Phylogenetic Relationships of the Angel Sharks, with Comments on Elasmobranch

Phylogeny (Chondrichthyes, Squatinidae)

Author(s): Shigeru Shirai
Source: Copeia , May 1, 1992, Vol. 1992, No. 2 (May 1, 1992), pp. 505-518
Published by: American Society of Ichthyologists and Herpetologists (ASIH)

Stable URL: https://www.jstor.org/stable/1446211

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Copeia, 1992(2), pp. 505-518

Phylogenetic Relationships of the Angel Sharks, with

Comments on Elasmobranch Phylogeny
(Chondrichthyes, Squatinidae)
SHIGERU SHIRAI

A new hypothesis of the phylogenetic position of the angel sharks, Squatina,

is proposed based on a cladistic character analysis of skeletal, myological, and
external morphologies. Squatina is compared with squaloids, pristiophorids,
Chlamydoselachus, hexanchoids, and all major rajiform taxa. Squatina is con-
cluded to be the sister group of pristiophorids plus rajiforms; a pristiophorid-
rajiform relationship is evidenced by four synapomorphies. Squatina, pristiopho-
rids, and rajiforms (the hypnosqualean group) share five distinct modifications
of the (1) cranio-vertebral articulation; (2) condyles of the scapulocoracoid car-
tilage that supports the metapterygium of the pectoral fin; (3) supraneurals of
the vertebrae; (4) dorsal-fin musculature, and (5) caudal-fin musculature. A most
closely allied group with the hypnosqualean group is now ambiguously recog-
nized; squaloids or a part of them form the most probable candidate.

A NGEL sharks comprise 12 species (Com- logenetic position of Squatina, provides an al-
pagno, 1984) in a single genus, Squatinaternative hypothesis of elasmobranch interre-
Dumeril. All species are benthic with a wide
lationships, in which Squatina is shown to form
distribution in temperate to tropical waters and
the sister group of pristiophorids plus rajiforms.
range from inshore to depths of 1000 m (Big-
elow and Schroeder, 1948; Compagno, 1984). MATERIALS AND METHODS
The relationships of angel sharks with other
living elasmobranchs have been controversial. Material examined includes seven species of
Previous authors aligned them with variousSquatina and 47 additional species: seven raji-
elasmobranchs, i.e., squaloids (Miiller and
forms, four pristiophorids, 19 squaloids, three
Henle, 1841; Jordan, 1923), squaloids + pris- hexanchoids, one species of Chlamydoselachus,
tiophorids (Regan, 1906; White, 1937; Aram- one heterodontoid, and 12 galeoids (see Ma-
bourg and Bertin, 1958; Nelson, 1984), Heter- terial Examined). Emphasis was placed on ex-
odontus + squaloids + pristiophorids (Norman, amining squaloid and pristiophorid members
1966), orectolobids (Holmgren, 1941), squa-because many former workers had regarded
loids + pristiophorids + Chlamydoselachus +them as close relatives of Squatina. Within raji-
hexanchoids (Maisey, 1980, 1984a, 1985), raji- forms, representatives of the less derived taxa
forms (Goodrich, 1909; Moy-Thomas, 1939;(pristoids, torpedinoids, and rhinobatoids) were
Melouk, 1954), pristiophorids + rajiforms examined because the monophyly of rajiforms
(Hasse, 1879), and squaloids + rajiforms (Isel-is highly corroborated (Compagno, 1977;
st6ger, 1937). Morphologically, Squatina agreesHeemstra and Smith, 1980; Nishida, 1989).
with rajiforms, squaloids (and/or their relatedAmong other living sharklike taxa, Orectolobus
groups), and some galeoids in various aspects and Heterodontus were examined because they
and is characterized by several unique features.
have been proposed as close relatives of Squatina
Squatina has a very long palaeontological his- by Holmgren (1941) and Norman (1966). Some
tory that can be traced back to the Upper Ju-other specimens of orectoloboid, lamnoid, and
rassic (Schweizer, 1964; Thies, 1983). Thesecarcharhinoid species were also studied to sup-
points of view suggest that Squatina might beplement the galeoid information.
an isolated lineage, derived from the neosela- External, skeletal, and muscular systems of
chian base as suggested by Compagno (1973,whole sharks and rays were examined. Illustra-
1977), who placed Squatina in the superorder tions were made using camera lucida images of
Squatinomorphii, apart from his other three specimens stained by alcian blue (Dingerkus and
major groups. Uhler, 1977) and then dissected.
The aim of this study, to elucidate the phy- The character transformation of Squatina and

? 1992 by the American Society of Ichthyologists and Herpetologists

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 506 COPEIA, 1992, NO. 2

its related groups was established

considerable by
variation of shark outgr
morphology
comparison (Nelson and Platnick,
(Schaeffer, 1981;
1967; Compagno, 1973), Wile
or because
1981). Because the higher phylogenetic
of the lack of fram
an apomorphic character shared
work of living elasmobranchs is 1977;
by all sharks (Compagno, still contro
Maisey, 1984a).
Two synapomorphies
sial, the functional ingroup have been
(FIG: proposed to a
Watrous
Wheeler, 1981) was unite postulated on of
all sharks: the presence the basi
an occipital
information extracted from fossil euselachians hemicentrum and a layer of parallelfibered
plus xenacanths that have been considered enameloid (PFE) in the teeth (Compagno, 1973;
closely related to modern taxa (Schaeffer and Thies, 1983; Maisey, 1984a, 1985). However,
Williams, 1977; Maisey, 1984b; Cappetta, 1987). as discussed in the following section, the pres-
The character change within FIG was polarized ence of an occipital hemicentrum is most likely
in comparison with the rest of living elasmo- symplesiomorphic at the modern level; and, ac-
branchs (functional outgroups: FOGs) only when cording to Maisey (1984a), "PFE is absent in
characters did not vary among FOGs because living Heterodontus teeth, and not all batoid
the relationships among the FIG and FOGs can- groups have been examined."
not be decided beforehand.
(2) Squatina plus some groups of galeoids:
Terminology follows mainly Bigelow and Norman (1966) brought Squatina, Heterodontus,
Schroeder (1948, 1953) for external morphol- squaloids, and pristiophorids together under the
ogy, Edgeworth (1935) and Holmgren (1941) same Squaloidea; and Holmgren (1941) pro-
for cranial structure, and Daniel (1934) for posed
the a sister-group relationship between Squat-
other characters. Institutional abbreviations ina and orectolobids. Norman's Squaloidea was
follow Leviton et al. (1985) with one addition: characterized by having dorsal-fin spines and a
MSM = Marine Science Museum, Tokai Uni- simple (not tridentate) rostral process. Dorsal-
versity, Shimizu. Unless otherwise indicated, the
fin spines were, however, considered to have
following names of higher taxa are applied: raji-
been lost in the several lineages of neoselachians
form refers to all the skates and rays, synony-(Hubbs and McHugh, 1951; Compagno, 1973;
mous with Batoidea (Compagno, 1973, 1977) Maisey, 1978). A simple rostral process is not
and Batomorphii (Cappetta, 1980), and the fiveonly possessed by other living taxa such as
suborders of rajiforms follow Bigelow andChlamydoselachus, hexanchoids, and rajiforms
Schroeder (1953); squaloid is used according to but is considered to be rather primitive in neo-
Bigelow and Schroeder (1948); hexanchoid ex-
selachians (Compagno, 1977, 1988; Maisey,
cludes Chlamydoselachus; galeoid (White, 1937; 1984a). Although Holmgren's (1941) hypoth-
Bigelow and Schroeder, 1948) refers to car-esis was evidenced by several common features
charhinoids + lamnoids + orectoloboids; orec-in the neurocranium, recent authors (Compag-
tolobids and hemiscylliids are applied following
no, 1973; Applegate, 1972; Dingerkus, 1986)
Applegate (1972). have rejected his idea because of the analogies
of these characters and the closer kinship be-
DEFINITION OF INGROUP tween orectolobids and other orectoloboid
members. Their discussion is enough to deny
The FIG of this study is the monophyletic
the possibility of relationship between Squatina
group comprising Squatina and its related and any galeomorph shark taxon.
group(s). To define the FIG, previous ideas of
(3) Squatina plus squaloids (with or without
elasmobranch phylogeny must be evaluated. The
pristiophorids): The groups closely related to
following five groupings might be considered
Squatina have long been generally considered
candidates for a FIG.
to be squaloids and pristiophorids (e.g., the
(1) A group comprising all shark taxa: Mostfourth shark group of Miiller and Henle, 1841,
previous systematic studies have regarded theSqualea of White, 1937, and Squaliformes of
sharks as an essentially different group fromBerg,
all 1940). However, some cranial structures
the skates and rays; for example, Selachoidei
suggest a close relationship among squaloids,
(Giinther, 1870), Pleurotremata (Regan, 1906),
hexanchoids, and Chlamydoselachus (Holmgren,
and Antacea (Garman, 1913). In other words,
1941; Compagno, 1977; Maisey, 1980). Mono-
the morphological peculiarity of rajiforms wasphyly of Squatina + squaloids thus cannot be
supported.
the basis for the traditional dichotomous system
since Linnaeus. Such a taxonomic system has(4) Squatina and rajiforms: Goodrich (1909),
been refuted by recent authors because of the Moy-Thomas (1939), and Melouk (1954) con-

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 SHIRAI-SQUATINID PHYLOGENY 507

sidered that Squatina was closely related FOG

to raji- FIG
I 1
forms on the basis of their specific similarity. / ;
HYPNOSOUALEAN
However, Squatina-rajiform relationships are GROUP

rather equivocal as discussed by Compagno

(1973, 1977) and Maisey (1984a). It is at least
not beneficial for the elucidation of elasmo-
branch phylogeny if these two groups are hy-
pothesized to be monophyletic beforehand.
(5) Orbitostylic group of Maisey (1980): This
group, comprising squaloids, Squatina, hexan-
choids, and Chlamydoselachus, is based on the
8-11
presence of an orbital process and some other
but not definitive characters (Maisey, 1980,
1984a). The orbitostylic group is monophyletic 3-7
if the proposed close relationships among raji-
forms and several shark taxa of the orbitostylic
group (e.g., pristiophorids, Squatina, and the 1-2
squaloid Deania) can be denied. A close kinship
among rajiforms and certain shark taxa should
now be reconsidered (Compagno, 1977; Mai-
(neoselachian base)

sey, 1984a, 1985). Fig. 1. Cladogram showing proposed relation-

Any higher taxa are thus not appropriate toof the hypnosqualean group with related taxa.
ships
the FIG of this study, and a nontaxonomical
Closed circles indicate hypothesized synapomorphies;
FIG = functional ingroup; FOG = functional out-
group including Squatina must be assumed here.
groups.
I hypothesize a monophyletic group composed
of the orbitostylic group and rajiforms as an
alternative idea (Node I in Fig. 1). This subotic
un- shelf of galeoids (Holmgren, 1940). Be-
named taxon was suggested by Maisey (1984a) cause the Mesozoic fossil elasmobranchs (cten-
acanthoids, hybodontoids, and/or xenacan-
based on the agglomeration of orbitostylic group
and the close relationships among a part of them
thids, which have been recently considered the
and rajiforms. The orbitostylic-rajiform con-
close relatives of the modern neoselachians) have
nection demands the assumption that the or- the suborbital shelf as the basic plan (e.g.,
bital process has been secondarily lost in raji-
Schaeffer, 1981; Thies, 1983; Maisey, 1984b),
forms, and there is no direct evidence for it
themust have been lost at the level of modern
newly hypothesized group. However, the fol- taxa.

lowing two characters support this idea (in theMany previous authors have recognized
analysis that follows, characters numberedsuborbital
as shelf in Squatina (e.g., Iselst
they occur as synapomorphies in the clado-
1937; Melouk, 1954; Compagno, 1973).
gram): ina has the shelflike expansion (sos?) at t
(1) Suborbital shelf absent: The suborbital terior part of the orbit, and it is aberrant
shelf (sos) is a basic structure of heterodontoids veloped (Fig. 2C). It is, however, not too
and galeoids (Fig. 2A; White, 1937; Holmgren, to say that this is similar to the suborbita
1941; Compagno, 1973) and it supports the of heterodontoids, galeoids, and Mesozoic
cranio-palatine articulation posteromedially. taxa only in relative size. Squatina has a te
The suborbital shelf continues to the ventro- mouth like many Mesozoic fossil el
lateral edge of auditory capsule (subotic shelf branchs,
= but it is supported by a differe
ternal structure from those of the latter
sots), which is pierced by the orbital artery. The
species of FIG (Fig. 2B) have no suborbital shelf,
is represented by the cranio-palatine art
but the basitrabecular process (btp) for the sup-tion, with the developed orbital process,
port of the cranio-palatine articulation is pres-is shared by the orbitostylic group of M
ent. A low expansion or process, pierced by the(1980). In Squatina (Fig. 2C-D), there is
orbital artery (sotp; the foramen for orbital ar-siderably elongated palatoquadrate (pq), w
tery is often absent as in Fig. 2B), is completely
strongly inclined orbital process (op). Th
separate from the basitrabecular process, and palatine and the foramen for the carotid
it is formed through a different course of the (fca) are situated below the middle of the

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 508 COPEIA, 1992, NO. 2

pq/ ~

sso

fca/

sotp

sos? sots? Op

*fcac

Fig. 2. Basicranium showing cranio-palatine articulation: (A) Proscyllium venustum, HUMZ 49348, 538 mm
TL, ventral view; (B) Zameus squamulosus, HUMZ 75872, 526 mm TL, ventral view; (C) Squatina nebulosa,
HUMZ 40027, 369 mm TL, ventral view; (D) Lateral view of C. btp = basitrabecular process; fca = foramen
for carotid artery; foa = foramen for orbital artery; op = orbital process; pq = palatoquadrate; sos = suborbital
shelf; sotp = low expansion or process at suborbital region; sots = subotic shelf. Scale bars = 10 mm.

and they are far anterior in comparison with articulation with the epibranchial of the suc-
those of other elasmobranchs. Moreover, the ceeding branchial arch (asterisk in Fig. 3D; Gar-
"suborbital shelf" of Squatina is wholly separate man, 1913). This projection should not be
from the subotic region (asterisk in Fig. 2D), equated with the pharyngobranchial blade be-
and it is the basic character of the basitrabecular cause it is situated at the proximal terminus of
process of FIG. These points suggest that thethe pharyngobranchials (somewhat apart from
terminal oral cleft of Squatina is derived, and itthe terminus in FOG) and because it is not re-
can be hypothesized that the internal features lated to the epibranchial longitudinal muscles.
of Squatina noted above are caused by a forwardIn the sharklike forms of FIG (Fig. 3B), anterior
expansion of basicranium. Therefore, the "sub-and succeeding branchial arches are connected
orbital shelf" of Squatina is not homologous to at least in part by the arculalis dorsalis, with two
the typical suborbital shelf of elasmobranchsheads of origin. The rajiform projection in
but is assumed to be homologous to the basi-question seems to be related to such a connec-
trabecular process of FIG. tion in sharks of the FIG.
(2) Bladelike expansion at base of pharyn-
gobranchials absent: In heterodontoids and ga- CHARACTER ANALYSIS
leoids, the pharyngobranchial blade (pbb), the
leaflike process near the proximal terminus of A phylogenetic hypothesis of relationships of
the pharyngobranchials, provides the origin forSquatina is presented in Figure 1. Synapomor-
the arcualis dorsalis (ad) and interpharyngo-phies at Nodes II and III are discussed in order,
branchialis (ipb; Fig. 3A). This is also the casepreceded by a brief description of the derived
in Hybodus cassagensis (Maisey, 1982, fig. 9), al- state. A monophyletic group comprising Squat-
though dorsal elements of branchial arches are ina, pristiophorids, and rajiforms is termed the
poorly preserved in fossil elasmobranchs. In the "hypnosqualean group" for the sake of con-
species within FIG, there is no similar structurevenience.
for these muscles (Fig. 3B-C), thus the pharyn-
gobranchial blade must have been lost in theNode II. Hypnosqualean Group (Squatina +
living forms.
Pristiophoridae + Rajiformes)
In pristoids, rhinobatoids, and torpedinoids, (3) Concavity for occipital hemicentrum ab-
the pharyngobranchial bears a projection for sent (Figs. 4-5): In modern shark taxa (Figs.

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 SHIRAI-SQUATINID PHYLOGENY 509

ipb

pbb ' "

vc
syn

Sbebl

eb3

Fig. 3. Dorsal part of branchial arches and musculature, left side: (A) Cirrhoscyllium japonicum, HUM
49866, 446 mm TL; (B) Centroscymnus owstoni, HUMZ 101723, 652 mm TL: (C) Rhinobatos hynnicepha
HUMZ 10062, 297 mm TL. ad = arcualis dorsalis; eb = epibranchial; ipb = interpharyngobranchialis; p
pharyngobranchial; pbb = pharyngobranchial blade; syn = synarcual; vc = vertebral column. Scale bars
10 mm.

Smag

1 .5

ohc c syn::

It, 401

- - - - - - -

ohc,

. .. . . ..

Otr.
oc oc:X

Fig. 4. Median aspect of th

95177, 584 mm, TL; (B) He
250 mm TL; (D) Squatina
387 mm TL. c = vertebral
occipital condyle; ohc = oc

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510 COPEIA, 1992, NO. 2

thm . ?. 7
P . ." .' . . ... ..... .... . ." . . .

OC

!:i !'
hhm
bvp
a hm
. ohoc
? -I; ? ,"
bvp /ohc
i''' ...

bvpp
synm
., h
' .." ":;g,.t'
W. ohc
"'!':I"'?
Tobvp

4,; .- .

?. e?

":.........,,.....

Fig. 5. Radiographs of the cranio-vertebral conjunction, showing t

(A) Miroscyllium sheikoi, BSKU 26161, 337 mm TL; (B) Orectolobusj
Narcine timlei, HUMZ 37675, 282 mm TL; (D) Squatina africana, FSF
cirratus, FSFL-EA681, 783 mm TL. bvp = basiventral process; hm =
see Figure 4. Scale bars = 10 mm.

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 SHIRAI-SQUATINID PHYLOGENY 511

4: O
?I:?

?:~C
:
SC '''
;i:
?s ?,i~1?? ?
?~
.?:.:??:J
?,,
: ~?;.t~'
'

P ???-.~?.
?ti r\F Fi; .,..,
.~~ i ?:r:?. ~
::?? ???
..S
... ??: ?S
ti
?,. ..
?'??
?;?? " .i .... ??;.??
I ?;cr?~ .~C '' ': '`" t? .. ?,. liW : -t
~'

~ ?P ::::
I .'S'.... '.
?
.. P '
I

C~I-?." 'a
- O
I? t P
??-

~??
\
?.?-
??, ?? O
Ulr~~ ??-r. s,~? ?. ~-'f?-~l? . ??'?...

~C ?~~:* i'
C i::?'.?
r ~cl I(.????;;:

r- ?.;9??~:
.S
"'~ ,?
ii:i~Pi?
.?.:. "??( j

'?????1:e.
it .??. '.??? ?: ~iz
:i~n???' ~t .d '
2::5 ~, ??: S -::
r? .-.:
f. ?:~:?-
P?

Fig. 6. Lateral aspect of right scapulo-coracoid showing the condyles for pectoral basals: (A) Proscyllium
venustum, HUMZ 49348, 538 mm TL; (B) Centroscyllium excelsum, HUMZ 69275, 588 mm TL; (C) Torpedo
tokionis, HUMZ 79517, 250 mm TL; (D) Squatina japonica, HUMZ 91670, 505 mm TL; (E) Pristiophorus
nudipinnis, FSFL-EA735, 878 mm TL. p = propterygium; s = mesopterygium; sc = scapulo-coracoid; t
metapterygium. Scale bars = 5 mm.

4A-B, 5A-B), an unpaired cone-shaped con- between the occipital condyle and the basiven-
cavity is generally situated just below the fora- tral process of first vertebra.
men magnum (mag) and is filled with the cal- Because the absence of a basioccipital fovea
cified or noncalcified centrum (occipital is confined to hypnosqualean members, it is as-
hemicentrum = ohc); this concavity is termed sumed to be derived among living forms. Pris-
the basioccipital fovea. The cranio-vertebral tiophorids and rajiforms share the absence of
conjunction is supported by an articulation be- an occipital hemicentrum, which represents a
tween the occipital hemicentrum and the first further derived state (Character 8).
vertebral centrum, with or without the other (4) Separate condyle for pectoral propterygi-
one between the occipital condyle (oc) and the um present (Fig. 6): In modern shark taxa, the
basiventral process of first vertebra (bvp). In scapulocoracoid (sc) generally possesses a single
rajiforms (Figs. 4C, 5C), several anterior ver- ridgelike (Fig. 6A) or humplike condyle (Fig.
tebrae are fused into the synarcual (syn), and 6B) that articulates with pectoral basal carti-
there is neither a basioccipital fovea nor an oc-
lages. In rajiforms (Fig. 6C), there are three or
cipital hemicentrum. Such differences have been more condyles, and each basal cartilage has its
said to be clear-cut distinction between sharks own separate condyle (e.g., Ishihara and Ishiya-
and rays (Compagno, 1973; Maisey, 1984a). ma, 1986; McEachran and Miyake, 1986; Nish-
However, the basioccipital fovea is also absent ida, 1989). Squatina (Fig. 6D) has two large con-
in Squatina (Figs. 4D, 5D) and pristiophorids dyles, one for the metapterygium (t) and the
(Figs. 4E, 5E). In Squatina, a poorly calcified other for the propterygium (p) and mesopteryg-
portion (ohc), probably homologous to the oc- ium (s). Pristiophorids (Fig. 6E) possess a small
cipital hemicentrum, is attached to the poste- but distinctly separate condyle for the propter-
rior extremity of the basicranium; but in pris- ygium, and two larger condyles for the mesopte-
tiophorids, there is no centrumlike piece rygium and metapterygium, as in rajiforms.
between the neurocranium and the first verte- Because the FOG has a single pectoral con-
bra. The cranio-vertebral conjunction of thedyle, the presence of a separate condyle for the
hypnosqualean group consists of an articulation metapterygium is derived at the level of modern

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512 COPEIA, 1992, NO. 2

sn

dfr

sor

bp'.
bpp

id "(?iI
EPAXIA

sn:l .i~,: ?; ~
...... ..... . . '

Fig. 7. Dorsal-fin skeletons and mus

acanthias, HUMZ 87733, 495 mm TL;
japonica, HUMZ 91670, 505 mm TL. (D
HUMZ 40027 (370 mm TL). (E-F) Sche
the hypnosqualean group and (F) sq
inclinator dorsalis; psr = prespinal ra

euselachians. One more

(6) Inclinator dorsalis directlyseparated
arising from
the propterygium may
vertebra (Fig. 7): have
In most shark taxa, the incli- bee
pristiophorids and
nator dorsalisrajiforms
(id) arises from the basipterygium (Cha
(5) Supraneurals enlarged
(bp) of the dorsal fin and from the dorsal(at side lea
of dorsal fins of(Fig. 7):(Fig.In
the epaxial musculature the
7F). In the hyp- hy
group (Fig. 7B, nosqualean
C), group, the supraneura
the platelike basipterygia of
ral spine" of Daniel,
the dorsal fins are1934) are
wholly attached to the dorsal usu
panded to formsidea large
of the plate
vertebrae (Fig. 7B-C), and the origin on t
column, immediately inliesfront
of the inclinator dorsalis deeply between the of t
Because the supraneural is absent
neural arches and the epaxial musculature (Fig.
FOG (e.g., Hasse,
7D-E). In 1882;
heterodontoids and Ridewood
some squaloids
iel, 1934), the enlarged supraneur
with developed fin spines supported by verte-
for the hypnosqualean group.
brae (Fig. 7A), the inclinator dorsalis is not re- It i
lated to the vertebral
reduced secondarily in higher column. Thus, the de-rajif
(K. Nishida, pers. comm.).
veloped dorsal-fin Two
muscle in hypnosqualeans
era, Squalus
andmust
Cirrhigaleus,
have been acquired within the FIG. hav
quadrate cartilages (psr
(7) Flexor caudalis extending= "presp
anteriorly into
Holmgren, 1941) the precaudal
preceding region (Fig. 8): In thethe FOG, se
fin spine (Fig. 7A). It is
Chlamydoselachus, uncertain
hexanchoids, and squaloids,
cartilages of squaloids
the flexor caudalis share the
(fx) is confined to the caudal sam
the supraneurals of
fin and inserts ontohypnosqual
the distal ends of elongated
cussion). haemal processes (hp) of the caudal vertebrae

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 SHIRAI-SQUATINID PHYLOGENY 513

ucl

'I i

fL~~ _ _ .\. . . . . . . . . . .:?

hp c

?f

Fig. 8. Development of flexor caudalis and the haemal processes of vertebrae: (A) Prist
FSFL-EA735, 878 mm TL, ventrolateral aspect (portion of musculature removed to sh
vertebrae); (B) Isistius (schematic diagram), vertebrae at precaudal and caudal regions
of flexor caudalis; (C) Squatina, same as (B). fx = flexor caudalis; hp = haemal proc
lobe; Ik = precaudal longitudinal keel; ucl = upper caudal lobe. Scale bar = 10 mm.

(Fig. 8B). In rajiforms with a lobelikedepressed

caudal fin,
dorsoventrally and has two art
pristiophorids, and Squatina, this muscle
condylesex-
that fit into two divided articul
tends anteriorly to the precaudal region and
sae (hmf) in the auditory region (Fig. 9A
inserts onto the distal ends of the haemal pro-
character has been pointed out as a raylik
cess, which are as elongated as those of the cau-
dition by Hoffman (1913), Holmgren (
dal vertebrae (Fig. 8A, C). The precaudal hae-
and Compagno (1973). In the FOG, Chla
mal process of the FOG, Chlamydoselachus,
selachus, hexanchoids, squaloids, and Squa
hexanchoids, and most squaloids are the
distinctly
hyomandibula is compressed anteropo
shorter than those of the caudal finriorly
(Fig. 8B);
and is characterized by a single ar
Squalus and Cirrhigaleus exceptionallycondyle.
have hyp-Based on outgroup comparison
nosqualean-like, elongated precaudal haemal
articular condyles and facets are a derive
processes, but the flexor caudalis of dition.
these taxa
does not extend into the precaudal region.
(10) Based
Coraco-hyomandibularis present
on the condition of the FOG, the 10):
elongated
The coraco-hyomandibularis (cohm
flexor caudalis is regarded as a synapomorphy
ally arises from the fascia of the rectus c
of the hypnosqualean group. (jrc =joint between coraco-arcuales and co
hyoideus)
Node III. Pristiophoridae + Rajiformes and inserts into the distal end o
mandibula by a long and tough tendon
(8) Occipital hemicentrum completely absent
10A). This muscle has so far been known
(Figs. 4-5): Most living sharks possess ina rajiform
skeletal taxa (Marion, 1905; Edgew
element for the conjunction between1935), the cra-
but pristiophorids have it also (Fig.
nium and the first vertebra, such as the occipital
In other shark taxa (Fig. 10C), this specia
hemicentrum and a poorly calcified muscle
element is in
absent, but a muscle arising fro
Squatina. This is absent in all rajiforms andposition
same pris- as the coraco-hyomandibular
tiophorids. See Character 3. serts onto the joint between the basihyal
(9) Dual ball and socket articulationand
between
ceratohyal (ch) as the coraco-branchi
hyomandibula and auditory region (Fig. (cob 9):
1). In
Based on the condition of the FO
pristiophorids and rajiforms, the proximal part
coraco-hyomandibularis is regarded as de
of the hyomandibula (hm) is relatively among
flat orFIG (see Discussion).

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 514 COPEIA, 1992, NO. 2

. ... ...
hmf h ih

hm
cohm
cohy

f hy
mc
dhm

bh cohm

ohy
cobl
cohy

Fig. 9. (A) Cranium, and mandibular and hyoid arches of pristiophorids showing the jaw suspension; solid
lines are articulations between elements, dotted line indicates mandibulo-hyoid connection. (B-D) Schematic
diagrams of jaw protrusion of (B) pristiophorids, (C) rajiforms, and (D) squaloids. Element in half tone is hyoid
arch; solid lines represent muscles that function in jaw protrusion. In (C), basihyal, ceratohyal, and coraco-
hyoideus are omitted because these elements are not attached to hyomandibula in rajiforms. cob1 = coraco-
branchialis 1; cohm = coraco-hyomandibularis; cohy = coraco-hyoideus; cp = coronoid process; dhm =
depressor hyomandibularis; fcp = ligamentous fossa for coronoid process; hm = hyomandibula; hmf = fossae
for cranio-hyomandibular articulation; ih = interhyoideus; mc = mandibula; pq = palatoquadrate.

(11) A separate condyle for propterygium (Fig. toral fin with many radials, and no anal fin.
6): See Character 4. Although only conditions of the orbital process
and anal fin are probably derived for Squatina,
DISCUSSION squaloids, and pristiophorids, these are not val-
id synapomorphies for the following reasons.
I conclude that Squatina is the sister group ofThe orbital process articulates with the sub-
a monophyletic group composed of pristiopho- orbital region behind the optic foramen (di-
rids and rajiforms. This is evidenced by a shared
rectly below this foramen in the squaloid genus
cranio-vertebral connection (Character 3); ar- Echinorhinus). It is not homologous with the "or-
ticular facet of the pectoral-fin support (4); bital
de- process" of galeoids because there are at
velopment of supraneurals (5); origin of the least
in- two different ontogenetic means by which
clinator dorsalis (6); and development of thethe ascending process of palatoquadrate is
flexor caudalis (7). Three previous, alternate
formed (Holmgren, 1940; Jollie, 1971; Maisey,
hypotheses of Squatina relationships are refuted
1980); so, Compagno's (1988) "panorbitostylic
below.
hypothesis," which put forward the homoge-
neity of all the ascending process for the cranio-
Squatina-squaloid relationship.-As noted above,palatine articulation of shark taxa, does not have
many authors have considered Squatina to have a logical basis. The orbital process is recog-
a close kinship with squaloids and/or pristio- nized, however, not only in squaloids, Squatina,
phorids. These relationships are suggested by and pristiophorids but in Chlamydoselachus and
a number of characters: trough-shaped ros-
hexanchoids (Maisey, 1980, 1984a). Moreover,
trum, developed postorbital wall, more or lessnow we must also consider the secondary loss
elongated orbital process (sensu Maisey, 1980),of the orbital process in rajiforms because the
long otic capsule, large mesopterygium of pec- jaw suspension of skates and rays is not essen-

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 SHIRAI-SQUATINID PHYLOGENY 515

cohm hm cohy
bh b h hm

phb I?t~

'. 0oo
dhm
gco ---
\cohm

ire ih co
Ich -- \ jrchm
? ?
Fig. 10. Ventral aspect of ventral vis
@
Pristiophorus nudipinnis, FSFL-EA735
basihyal; gco = genio-coracoideus; hy =
phb = dorsal and ventral pseudohyoid

tially different Squatinactis; from Zangerl,

that 1973, 1981),
of which had a
shar
acters 9-10). These observations
strongly depressed body like living skates and
the hypothesis that rays, also makes
the thisorbital
hypothesis ratherpro uncer-
apomorphy for tain. the
Similarity of FIG of
the gill slits this
is also question-
Chlamydoselachus, hexanchoids,
able: although the gill slits of Squatina open sq ven-
the hypnosqualean trally in group.
part as in rajiforms, there is no essential
Absence of an anal difference infin
the external and internaldoes
also struc- n
a relationship between tures of the branchial Squatina
region between Squatinaa
(and/or pristiophorids). and other shark taxa. The The position
anal of dorsal
fi
in rajiforms, and fins this feature
is also ambiguous because many rathe
exceptions
izes squaloids and hypnosqualeans
can be enumerated in living euselachians, such
vious workers have maintained that the loss of as Rhina and Rhynchobatus (most forward dorsal
the anal fin must have occurred in two or more fins among skates and rays), or orectolobids and
lineages. Such a thought was probably basedhemiscylliids
on (far posterior among non-Squa-
the historical treatment of rays as a separate tina-rajiform groups). The condition of the anus
taxon from sharks. and the number of heart valves are recognized
as derived in my FIG-FOG analysis. However,
Squatina-rajiform relationship.-The Squatina-
these two affinities do not convert many synapo-
rajiform relationship is supported by a forwardmorphies among pristiophorids and rajiforms
extension of the pectoral fin and pectoral pro-into homoplasies.
pterygium directed anteriorly, gill slits openingA sister relationship between pristiophorids
ventrolaterally, anus separated from the ventral
and rajiforms is more plausible, and it is cor-
fins, posterior position of the dorsal fins (Good-
roborated by four synapomorphies (Characters
rich, 1909; Moy-Thomas, 1939; Melouk, 1954), 8-11). Of these, Characters 9 and 10 suggest
and the high number of heart valves (Marples, that they also share a similar mechanism of jaw
1936). These characters are, however, rather protrusion. In most shark taxa (Fig. 9D), the
equivocal as discussed by Compagno (1973, jaws are protruded by rotating the whole of
1977) and Maisey (1984a). Pectoral-fin condi- hyoid arch anteroventrally. This motion is
tion can be regarded as derived, but in Squatina
caused indirectly by the coraco-hyoideus and
there is neither the connection between the coraco-branchialis 1 pulling back the developed
propterygium and cranium nor the separatebasihyal and ceratohyal. In skates and rays (Fig.
9C), the hyomandibula is not rotated antero-
condyle for a pectoral propterygium (Character
11), both of which are characteristics of ventrally
raji- but is depressed ventrally by the cor-
forms. The similar pectoral basals of some Pa-
aco-hyomandibularis and depressor hyoman-
leozoic chondrichthyans (e.g., Janassa dibularis,
and which insert onto the hyomandibula.

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 516 COPEIA, 1992, NO. 2

The jaw suspension of ters pristiophorids

with hexanchoids and Chlamydoselachus
(Fig. 9B (or
is rather sharklike in the orbital articulation and
a part of them), e.g., relatively long jaws (Echi-
ligamentous attachment of the hyomandib-norhinus and Centroscyllium; Holmgren, 1941;
ula and coronoid process of the mandibula.Compagno, 1973) and subnasal fenestrae (Hep-
However, the double articular facets of the tranchias, Hexanchus, and many squaloid taxa;
cranio-hyomandibular connection, coraco-hyo-Holmgren, 1941; Compagno, 1973). Further-
mandibularis, and inter-hyoideus (probably ho-
more, as mentioned in Characters 5 and 7, hyp-
mologous to depressor hyomandibularis be-nosqualeans share some platelike supraneurals
cause of their origins and innervations; immediately in front of the second dorsal fin
Edgeworth, 1935) presumably make the hyo-and relatively long haemal spines at the poste-
mandibula depress ventrally to strongly pro- rior part of the precaudal region with two squa-
trude the jaws, a very raylike manner. Further-loid genera, Squalus and Cirrhigaleus. These facts
more, monophyly of pristiophorids and sugest that the sister group of hypnosqualeans
rajiforms can be supported by the conditions ofis confined to only a part of squaloids. The phy-
the antorbital cartilage, hypobranchial and ba- logenetic position of the hypnosqualean group
sibranchial skeletons, and tubelike snout pro- requires further comprehensive work.
cesses (e.g., Hoffman, 1913; Holmgren, 1941;
El-Toubi and Hamdy, 1959). These additional MATERIAL EXAMINED

characters were, however, not used in this study Squatinidae: Squatina japonica, HUMZ 91670; S. nebulosa, HUMZ
because modifications of these structures are 40027; S. africana, FSFL-V619, FSFL-EL205; S. oculata, USNM 222022;
too various among living elasmobranchs to S. argentina, FSFL-EM299; S. australis, FSFL-EA904;
eval-
EA947.
S. tergocellata, FSFL-

uate their polarities precisely. Pristoidei: Pristis microdon, USNM 081075.

Rhinobactoidei: Rhina ancylostoma, HUMZ 90897; Rhinobatos hynni-
cephalus, HUMZ 110062; Rhynchobatus djiddensis, HUMZ 6135. Tor-
Squatinomorphii of Compagno (1973).-Compag-
pedinoidei. Narcine maculata, HUMZ 37615; N. timlei, HUMZ 37675;
no (1973, 1977, 1984, 1988) considered Squa-
Torpedo tokionis, HUMZ 79517.
tina an isolated taxon among living sharks Pristiophoridae:
and Pliotrema warreni, RUSI 6225; Pristiophorus cirratus,
FSFL-EA681; P. japonicus, HUMZ 49349; P. nudipinnis, FSFL-EA735.
rays and placed them in the Squatinomorphii. Squalidae: Aculeola nigra HUMZ 90412, USNM 220266; Centrophorus
He explained the validity of his Squatinomor-
granulosus, USNM 220221; Centroscyllium fabricii, HUMZ 112559; C.
excelsum, HUMZ 69275; Centroscymnus coelolepis, USNM 206064; Cir-
phii as follows: it "combines a blend of batoid,
rhigaleus barbifer, HUMZ 95177; Dalatias licha, HUMZ 74603, HUMZ
squalomorphs, and a few galeomorph charac-
95229; Deania calcea, FRSKU-S 1662; Etmopterus spinax, FSFL-S348, SU
ters with many unique features, suggesting20617;
that Euprotomicrus bispinatus, SIO 76-233; Isistius brasiliensis, HUMZ
86585, HUMZ 89900; Miroscyllium sheikoi, HUMZ 74982, BSKU 26161;
the Squatinomorphii are an offshoot fromOxynotus
the centrina, FSFL-EI716; Scymnodon ringens, BMNH 1973:10.29:
euselachian base of three other groups" (Com-
28; Somniosus microcephalus, HUMZ 112816; Squaliolus laticaudus, HUMZ
74972; Squalus acanthias, HUMZ 87733, HUMZ 91533; Zameus squa-
pagno, 1973). His concept was probably based
mulosus, HUMZ 75872, HUMZ 95248.
on a balance of character distributions. Al- Echinorhinidae: Echinorhinus brucus, HUMZ 113400.

though his basic idea was "confirmed"Hexanchoidei:

in his Heptranchias perlo, HUMZ 101712; Hexanchus griseus,
HUMZ 95104; Notorynchus cepedianus, HUMZ 6749.
later cladistic work (Compagno, 1977), evi-
Chlamydoselachidae: Chlamydoselachus anguineus, MSM-88-40.
dence of it was not clarified. At least the balance Heterodontoidei: Heterodontus zebra, HUMZ 37666.
of character distributions is not suited to the Orectoloboidei: Chiloscyllium plagiosum, HUMZ 109476; Cirrhoscyl-
liumjaponicum, HUMZ 49866; Orectolobusjaponicus, HUMZ 113410.
cladistic methodology, and uniqueness doesLamnoidei:
not Alopias superciliosus, HUMZ 103753; Lamna nasus, HUMZ
necessarily mean phylogenetic independence
114045; Pseudocarcharias kamoharai, HUMZ 94348.
Carcharhinoidei: Atelomicterus macleayi, FSFL-T830; Cephaloscyllium
(Hennig, 1966). umbratile, HUMZ 35479; Mustelus manazo, HUMZ 105880; Prionace
glauca, HUMZ 88195; Proscyllium venustum, HUMZ 49348; Scyliorhinus
torazame, HUMZ 76078.
Phylogenetic position of the hypnosqualean group.-
The interrelationships among FIG taxa and the ACKNOWLEDGMENTS
higher framework of living elasmobranchs are
I express sincere appreciation to K. Amaoka
expressed as a cladogram in Figure 1. The hyp-
nosqualean group shares a single but distinct
and K. Nakaya who spent much time reading
apomorphic state with squaloids, the loss myof an
manuscript and discussing the conclusions
anal fin, but does not share any derivedofcon- my analysis. I also thank J. McEachran who
ditions exclusively with hexanchoids or Chla-
kindly undertook to read the manuscript twice
mydoselachus. However, despite considerable andef-
who pointed out much redundancy and in-
fort, monophyly of squaloids has not adequatebeen expression. J. Maisey gave me advice
elucidated (Maisey, 1980; Shirai, unpubl.). and
Somevaluable information on fossil chondrich-
squaloids share several plesiomorphic charac-
thyans. Materials for this study were loaned to

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 SHIRAI-SQUATINID PHYLOGENY 517

me by L. J. V. Compagno, W. N.F. Eschmeyer,

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