Asiatic Herpetological Research

1997

Vol. 7, pp. 32-37

Phylogeny of Genus Scutiger (Amphibia: Megophryidae): A Re-evaluation
Jinzhong Fu, Amy Lathrop, and Robert W. Murphy
Department of Ichthyology and Herpetology, Royal Ontario Museum, 100 Queen's Park, Toronto. Ontario,
Canada M5S 2C6, and Department of Zoology, University of Toronto
Abstract. - A re-analysis of a published data set from Ye et al. ( 1992) indicates that their phylogeny for the genus

Scutiger does not reflect the most parsimonious explanation of the data. The consensus of the resulting trees
from the original data set is a "bush" with only three resolved nodes. A re-evaluation of the character states, andtheir respective polarizations, resulted in alternative phylogenetic hypotheses. However, measures of homoplasy

and data consistency for the re-evaluated topologies were relatively low, suggesting that little confidence could
be obtained in these relationships.

More data are needed to generate a defensible hypothesis of the relationships

within the genus Scutiger.

Key words: Amphibia. Anura, Pelobatoidea. Megophryidae, Scutiger, morphology, phylogeny, parsimony

thisgroup has been wanting. The genealogical rela-tionships of this group would be useful for assessing
theories of the geologic events that have been linked

with the uplift ofregion. Recently, Fei andthis(1990) and Xu et al.

Ye(1992) investigated the relation-

ships of megophryids.

Of particular interest. Ye et al.

(1992) presented a phylogeny of genus Scutiger using

29 morphological characters.
Unfortunately, someinvalid methods were employed in both the character
analysis and tree selection, and these nullify theirCharacter 27
Lineaabsenthypothesis.

musculinae(0);present

al.

(1)

1

Figure 1.

ancestral state for Oreolalax

Phylogeny of Oreolalax with the character

states of linea musculinae optimized on the tree.

Theprimitive condition of linea musculinae for the phylog-

eny of Scutiger is 1.

We performed a re-evaluation of the Ye et(1992) data, and examined their proposed phylog-

eny of Scutiger.

Methods
The data of Ye et al. (1992) consisted of 29 morphological characters for 16 species of Scutiger, and one

outgroup taxon (Appendix I). Initially, we analyzed
these data without modification. Following Ye et al.
(

Introduction1992), five species, Scutiger ningshanensis, S. macu-

and S. adungenwere excluded from the analysis owing to many

latus. S. nepalensis. S. occidentalis,family Megophryidae have long capti-

Frogs

in thevatedmany herpetologists,

especially Chinese col-leagues, partly because of their supposed transitional

position between "primitive" and "advanced" frogs(Lynch, 1973, Ford and Cannatella, 1992) and also

sis,unknown character states (Appendix II).

We usedoutgroup analysis (Maddison et al., 1984) to reassesscharacter state polarizations. Oreolalax was used as
the outgroup and polarizations of the character states

because of asthetic appeal. The phylogeny of peloba-

were determined from previous work (Fu and Mur-

toids is largely unknown, and we now realize that thephy, in press).

concepts of "primitive" and "advanced" taxa are phylogenetically flawed and hence unacceptable: only

identify pleisomorphic character states for Oreolalax,

character states have these attributes.

Thirty-two species of Scutiger occur in the highaltitudes of the Tibet Plateau in southwestern China.

Burma. Nepal, and northern India.

A phylogeny ofFrom this phylogeny, we were able towhich were then used to polarize the character states
for scutigers. For example following Maddison et al.
1991 ). we assigned character(1984) and Wiley et al.

(states for the terminal

branchesreaching the root node (see Fig.
of Linea Musculinae).

1

down the tree until
for the optimization

Vol. 7. p. 33

Asiatic Herpetological Research

1997

Orootelax
Hypothetical ancestor
Itupanonsis

S chintingensis

SS.

s chlntlngmnsla
S. pingwuensts
S boutongon
S.

S

brovipas

S mammatus

S-

S. tuberculatus(1992) original data.

gongshanests

S brevipes
S mammatus
S muliensis

S gongshanosis

Figure 2. Strict consensus tree of the phylogeny ofal.'s
Scutiger, derived from our reanalysis of Ye ettiupanensis

S beulengen
S nymgchiensis
S tuberculatus

nytngchlansls

S sikklmansts
S.

sikhimensis

S pingwuensis

MPTs
Figure 4. Phylogeny of Scutiger. One of 16
derived from Ye et al.'s (1 992) data using Oreolalax as
the outgroup. When the outgroup condition was notknown, the original character state polarizations of Ye
et al. were used. This topology was reached by suc-Hypothetical ancestor

S
5

I

Itupanonsis

S plngwu&nsls
S chintingensis

cessive approximations; numbers indicate unambigu-

ous synapomorphies occuring at each correspondingnode.

S Oouleng&n
2
IS.

muli&nsts

S brevipes
2

D

S tuberculatus
S gongshanasls

S nytngchiensis
S sikkimensfs

tuberculatus and S. gongshanensis were resolved
by Ye et al. (1992). Excluding these relationships, all.S\others were ambiguous.

et

al.

requires 63 steps to explain the data, one steps longer

than
Figure 3. One of 20 MPTs depicting the phylogeny ofof Ye etScutlgerthai was derived from our reanalysis
al.'s (1 992) original data. When the outgroup condition

The topology of Ye

ourmost parsimonious

tree.

A

successive

approximations evaluation resolved a single tree, oneof the original 20 MPTs (Fig. 3).

Re-examination of the character polarizations of

was not known, the original character state polarizations of Ye et al. were used. This topology was

Ye et al. (1992) shows that characters 3 and 27 werereached by successive approximations (Farris. 1969);

incorrectly polarized in the original work.

numbers indicate unambiguous synapomorphies
occuring at each corresponding node.

unable to polarize character 25 because both statesoccur in the outgroup; the presence or absence of spinal patches on the forelimbs are equally probable as a

Phylogenetic analyses were conducted using(PAUP) version 3.1.1 (Swofford, 1993) and employan heuristic search with stepwise addition. Treeing

optimization was performed using the tree bisectionbranch swapping option, steepest
reconnection
descent, and retainingallmost parsimonious trees.

Tree topologies were analyzed in MacClade 3.04
(Maddison and Maddison, 1992). To choose among
the most parsimonious trees, we employed successive1969).
(Farris.
Decay analysis
approximations(Bremer. 1988) was used to assess nodal stability.

plesiomorphy for Scutiger. Characters

1

We wereand 26 haveautapormorphic states only, making them phylogenetexcluded from subseically uninformative; they werequent analyses. Polarization of characters 7, 8, 9, 10,
II. 15. and 17 was not possible using outgroup criterion

because thestate(s)intheoutgroup are notknown. These characters were treated both using theand subseoriginal polarizations of Ye et al. (1992).
quently by treating them as missing data in the outgroup.

Our analysis using the polarizations of Ye et al.
(1992) for characters 7-1 1, 15, and 17 resulted in 16

MPTs, 60 steps in length (ci = 0.45. ri = 0.53). The

Results

strict consensus tree is identical to that of the original

Our initial evaluation of the phylogeny of Scutiger
using the unmodified original data of Ye et al. (1992)

sucanalysis with only three nodes resolved. Usingiswhichcessive weighting resulted in a single

resulted in 20 most parsimonious trees (MPTs), eachone of the 16 MPTs (Fig. 4). When supporting characters were mapped on the phylogeny, most of the nodes

with a consistency index (ci) of 0.46, retention index(ri)

of 0.53 and a length of 62 steps.

A strict consen-

MPT

received verysus tree revealed only three consistent nodes (Fig. 2).

data.

Scutiger gongshanensis with S. tuberculatus wereresolved as sister species, as were S. pingwuensis andthat

Only the latter relationship and theassociation of S. mammatus. S. brevipes, S. muliensis.

S. chintingensis.

littleunambiguous support from these

The alternative approach treated character states
were unknown in the outgroup as missing data.
tree (Fig. 5), ci =This resulted in most1

parsimonious

1997

Asiatic Herpetological ResearchVol. 7, p. 34- Oreolalax

Oreolalax

S sikkimensis

S nyingchiensis
S boulengen
S.

0_
5
i

2
4

2

S tuberculatus

S gongshanesis
S brevipes
S mammatus
S muliensis

Figure 6.

In this topology, like the(1992). or we treated the outgroup states as missing,

unpolarized.

The

former analysis resulted in 16 MPTs
strict consensus tree was identical to our first analysis.
The latter analysis resulted in one tree depicting(1992). recognized two subgenera in thegenus Scutiger. Scutiger and Aelurophryne. They
identified three synapomorphies for the latter, andbased on the derived relationships and current distri-drew conclusions about the origin of

S gongshanein

Discussion

butions,

B muliensis•

The resulting strict consensus tree of Scuti-

thereby treating the characters asothers, few unambiguous changes have occurred.

al.

-

ger after saving all trees one step longer than the
shortest tree, from the data set where unknown outgroup states were left as missing.

unambiguous synapomorphies occuring at each node.

etpingwuensis- S sikktmensis

A single MPT for the relationships of Scutiunknown states for the outger. The data in whichasleftmissing. Numbers indicate
group areYellupan-- S- S. Doulengen- S nyingchiensis

liupanensis

S chmtmgensis
S pingwuensis

Figure 5.

0.49, ri = 0.57 and 59 steps.

- S- S. chintlngensts

2_

the

scutigers.

Our results show that the phylogeny of Ye et al.

which theAelurophyrne as monophyletic. and S. chintingensis
and S. pingwuensis as sister species. It did not resolve
the subgenus Scutiger as a monophyletic assemblage.
Itisdesirable to assess the support for individual

nodes and the entire phylogeny. Several methods havebeen proposed. One procedure, bootstrap (BS) analy1985), assesses relative support forsis (Felsenstein.

(1992) was not the most parsimonious explanation of
their data. We resolved 20 trees that were more parsi-

each node of a phylogeny (for criticisms of themethod see Carpenter, 1992; Hillis and Bull, 1993;

A strict consensus of our shortest trees

Kluge and Wolf. 1993; Trueman, 1993). One prerequisite to a BS analysis often overlooked, is that a min-monious.

resulted in a tree with only three nodes resolved. As

was true in Ye et al.'s tree, Aelurophryne was monophyletic and supported by three synapomorphies.
Within this clade the sister relationships of only two
could
species, S. tuberculatus and S. gongshanensis,

be unambiguously resolved.

The remaining scutigers

the
with
polytomy
S. chintwere
resolved.
but
twospeciesAelurophryne.

formedasinglebasal

This sister relationshipingensis and S. pingwuensis.
was also seen in Ye et al.'s tree,

our analysis did not

resolve the subgenus Scutiger as a monphyletic group.

imum three characters per node is required to obtain a
BS value. Unfortunately, ourstatistically significant
have
MPTs do notenough unambiguous characterchanges at each node to generate statisticallymean-ingful BS values.

Decay analysis (Bremer.
method, keeps

all1988).

an alternative

trees that are a specified length

the assessment of
longer than the MPTs. It permits
nodal support by identifying only those monophyleticancestor rather than Oreolalax as the outgroup. somegroups that are common to all of the possible
This method presumes that all relationships receiving
sound support from these data will be present in acharacters were incorrectly polarized.

strictYe et al. (1992) apparently used a hypothetical
Consequently,

trees.

consensus tree of all trees one or two steps
When we held all MPT plus those one step

we believe that any conclusions derived from either

longer.

their phylogeny or our reanalysis of the original data

longer, 241 trees

set are invalid.

consensus

The proper ordering and polarizations of character
states using the outgroup criterion proved very important.

Failure to defensibly order states of multistatecharacters resulted in the resolution of less parsimoni-

ous solutions. Even though we changed the polarizations of two characters, seven other characters could
not be polarized. Consequently, subsequent analyses
either left the polarization asassumed by Ye etalwere retained. The resulting strict
showed no resolution; all of theHowingroup taxa were resolved from a single node.
tree

when the ambiguously polarized states werecoded as missing data in the outgroup, the MPTs andthose one step longer included 27 trees, and the strictever,

one ingroup clade,into
all trees two steps
Holding
Aelurophiyne
longer resulted in 362 trees and a single polytomy.
consensus

tree

broke

(Fig. 6).

1997

Asiatic Herpetological ResearchTheof the subgenera Aelurophryne andstatusScutiger has been debated (Myers and Leviton, 1462;
Noble. 1931; Pope and Boring. 1940; Liu. 1950) and

Aelurophryne was previously diagnosed by theabsence of maxillary teeth.
Meyers and Leviton(1962) stated that the absence of teeth actuallyreflected a graded trend within the genus Scutiger, and
could

not

be

used

Scutiger fromalso true for two of the threeto

Aelurophryne. This ischaracters used by YeetHowever,bone can be

al.

the

Aelurophryne.
metacarpal

separate(1992)

todefinepresence of a robust
usedtodistinguish

Aelurophryne from other scutigers.

Ye et al. (1992). used their phylogeny to discussand specialization of Aelurophryne.
described
the subgenus as having become moreTheyevolution

theVol. 7, p. 35

plesiomorphic condition in Oreolalax. Once a soundphylogeny of the genus has been achieved, it will bepossible to address biogeographical, ecological, andbehavioral questions.

Acknowledgments
Many thanks to D. Upton, whose comments greatly
improved the quality of this paper. This work is supported by Natural Sciences and Engineering ResearchCouncil of Canada grant No.

No.

A3 148 to RWM, andOGP46464 to K. Coates.

This

is

contribution

XXX from the Centre for Biodiversity and Conservation Biology of the Royal Ontario Museum.

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and recognize

Bremer. K. 1988. The limits of amino acid sequence

three synapomorphies: robust metacarpal bone, thickhumerus, and the no keritanized spines on the dorsum.

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Ford. L. S. and D. C. Cannatella. 1993.

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Therefore, ouranalysis requires that the subgenus Aelurophryne not
be recognized if a holophyletic classification is to be

maintained.

One problem that permeates the data base is theselectionofresolution.

However, we cannot comment on thecharacters.

highlyhomoplastic
Homoplastic characters tend to provide no definitive
quality of characters until

we can see how they per-form during a defensible phyletic estimation. We arecertain that too few characters were used to generate

support for any of the relationships on the phylogeny.

The information summarized by Ye et al. (1992)
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Lynch, J. D. 1973. The transition from archaic toadvanced frogs, pp 133-182. In Evolutionary biology

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Appendix

I

Modified data set ofYe et al (1992). Characters were polarized using Oreolalax as the outgroup. Those charactersinbold were omitted from the analysis because they are apomorphic.

Character

1

11111 11112 22222 2222

number12345 67890 12345 67890 12345 6789

Oreolalax

001 00 00000 00000 00000 0000- 01 00

S. liupanensis

11101 00011 10101 01101 110100000

S. pingwuensis

01111 00111 10001 00101 11011 0011

S. chintingensis

00111 01101 00001 01001 11001 0011

S. boulengeri

01101 10000 10100 01100 11010 0000

S. nyingchiensis

01 001 00001 01 000 1 1 01 1

S. sikkimensis

01 1 00 1 1 1 1 1S.

mammatus

10000 0001

00000 01111 1 1 000 1 001

01001 10010 01110 10100 10100 0001

S. brevipes

01101 10000 01110 10101 10000 0001

S. tuberculatus

01011 10000 01110 11101 10000 0011

S. muliensis

01011 10000 01110 10101 10100 0001

S. gongshanensis

00111 10011 11110 1111000000 0111

Asiatic Herpetological Research

1997

Appendix

0: ossified,II

Character used by Ye et al (1992).
1

16.

0:

0:

width > length.

1

width < length

:

0:

1:

very small or absent

0: articulated,

1:

1

:

0: absent,

0: long, articulated or overlapped with maxilla,

0: seperated.

1:

0: present,

absent1 :1:

two pair

23. Spines on the chest
0: small.

1:big

24. Spinal warts on belly

Hyoid fenestra
0: present

0: absent,1:

present

25. Spinal patches of forelimb1:absent0: absent.

1:

present

26. Nuptial spinescomplete circle.

1:

circle incomplete

10. Omosternum and xiphisternum

0: small. 1:

big

27. Linea musculinae

Width of omosternum < width of xiphister-

0: absent.

num. 1: width of episternum >width of xiphis-1:present

28. Labial margin of tadpole

ternum.

present

22. Spiney patches on the chest

HPAP < DFAP. 1: HPAP > DFAP

9. Cricoid cartilage

1

1:

0: one pair.

(DFAP)

1absent

:

.

fused

7. Hyoid plate plus anterior process (HPAP) and the
distance between the out flank of the anterior process

0:1

2 1 Vocal sac

short, wildly seperated from maxilla

6. Prootic and exoccipital bone0:

present:

20. Metatarsal tubercle

absent5. Quadratojugal

8.

without horny spines

0: present, 1: absent

0: present

0::

19. Webbing between toes

4. Columella:

1

0: present.

seperatedI

18. Post-femoral gland

3. Nasal and sphenethmoid1with homy spines,

0: absent.

well developed.

cartilage

17. Large warts near vent

Maxillary teeth

2.

1:

Dorsal skin

Head width to length.

Vol. 7, p. 37

0:

Omosternum

narrow, with many tubercles,

1:wide, withfew or no tubercles
0: partially ossified. 1: entirely cartilage

29. Labial teeth formula of tadpole.

12. Humerus in male0:13.

length/width > 4. 1:

length/width < 4

Inner crest of radioulna in male
0: absent.

1:

present

14. Inner two metacarpals and phalanges in male0:

normal. 1: robust

15. Prepollex

Number of toothrows
0: >I:5-5/I:5-5,

1:< 1:5-5/1:5-5.