ;lamb:rti
9 H.(C.)caerulescens
11 H.(C.)laDemoides
12 H.IC.)mamillaris
L2 il
H.(C.)bituberculatus
7 H.IC.)belcheri
8
$20E
11211
14 H./C.)stricticollis
=2&
Tree 4
N. cutatus
1 P.:extilis
0
it-
H. C. orn us
.5E 13
10 H. [C. ;lam%ti
9 H.IC.)caerulescens
11 H. IC. )laDemoides
12 H.IC.)mamillaris
8 H. C. bituberculatus
2 1 g 7 H. {C.ibelcheri
4 H. H. fasciatus
1 6 E 3 H.!H.lbrookii
15 H.fC.)torauatus
Figure 7 . ?‘he four most parsimonious cladograms (37-strps) indicated for speries examined by
Hennig86. T h e subgeneric assignments are those given by McDowell (1972, see text Tor details). The
preferred cladogram is tree no. I . Numbers denote clades referred to in thc text.
Evaluation of characters
The character transformations proposed in the section ‘Character description’
are in good agreement with those shown on the cladogram (for characters 0 and
3 see above), with the following character reversals and convergences assumed to
have taken place in the ingroup.
T h e following characters show reversal within the ingroup: character 5 (dorsal
parietal crest) has been lost in the small-headed species H. ( H . ) fascialus and
A.
174
R. RASMUSSEN
0 N.
tatus
= 2 6 r 1 P.:f:tilis
ir
li=
8 H. C.)bituberculatus
1 9 E 7 H.!C .)belcheri
14 H.IC.
icticolli&
16c 3
4 H. !H.
'::rbro;faeciatus
okii
L20Llf3[
lr
Figure 8. The consensus tree of the four cladograms shown in Fig. 7.
H . ( H . ) brookii. Character 7 (vomer ring; see discussion under character
description). Character 13 (lateral process of the palatine) was used by
McDowell (1972) to separate Chitulia and Leioselasma from Hydrophis; however, in
the preferred cladogram the character reversed in the ancestor of H. (L.)
cyanocinctus and H . ( L . ) spiralis. Character 18 (number of dentary teeth) see
discussion under clade 19 in 'Evaluation of tree 1'.
The following characters have evolved convergently within the ingroup:
character 8 (nasals): state 1 is found in H. (C.) lumberti, H. (C.) caerulescens and
also in clade 18; character 18 (number of dentary teeth) see discussion under
clade 19 in 'Evaluation of tree 1'; character 21 (dentary foramen): state 1 is
found in H. (C.) caerulescens and in clade 2 1 ; however, other characters (1 3, 15,
and 16) support the hypothesis that character state 1 has evolved twice within
the ingroup.
It is worth noting that there are two sets of characters which have the same
distribution of scores across the taxonomic units: characters 0 and 3, and
characters 1, 2, 6, 10 and 11 (one missing score for 11). This means that, for the
22 characters, there are 17 different patterns of scores. This is only two more
than the minimum (15) required for the analysis of 16 taxa in the complete
absence of homoplasy.
Test of McDowell's (1972) hypothesis
The cladogram in Figure 9 was constructed on the basis of McDowell's (1972)
classification. The cladogram was entered into Hennig86 with the command
'tread' and tested using the same 22 characters as those appearing in the
preferred cladogram. The tree has a length of 45 steps and a consistency index of
0.48; the tree based on McDowell's hypothesis is thus eight steps longer than the
preferred tree.
AN ANALYSIS OF SUBGENUS CHITULIA
I75
0 N.scutatu
= z K 1 P.textiliz
6 H. L. s ir l i
L 27
2
2 5 ~H
.IL . c;anXctus
3 H. H. brookii
4 H. IH. ifasciatus
15 H.(C.)torouatus
14 H. (C.)stricticollis
8 H. C. bituberculatus
1
8
g 7 H. I C . ;belcheri
9 H.(C.)caerulescens
11 H.(C.)laDernoides
.
H ( C . I larnberti
H.(C.)ornatus
Figure 9. Cladogram constructed on the basis of McDowell’s (1972) classification. The tree has a
length of 45 steps and a consistency index of 0.48.
Remarks concerning the use of Hennig86
The data matrix (Table 1) was analysed eight times, differing only in the
order of taxa, and analysed with Ye*’. The result showed no change in the
ingroup, but four new equally parsimonious cladograms with the same length as
the four cladograms first produced showed up. The changes in these cladograms
took place only when the three outgroup taxa were moved from the top to the
bottom of the data matrix. The four extra cladograms found differ from the first
four only in the position of A . eydouxi. In the four first cladograms, A . eydouxi is
the sister-group of the ingroup; in the last four A . eydouxi forms a trichotomy
together with a clade containing JV.scutatus and P. textilis and the ingroup. T h e
two different solutions concerning the relationships of the outgroups are further
complicated by the way in which the cladograms are displayed. Hennig86
always displays cladograms with a trichotomy at the root. I t is also worth
mentioning that Hennig86 failed to find all the most-parsimonious trees for
certain other data matrices (Maddison, 1991). Especially if preliminary searches
indicate low retention indices for the most parsimonious trees (less than 0.67)
and the number of terminal taxa is much greater than 20 (Maddison, 1991).
The character state of four of the two-state characters in H. mamitlaris are
unknown (marked by a ‘?’ in the data matrix). In such cases, algorithms should
allow for both possibilities in the unknown states when selecting the most
parsimonious cladograms. The 16 different ways of combining the character
states for the four unknown characters are shown in Table 3. Hennig86 selected
a solution (character states 0101 for the four missing characters) which gave the
four shortest trees (test 1 1 in Table 3 ) . However, it is interesting to note that if
the correct state of one of the four missing characters for H. mamillaris is opposite
to the state predicted by Hennig86, the results gave four other solutions (test 7,
18 trees; test 8, 49 trees; test 13, 4 trees; and test 16, 4 trees) which all have a
A. R. RASMUSSEN
TABLE
3. ‘l‘he 16 diflercnt configurations for the four unknown
characters (4,7, 8, 1 I ) of Hydrophis mamillaris were tested using
‘ie*’. ’l‘hc number of strps, the consistency index, and the
number of trees resulting from each test are shown and are
dependant on which of thr four character states are selected for
H. mamillnri.r.
Test
ie*
Chdrdr I C T
srdtes
Consistenry
Number of
steps
index
trees
39
0.56
0.56
0.56
0.56
0.56
0.56
0 57
0.57
0.55
0.55
0.59
0.53
0.57
0.55
0.55
0.57
149
67
~-~
-~
~
I
2
0000
001 1
3
1111
1100
0110
1001
0111
000 1
4
5
6
7
8
9
10
II
12
13
14
15
16
I000
1110
0101
1010
0100
1011
0010
I101
39
39
39
39
39
38
38
40
40
37
41
38
40
40
38
18
4
18
49
18
49
149
18
4
200
4
67
200
4
length of 38 steps and a consistency index on 0.57. It should be mentioned,
however, that the four most parsimonious cladograms (Fig. 7 ) found in test 1 1
were also found in the 15 other tests in Table 3 (see also Platnick et al., 1991 and
Nixon & Davis, 1991 regarding other problems concerning missing entries in
cladistic analysis).
DISCIISSION
Phylogeny and taxonomy
McDowell (1972) divided the genus Hydrophis into three subgenera based on
the number of teeth on the maxilla, pterygoid and dentary bone, the presence or
absence of a triangular flange on the palatine, the position of the tip of the fang
in relation to solid teeth on the maxillary bone, and whether the parasphenoid
anters into the margins of the optic fenestra. ‘lhe relations of the proposed
subgenus Chitulia to the two other proposed subgenera was examined here using
22 characters, T h e conclusion of this analysis is that Chilulia is based solely on
plesiomorphic character states. In particular, the number of teeth on the
maxillary, pterygoid and dentary bones shows a tendency to diminish from the
root to the top in the ciadogram. State 1 of character 13 (lateral process of the
palatine) was used by McDowell (1972) to separate the subgenus Hydrophis from
the two other subgenera; however, both H. slriclicollis, which is the sister-group
of clade 19 (Fig. 7 , tree 1 ) and H. lorquatus, which is the sister-group of clade 16
(Fig. 7, tree 1 ) have the apomorphic condition. The only character state that
justifies McDowell’s subgenus Chilulia (but not H . lorquatus) is 18(0) (number of
dentary teeth). As ancestral character states are inappropriate in the elucidation
of relationships of any kind (Wiley, 1981), and as Chilulia appears to be
AN ANALYSIS OF SUBGENUS CHITLILIA
177
paraphyletic, I conclude that McDowell’s subgenera should be rejected.
Nevertheless, McDowell’s definition of the genus Hydrophis suggests it to be
monophyletic. However, a cladistic analysis of Hydrophis sensu lato still remains to
demonstrate whether Hydrophis is a monophyletic group.
Burger & Natsuno (1975) suggested including the genus Disteira in the genus
Hydrophis as a fourth subgenus; this appears to me to be without foundation.
Species such as Astrotia stokesii and Enhydrina schistosa (Disteira sensu McDowell,
1972) appear to constitute monotypic genera, and most studies show that Disteira
is composed of several distinct phyletic lines (Cogger, 1975; Smith, 1926; Voris,
1977). As Kharin (1984) based his proposal to raise the three subgenera created
by McDoweH to generic status on the same characters as McDowell, this
suggestion should also be rejected.
Young (1987) questioned some of McDowell’s characters because functional
morphological criteria were not utilized in these studies. The same claims could
be made against the present study, as no attempt has been made to include
functional morphological criteria. However, functional morphological criteria
still have to prove that they are a necessary component of phylogenetic analysis
(Bonde, 1982; Cracraft, 198 1 ) .
Biogeography
When I started to test McDowell’s hypothesis, I assumed the subgenus Chitulia
to be a monophyletic group. However, the preferred cladogram indicates that
Chitulia is paraphyletic. Therefore, it is not possible to conduct a cladistic
biogeographical analysis of Chitulia, which is appropriate for monophyletic
groups only (Nelson & Platnick, 1981; Humphries & Parenti, 1986). However, a
few comments are added below on the biogeography of some of the species
within the preferred cladogram.
H. belcheri (sensu McCarthy & Warrell, 1991) and H . bituberculatus, which
comprise a small monophyletic group, are not found sympatrically, but show a
vicariance pattern. H. belcheri has been recorded from the Gulf of Thailand and
the Java Sea (McCarthy & Warrell, 1991), and H. bituberculatus is known from
Sri Lanka and the Andaman Sea (Rasmussen, 1992). None of the other speciespairs in the analysis show a vicariant pattern. Three species have a very limited
distribution area, H. mamillaris and H. .rtricticollis are both endemic to the eastern
part of the Indian Ocean, and H. torquatus has been recorded only from the
Malacca Strait and the Gulf of Thailand (Minton, 1975; Smith, 1926; Taylor,
1965). The other species are all more widely distributed.
ACKNOWLEDGEMENTS
I thank the staff of The Phuket Marine Biological Center, Thailand; CODEC
Project, Chittagong, Bangladesh; Ministry of Commerce and Agriculture,
Directorate of Fisheries, Bahrain; S. Bagge, Cowi- Almoayed Gulf, Bahrain; J.
Jensen, Danida, and M. Andersen who helped me during the collection. Drs
N. M. Andersen, D. Eibye-Jacobson, and N. Scharff gave valuable advice and
constructive criticism on using ‘Hennig86’.
M. Andersen, A. B. Helwigh, Drs A. Greer, 0. Seberg, and especially Drs C.
McCarthy and J. B. Rasmussen provided valuable advice and constructive
I78
A. R. RASMUSSEN
criticism of the manuscript. T h e study was supported by Dansk Naturhistorisk
Forening, the Johannes Schmidts Grant, T h e Krista and Viggo Petersens Grant,
and the Danish National Research Council, Grant no. 11-8209.
REFERENCES
Bonde N. 1982. Functional anatomy and reconstruction of phylogeny. Aries du Lymposium paleonfologigve. 1982:
1 1-26. France: Georges Cuvier, Montebeliard.
Burger WL, Natsuno T. 1974. A new genus for the Arafura smooth seasnake and redefinitions of other
seasnake genera. The Snake 6: 61-75.
Cadle JE, Gorman GC. 1981. Albumin immunological evidence and the relationships of sea snakes. Journal oJ
Herpetology 15: 329-334.
Cogger HG. 1975. Sea snakes of Australia and New Guinea. In: Dunson WA, ed. The biology of sea snakes.
Baltimore, London & Tokyo: University Park Press, 59- 139.
Cogger HG. 1986. Reptiles and amphibians o f Australia. Revised editiun. Sydney: A. H. & A. W. Reed.
Cracraft J. 1981.The use of functional and adaptive criteria in phylogcrietic systrmatics. American zoologisf 21:
21-36.
Farris JS. 1988. Hennig86, uersion 1.5. Computer program and ducumentation. New York: Port Jefferson Station.
Humphries CJ, Parmti LR. 1986. Cladisfic biogeography. Oxford monographs un biogeography. Oxford: Clarendon
Prcss.
Kharin VE. 1984. A review of sea snakes vf the group Hydruphis sensu lato (Serpentes, Hydrophiidae). S. the
genus Leioselasma. <oologicheskij l h u m a l 63: 1535- 1546.
Maddimon WP,Donoghue MJ, Maddison DR. 1984. Outgroup analysis and parsimony. $ylernaftc <oolo,g
33: 83-103.
Maddison WP. 1991. The discovery and importance of multiple islands of most-parsimonious trees. Systematic
< O O ~ O ~ J40: 315-328.
Marx H, Rabb GB. 1972. Phyletic analysis of fifty characters of advanced snakes. Fieldiana, <oology 63: 1-32 I .
McCarthy CJ. 1986. Relationships of the laticaudine sea snakes (Serpentes: Elapidae: Latiraudinae). The
Bulletin of the Hritish Museum of Nafural History (<oology Series) 50: 127-161.
McCarthy CJ, Warrell D. 1991. A collection of sea snakes from ‘rhailand with new records of &drophi5
belchrri (Gray). The Bulletin of the Britbh Museurn of Natural History (<oology Series) 57: 161 166.
McDowell SB. 1972. The genera of sea-snakes of the Hydrophis group (Scrpcntes: Elapidar). Transactions oflhe
<oological Sociely of London 32: 189-247.
Minton SA. 1975. Geographic distribution of sea snakes. in: Dunson WA, ed. The biologj of sea snako.
Baltimore, London & Tokyo: University Park Press, 21-31.
Nelson G, Platnick N. 1981. Systematics and bzogeugraphy cladislics and uicarianre. New York: Columbia
University Press.
Nixon KC, Davis JI. 1991. Polymorphic taxa, missing values and cladistic analysis. CladzJtzcs 7: 233- 241.
Platnick NI, Criswold CE, Coddington JA. 1991. O n missing entries in rladistic analysis. Cladistics 7:
337-343.
Rasmussen AR. 1989. An analysis of Hydrophis ornatus (Gray), H . lamberfi Smith, and H . inurnafu.\ (Gray)
(Hydrophiidae, Serpentes) based on samples from various loralities, with remarks on feeding and brccding
biolvgy of H . ornalus. Amphibia-Replilia 10: 397-41 7.
Rasmussen AR. 1992. Rediscovery and redesrription of Hydrophis hitubertulafus Pctcrs, 1872 (Serpentcs:
Hydrophiidae). Herpefologica 4181 85-97.
Rasmussen AR. 1993. The status of the Persian Gulf Sea Snake Hydrophi3 lapemuzdvs (Gray, 1849) (Serpentes,
Hydrophiidae). The Bullefin of fhe B r i h h Museum of .Natural I h t o r y (<oology Series) 59(2):97-105.
Rasmussen JB. 1979. An intergeneric analysis of some boiginc snakes Bogert’s (1940) group XI11 and XIV
(Boiginae, Serpentes). Videnskablige Meddelserfra Dansk .Naturhisforisk Forening 141: 97- 155.
Schwaner TD, Bavcrstock PR, Dessauer HC, Mengden CA. 1985. Immunological evidence for thc
phylogeneiic relationships of Australian elapid snakes. In: Grigg G, Shine R, Ehmann H, eds. Biolqpv of
AurlralianJrogs and repliles. Australia: Beatty & Sons, 177-184.
Smith MA. 1926. Monograph oJ fhe sea-snake& { Hydrophiidae). London: British Museum (Natural History).
Taylor EH. 1965. The serpents of Thailand and adjacent waters. liniuersily of Kansas Science Bulletin 45:
609- 1096.
Underwood G. 1967. A cunfribution lo the clnJJzJicnfionof makes. London: British Museum (Natural History)
Publication 653.
Voris HK. 1977. A phylogeny of the sea snakes (Hydrophiidaej. Fieldiana, <ou/u,cy 70: 79 166.
WUey EO. 1981. PhylogenelicJ: Ihe fhrory and prnclice ?f phy/ogenelic syslematics. New York: John Wilcy & ~ I J I l S .
Williams KL, Wallach V. 1989. Snakes UJ‘ !he uarld. Voi. I . Synopsis qf snnke genrrir namrs. Florida: Krieger
Publishing Company Malahar.
Young BA. 1987. The cornparativc cephalic osienlogy and myology of three species of sea snakcs. ~ 0 : 0 0 / 1 J ~ ~ Z J ~ ~ h Y
,]ahrhuecher. dbfeiiung fuer Anafumie und Ontogenir der Tiere 116: 421 452.