Syst. Biol. 48(3):455–490, 1999
The Position of Cetacea Within Mammalia: Phylogenetic Analysis of
Morphological Data from Extinct and Extant Taxa
1
MAUREEN A. O’LEARY1,3 AND JONATHAN H. GEISLER2
Department of Anatomical Sciences, State University of New York, Stony Brook, New York 11794-8081 ,
USA; E-mail: [email protected]
2
Department of Vertebrate Paleontology, American Museum of Natural History, New York, New York
10024-5192 , USA; E-mail: [email protected]
Abstract.— Knowledge of the phylogenetic position of the order Cetacea (whales, dolphins, and
porpoises) within Mammalia is of central importance to evolutionary biologists studying the transformations of biological form and function that accompanied the shift from fully terrestrial to fully
aquatic life in this clade. Phylogenies based on molecular data and those based on morphological
data both place cetaceans among ungulates but are incongruent in other respects. Morphologists argue that cetaceans are most closely related to mesonychians, an extinct group of terrestrial ungulates.
They have disagreed, however, as to whether Perissodactyla (odd-toed ungulates) or Artiodactyla
(even-toed ungulates) is the extant clade most closely related to Cetacea, and have long maintained that each of these orders is monophyletic. The great majority of molecule-based phylogenies
show, by contrast, not only that artiodactyls are the closest extant relatives of Cetacea, but also that
Artiodactyla is paraphyletic unless cetacean s are nested within it, often as the sister group of hippopotamids. We tested morphological evidence for several hypotheses concerning the sister taxon
relationships of Cetacea in a maximum parsimony analysis of 123 morphological characters from
10 extant and 30 extinct taxa. We advocate treating certain multistate characters as ordered because
such a procedure incorporates information about hierarchical morphological transformation. In
all most-parsimonious trees, whether multistate characters are ordered or unordered, Artiodactyla
is the extant sister taxon of Cetacea. With certain multistate characters ordered, the extinct clade
Mesonychia (Mesonychidae + Hapalodectidae) is the sister taxon of Cetacea, and Artiodactyla is
monophyletic. When all fossils are removed from the analysis, Artiodactyla is paraphyletic with
Cetacea nested inside, indicating that inclusion of mesonychians and other extinct stem taxa in a
phylogenetic analysis of the ungulate clade is integral to the recovery of artiodactyl monophyly.
Phylogenies derived from molecular data alone may risk recovering inconsistent branches because
of an inability to sample extinct clades, which by a conservative estimate, amount to 89% of the
ingroup. Addition of data from recently described astragali attributed to cetaceans does not overturn artiodactyl monophyly. [Artiodactyla; astragalus; Cetacea; fossils; homoplasy; Mesonychia;
morphology; phylogeny.]
The importance of fossils in phylogeny
reconstruction is most keenly appreciated
when a clade is of great antiquity and has
suffered numerous extinctions. Gauthier et
al. (1988), Donoghue et al. (1989), and Novacek (1992a, 1994) have emphasized that
under such circumstances, the importance
of fossils in phylogeny reconstruction can
outweigh the drawback of their incompleteness. These authors have shown that fossils
often capture the primitive morphotype of
a clade, because many fossil taxa have had
less time to evolve homoplasies than have
extant members of the same clades. Because
fossils often have combinations of primitive and derived features not found in extant taxa, they can be critical for untangling
3
Address correspondence to Dr. Maureen A.
O’Leary, Department of Anatomical Sciences, HSC T8 (040), SUNY at Stony Brook, Stony Brook, New York
11794–8081, USA.
problems of long-branch attraction, where
homoplasies masquerade as homologies.
Depending on the sampling of characters
and taxa, convergent similarities can have
the potential to draw taxa together phylogenetically, as in the celebrated example of
the paraphyletic clade “Haematothermia”
that links birds and mammals but excludes
crocodiles (Gauthier et al., 1988; Eernisse
and Kluge, 1993).
Mammalian systematists in particular
continue to spar (Catzeis, 1993; Graur,
1993a, 1993b; Novacek, 1993) over the signiŽcance of the often strongly differing tree
topologies that emerge from phylogenetic
analyses of data sets partitioned between
molecular and morphological data or between extinct and extant taxa. The problem
is exacerbated by different types of missing
data: phylogenies based on molecular data
cannot sample extinct taxa, and those based
455
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SYSTEMATIC BIOLOGY
on morphological data and drawing on fossil taxa cannot sample all morphological
characters, even from the most exquisitely
preserved fossils (Gauthier et al., 1988; Novacek, 1994; Simmons and Geisler, 1998).
The part of the mammalian tree relating
to the origin of Cetacea (whales, dolphins,
and porpoises) has been the subject of particular controversy of late because of differing results from phylogenetic analyses
based on molecular data and those based
on morphological data. Both types of analyses support the hypothesis that cetaceans are
nested within ungulates (Novacek, 1992b),
but there is virtually no agreement as to the
sister taxon of Cetacea or whether certain
ungulate clades close to Cetacea are monophyletic. Without knowledge of the sister
taxon of Cetacea, we cannot begin to understand the drastic anatomical and physiological transformations that occurred as terrestrial mammals returned to aquatic life and
evolved into some of the most specialized
known vertebrates.
Initial phylogenetic analyses of morphological evidence bearing on the question of cetacean origins nothwithstanding
(Prothero et al., 1988; Thewissen, 1994), a
comprehensive phylogenetic analysis testing morphological evidence for the monophyly of various modern ungulate orders
with respect to Cetacea has been conspicuously absent from the paleontological literature until recently (Geisler and O’Leary,
1997; Geisler and Luo, 1998). This is a serious
shortcoming, because detailed morphological analyses are an integral part of any total evidence analysis (Kluge, 1989; and references therein) combining molecular and
morphological data (also referred to as simultaneous analysis; Nixon and Carpenter, 1996). Lack of a comprehensive phylogenetic analysis of morphological data has
persisted despite the suggestion by some
molecular biologists that because of the “numerous extinctions along the stem lineage
of cetaceans, most major insights into the
transformation from a terrestrial ungulate to
a fully aquatic cetacean will come from fossil taxa” (Gatesy et al., 1996:960) . Here we
attempt to correct this shortcoming.
VOL. 48
BACKGROUND ON CETACEAN ORIGINS
Morphological Contributions
Morphologists at one time viewed understanding the phylogenetic relationships of
cetaceans to other orders of mammals as an
intractable problem because the anatomy of
cetaceans is so transformed relative to that
of other mammals (e.g., Simpson, 1945).
Within the last three decades, however, attributable in no small part to discoveries
of new fossils, paleontologists have developed the hypothesis that an extinct order of
carnivorous, hoofed mammals, the Mesonychia, is most closely related to Cetacea (Van
Valen, 1966, 1968, 1969, 1978; McKenna,
1975; Prothero et al., 1988; Thewissen, 1994;
Zhou et al., 1995; McKenna and Bell, 1997;
Geisler and Luo, 1998; O’Leary, 1998a). Van
Valen (1966) initially based this hypothesis on a variety of dental and cranial similarities. Mesonychians (Mesonychidae and
Hapalodectidae [but not Andrewsarchus; see
Van Valen, 1978; McKenna and Bell, 1997;
O’Leary, 1998a]) , a group that some paleontologists argue is paraphyletic (Thewissen,
1994; Geisler and Luo, 1998), are known
from the Early Tertiary of the Holarctic. Because they had hoofs, mesonychians have
generally been classiŽed among ungulates
(Van Valen, 1966), but they differ from
virtually all other ungulates in possessing
laterally compressed, homodont lower dentitions that are strongly suggestive of a carnivorous diet (Szalay and Gould, 1966; Szalay, 1969a, 1969b; Zhou et al., 1992; O’Leary
and Rose, 1995a, 1995b). McKenna (1975)
classiŽed Cetacea and Acreodi (Mesonychidae) together in the mirorder Cete within
the grandorder Ungulata, thereby formalizing morphological arguments advanced
by Van Valen (1966; see also McKenna and
Bell, 1997). Paleontologists have not argued
that mesonychians are nested among any of
the following ungulate clades that have extant members: Artiodactyla, the even-toed
hoofed mammals (ruminants, pigs, hippos, and camels); Perissodactyla, the oddtoed hoofed mammals (horses, rhinos and
tapirs); or among the paenungulates: Proboscidea (elephants), Hyracoidea (hyraxes),
and Sirenia (dugongs and manatees).
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
Initially, interpretations of morphological evidence for the extant clade most
closely related to Cetacea tended to converge on Perissodactyla or were simply ambiguous. Among more recent treatments,
Novacek (1982) placed cetaceans in an
unresolved polytomy with Artiodactyla,
Perissodactyla, and tentatively, Tubulidentata (aardvarks), with paenungulates as
the next most closely related clade. A
series of subsequent parsimony analyses
of the mammalian orders tackled more
precisely the morphological evidence for
cetacean–ungulate relationships. On the
basis of cranial traits, Novacek (1986)
found cetaceans to be related to ungulates in the following manner: Artiodactyla
(Cetacea (Perissodactyla (Hyracoids (Sirenians + Proboscideans))))–a result broadly
consistent with information from patterns
of variation in the stapedial artery (Wible,
1987). Novacek and Wyss (1986) and Novacek (1989) obtained similar results based
on morphological information from several
anatomical systems but introduced the possibility that Perissodactyla might be more
closely related to Cetacea than is Artiodactyla. In a study including a variety of
extinct “condylarths,” Prothero et al. (1988)
argued that Cetacea was the sister group of
Andrewsarchus and that, of the extant ungulate orders, Perissodactyla was most closely
related to Cetacea. Their tree, however, may
not be the most–parsimonious explanation
of their data because these authors did not
perform a parsimony analysis on their entire data set. Thus, phylogenetic analyses of
morphological data initially tended to favor
a close relationship between paenungulates ,
perissodactyls, and Cetacea but were unable
to demonstrate this relationship with great
certainty.
In many of the studies described above,
monophyly of Artiodactyla was assumed
and not tested. The assumption that Artiodactyla is monophyletic originates primarily from the observation that artiodactyls
share an ankle joint morphology known as
the double-pulleyed astragalus (Schaeffer,
1947; Vaughan, 1986) (Fig. 1), a unique condition. This skeletal feature is one of the few
characters that can be directly veriŽed in
457
both extant and extinct forms, and its presence has been the primary criterion for membership in the order, particularly for fossil taxa. The signiŽcance of the artiodactyl
ankle is that it restricts the distal hindlimb
to parasagittal motion and is thought to be
less likely to dislocate as the animal engages in high–speed quadrupedal running
across a terrestrial substrate (Schaeffer, 1947;
O’Leary and Rose, 1995b). Despite the broad
radiation of this group, the morphology of
this joint has remained remarkably constant
since its Žrst known appearance (Schaeffer,
1947) at the base of the Eocene ( ~ 55 million
years ago). Figure 1 shows the astragali of
various mammals associated with the basal
ungulate radiation. Relatively unspecialized
Early Tertiary mammals like Chriacus have
an astragalus with a relatively at proximal end (trochlea) and a convex distal end
(head). The astragalus of Phenacodus, a more
derived ungulate, has a convex head but
a grooved trochlea. Artiodactyls, perissodactyls, and some mesonychians also have
a relatively grooved trochlea. These taxa
differ, however, in the structure of the astragalar head, speciŽcally in its articular
facet for the navicular, and each morphology is thought to be a convergent specialization for cursorial locomotion (O’Leary
and Rose, 1995b). Both perissodactyls and
mesonychians exhibit a saddle-shaped head
(O’Leary and Rose, 1995b) but differ in that
mesonychians have a distinct facet for the
cuboid. Artiodactyls have a deeply grooved
head with a more substantial cuboid articulation (e.g., Bunophorus [Fig. 1]; Schaeffer, 1947). Despite variations in body size
and locomotor capabilities among artiodactyls, the morphology of the astragalus
remains a diagnostic feature of the order
(Schaeffer, 1947; Vaughan, 1986). Stem taxa
outside of Artiodactyla exhibiting transitional morphologies leading to the primitive
artiodactyl morphotype remain virtually
unknown (Rose, 1987, 1996). A complete
astragalus associated with other diagnostic material of a very primitive cetacean
has never been described (Milinkovitch and
Thewissen, 1997). For the archaic cetacean,
Ambulocetus, the taxon for which we have
the most detailed knowledge of skeletal
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SYSTEMATIC BIOLOGY
VOL. 48
FIGURE 1. Right astragali of Early Tertiary mammals associated with the basal ungulate radiation: the proximal end of the astragalus (trochlea); the articular facet for the distal tibia (character 109), towards the top of each
drawing; the distal end of the astragalus (head); the articular facet for the navicular; and sometimes the cuboid
(characters 104 and 106), towards the bottom of the page. Chriacus (AMNH-VP 92832) , an oxyclaenid arctocyonid
(morphology resembles that of Arctocyon coded in this analysis); Phenacodus (AMNH-VP 15287), a stem taxon
to extant perissodactyls; Dissacus (AMNH-VP 3359) and Pachyaena (AMNH 16154), mesonychians; Bunophorus
(AMNH-VP 92847), an artiodactyl (morphology resembles that of Diacodexis coded in this analysis, representative
of the artiodactyl double-pulleyed astragalus); Heptodon (AMNH-VP 95866), a perissodactyl; and Ambulocetus
(H-GSP 18507) , an archaic cetacean (redrawn from Thewissen et al., 1996). The head and part of the trochlea of
the Ambulocetus astragalus are not preserved in this specimen. Scale bar = 10 mm.
anatomy, only the proximal astragalus is
known (Fig. 1). It has a grooved trochlea
that distinguishes it from generalized mammals such as Chriacus and Arctocyon, but
the more diagnostic head is not preserved.
Two partial astragali have recently been attributed to the archaic cetaceans Ambulocetus
and Pakicetus on the basis of their grooved
trochleae, large size, and faunal associations
(Thewissen et al., 1998). The authors interpret these bones as possessing certain derived similarities that might link cetaceans
to artiodactyls but not to mesonychians but
qualify their argument by stating that these
“cetacean” astragali do not have trochleated
heads as in artiodactyls. Because these fossils are fragmentary and are not associated
with diagnostic cetacean material, we continue to consider the morphology of the
cetacean astragalus to be relatively poorly
established.
Three other relatively recent fossil discoveries also suggest the possibility of a close
link between Cetacea and Artiodactyla. The
hind foot of the archaic cetacean Basilosaurus
(Gingerich et al., 1990) exhibits a paraxonic
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
condition (i.e., the axis of symmetry passes
between the third and fourth digits), a feature consistent with a close phylogenetic
relationship between cetaceans and both
Mesonychia and Artiodactyla. The morphology of the incus of another archaic
cetacean, Pakicetus (Thewissen and Hussain, 1993), has been argued to support a
close relationship between Artiodactyla and
Cetacea, as have features of the skeleton of a
third archaic cetacean Ambulocetus (Thewissen et al., 1994, 1996), such as hoofs and a
paraxonic foot, which reinforce a link with
Mesonychidae as well.
Thewissen (1994) conducted the Žrst parsimony analysis of morphological data bearing on the question of cetacean origins and
identiŽed several dental synapomorphies
supporting a sister-taxon relationship between cetaceans and certain mesonychids.
He found Mesonychia (Mesonychidae + Hapalodectidae) and Mesonychidae to be paraphyletic with respect to Cetacea and, in
contrast to Thewissen and Hussain (1993),
argued that the extant sister taxon to Cetacea
was Perissodactyla, a hypothesis championed by Prothero (1993) as well. Thewissen’s (1994) analysis did not directly test
monophyly of Artiodactyla because it included only one artiodactyl, Diacodexis.
However, when Geisler and O’Leary (1997)
and Geisler and Luo (1998) included several artiodactyls in parsimony analyses of
morphological data, support emerged for a
clade that included Artiodactyla, Cetacea,
and Mesonychia to the exclusion of Perissodactyla, and for monophyly of Artiodactyla,
Perissodactyla, Cetacea, and Mesonychidae. New dentitions of archaic cetaceans led
O’Leary (1998a) to argue that Mesonychidae and Mesonychia are each monophyletic
clades (in contrast to Prothero et al., 1988;
Thewissen, 1994), the former being nested
within the latter. Our work here represents
a combination and expansion of these most
recent phylogenetic analyses.
Molecular Contributions
Like morphological analyses, molecular
analyses of cetacean origins have varied in
their taxon and character sampling, methods of phylogenetic reconstruction, and
459
ultimately in their conclusions. Some initial parsimony analyses of amino acid sequences (Goodman et al., 1985; Miyamoto
and Goodman, 1986) or of a combination
of amino acid sequences, immunodiffusion,
and morphology (Shoshani, 1986) generally revealed no greater resolution than
that Cetacea formed a clade with Artiodactyla and Perissodactyla. Evidence supporting a close relationship between Perissodactyla and Cetacea to the exclusion of
Artiodactyla emerged from parsimony analyses of amino acid sequences of eye lens proteins (De Jong, 1985; McKenna, 1992), and
from analysis of a combination of nuclear
gene sequences and amino acid sequences
(Stanhope et al., 1993). This last result has
been among the minority of results based
on molecular data. The molecule-based hypothesis that Artiodactyla is the closest living relative of Cetacea was Žrst put forth on
the basis of serological precipitin tests (Boyden and Gemeroy, 1950). Maximum parsimony analyses of amino acid sequences of a
and b hemoglobin chains (Shoshani et al.,
1985; Czelusniak et al., 1990b), pancreatic
ribonucleases (Beintema et al., 1986, 1988),
and a combination of eight different types
of amino acid sequences (Czelusniak et al.,
1990a) also showed that Cetacea grouped
more closely with artiodactyls than with
perissodactyls.
Several molecular analyses, however, began to recover phylogenies with Cetacea
nested within Artiodactyla, a highly controversial result from a morphological perspective, given the reknowned monophyly
of Artiodactyla. Czelusniak et al. (1990b)
recovered a clade of cetaceans and pecorans (deer, sheep, giraffe, and their close
relatives) to the exclusion of other artiodactyls in maximum parsimony analyses of
amino acid sequences. They qualiŽed their
result as likely to be “phylogenetically incorrect” (Czelusniak et al., 1990b:614) because the new topology differed from established ideas of relationships and was based
only on a small subset of all molecular evidence. Using a combination of amino acid
and nucleotide sequences for 18 artiodactyls
(including Hippopotamus, camels, suids, and
pecorans, a fair representation of taxonomic
460
SYSTEMATIC BIOLOGY
variation within Artiodactyla), Czelusniak
et al. (1990a) found some evidence for artiodactyl paraphyly, but equally parsimonious
trees also supported artiodactyl monophyly.
Their cautious interpretations of trees supporting artiodactyl paraphyly were not followed by other researchers examining nucleotide sequence data.
Parsimony analyses of nucleotide sequence data of the mitochondrial cytochrome b gene (Árnason et al., 1991)
and of the 12S and 16S ribosomal genes
(Milinkovitch et al., 1993) recovered a sistertaxon relationship between Artiodactyla
and Cetacea to the exclusion of Perissodactyla, based on relatively small samples
of artiodactyls (1 to 3 taxa). Increasing the
artiodactyl sample to 11 taxa for mitochondrial cytochrome b gene sequences, Irwin
et al. (1991) recovered a paraphyletic Artiodactyla with Cetacea nested inside as
the sister taxon of camels. A sister taxon
relationship between Cetacea and ruminants resulted from parsimony analyses of
combined nucleotide sequences of both cytochrome b and cytochrome c oxidase subunit II (Honeycutt et al., 1995) and received
mixed support from nuclear gene sequences
(Stanhope et al., 1996). Graur and Higgins
(1994) analyzed 11 nuclear-encoded protein
sequences and Žve mitochondrial DNA sequences in four taxa, using maximum likelihood (with the assumption of constant
rates of substitution [Hasegawa and Adachi,
1996]), neighbor joining, and maximum parsimony, and found that Cetacea was the sister group of the cow to the exclusion of
pigs and camels. They advocated revisions
to mammalian ordinal-level taxa to formalize their result, despite its genesis from relatively poor taxonomic sampling.
Others criticized the four-taxon method of
Graur and Higgins (1994), recognizing that
it risks recovering “robust, but false relationships” (Philippe and Douzery, 1994:149; see
also Adachi and Hasegawa, 1996) because
of such confounding factors as long-branch
attraction. Authors of other nucleotide sequence analyses that had recovered artiodactyl paraphyly (Queralt et al., 1995; Smith
et al., 1996) qualiŽed their results as tentative, sensitive to such variables as outgroup
VOL. 48
choice and ingroup sampling, and possibly
reective of the unique evolutionary history
of a particular gene but not of the clades in
question. Hasegawa and Adachi (1996) reexamined the data sets of both Graur and Higgins (1994) and Irwin and Árnason (1994),
combined with hemoglobin sequences, using a maximum-likelihood analysis with
a rate heterogenous model for nucleotide
substitution. They found greatly reduced
statistical support for artiodactyl paraphyly
but still achieved that result. This suggested
to them that artiodactyl monophyly is a viable alternative hypothesis that could not
be dismissed until more genes had been
examined.
None of the above nucleotide sequence
analyses included hippopotamids in the
sample of artiodactyls, and none explicitly
tested the effect of this group of artiodactyls
on tree topology. Once hippopotamids were
included with 11 other artiodactyls in a parsimony analysis of nucleotide and amino
acid sequences of the cytochrome b gene,
hippopotamids formed a clade with Cetacea
to the exclusion of other artiodactyls (Irwin and Árnason, 1994). Gatesy et al. (1996)
found a similar result from parsimony analysis of milk-protein gene sequences, concluding that the next outgroup to the hippocetacean clade was ruminant artiodactyls,
then pigs and peccaries, and Žnally camels.
Increasing the number of genes and the
number of taxa examined (Gatesy, 1997) produced similar results, and Montgelard et al.
(1997), using cytochrome b and 12s rRNA
sequences, also found support for an Ancodonta (Hexaprotodon + Hippopotamus) +
Cetacea clade to the exclusion of other artiodactyls. By contrast, the hippo-cetacean
clade had not been recovered in an earlier
parsimony analysis of amino acid sequences
(Czelusniak et al., 1990a).
Finally, Shimamura et al. (1997) found evidence for artiodactyl paraphyly on the basis of retroposons: nucleotide sequences that
have been inserted into a genome at particular loci (Li, 1997). As implemented by
Shimamura et al. (1997), the homology
statement for retroposons is their presence
or absence in a particular position in the
genome. The results of these authors demon-
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
strated a close relationship between Hippopotamus, ruminants, and cetaceans, to the
exclusion of the camel pig and several outgroup taxa. On the basis of these characters alone, Shimamura et al. (1997:669) asserted “we believe that recent molecular
data will lead to the reinterpretation by paleontologists of many fossil records of Artiodactyla to match our conclusions.” Furthermore, Milinkovitch and Thewissen (1997)
claimed that retroposons are “noise-free,”
arguing that it is improbable that retropositional elements inserted themselves independently into orthologous positions in the
genomes of different taxa. No phylogenetic
data, however, are known a priori to be free
of homoplasy (Wiley et al., 1991).
Thus, molecular papers arguing for artiodactyl paraphyly are numerous. Different molecular analyses have found perissodactyls, hippopotamids, ruminants, and
camels each to be most closely related
to cetaceans. A hippopotamid–ruminant–
cetacean grouping describes the most common Žnding of many of these studies,
notably those with the densest character
and taxon sampling. These unconventional
topologies recovered from molecular analyses have implications not only for cetacean
phylogeny but also for the monophyly of
clades within Artiodactyla. A previous phylogenetic analysis of morphological characters divided Artiodactyla into two clades,
each with extant and extinct members (Gentry and Hooker, 1988): Selenodontia, consisting of various ruminating artiodactyls
(including Tragulidae, Cervidae, GirafŽdae,
Antilocapridae, and Tylopoda and fossil relatives); and Bunodontia (including Suidae,
Tayassuidae, and Hippopotamidae and fossil relatives). Many of the molecular topologies, however, support paraphyly of the
clade including Suidae, Tayassuidae, and
Hippopotamidae, challenging the hypothesis that these taxa are more closely related to each other than any is to either
camels or ruminants (Matthew, 1929; Pickford, 1983; Gentry and Hooker, 1988). An
analysis of cytochrome b and 12s rRNA
sequences, combined with morphological
data for extant taxa only (Montgelard et al.,
1998), and aimed at testing the monophyly
461
of the clade that includes Suidae, Tayassuidae, and Hippopotamidae, reinforced the
notion that conicting signals are present in
morphological and molecular data sets. This
analysis did not include cetaceans, thereby
making it difŽcult to interpret the results in
the context of many other molecular analyses. At the same time, monophyly of ruminants and camels, to the exclusion of pigs,
peccaries, and hippos, has been argued on
the basis of suites of morphological characters (Webb and Taylor, 1980; Vaughan, 1986;
Gentry and Hooker, 1988; Langer, 1988)
but is disrupted in many of the molecular
phylogenies.
The hypothesis that Artiodactyla is
paraphyletic with respect to Cetacea contradicts traditional morphological ideas of
artiodactyl monophyly but merits explicit
testing in the wake of the numerous molecular studies supporting artiodactyl paraphyly. Furthermore, the morphological hypothesis of artiodactyl monophyly has been
formulated without knowledge of the morphology of the astragalus of a primitive
cetacean—the skeletal character argued to
be among the most important for determining membership within Artiodactyla (Luckett and Hong, 1998). Because it is paraphyly, not polyphyly, of Artiodactyla that
is in question, lack of evidence about the
cetacean astragalus invites the query: on
what basis do morphologists know that
whales are not highly derived artiodactyls?
We therefore investigated the morphological evidence for the following four questions: (1) Is Artiodactyla monophyletic with
respect to Cetacea; (2) what is the sister taxon
of Cetacea; (3) does exclusion of fossil taxa
from the phylogenetic analysis result in a
pruned version of the tree based on extant
taxa alone or a different tree; and (4) what
impact does the morphology of the astragalus of a primitive cetacean have on tree
topology?
MATERIALS AND METHODS
The SigniŽcance of a Morphological Data
Partition When Most of the Ingroup Is Extinct
We subscribe fully to the notion that a total evidence analysis (i.e., one based on com-
462
VOL. 48
SYSTEMATIC BIOLOGY
bined molecular and morphological data) is
an important step in the overall investigation of the position of Cetacea within Mammalia and that it is preferable to a taxonomic
congruence approach for reasons outlined
by Kluge (1989). It also has been argued in
the overall discussion of the signiŽcance of
total evidence that system-based data partitions (i.e., molecules, osteology, behavior,
or various subsets of these partitions) are
not at present derived from an understanding of biological processes but are instead
based on intuition (Kluge and Wolf, 1993).
Total evidence analyses combining molecular data for a few extant taxa with morphological data for extant taxa and a large
number of extinct taxa, however, face an
operational obstacle imposed by extinction.
With > 99% of all organisms extinct (Novacek and Wheeler, 1992), can such total evidence analyses be considered robust when
there are no molecular, soft tissue, or behavioral data for the vast majority of life?
Because of the potential importance of numerous extinct taxa for reconstructing the
phylogeny of Cetacea, taxa that are known
only from morphology and not from molecular biology, we believe it is also important
to investigate and present the morphological (predominantly osteological) signal independently. In such a data partition, extinct
taxa, which can far outnumber extant taxa in
an ingroup, can be maximally inuential on
tree topology.
The vast majority of ingroup taxa relevant to cetacean phylogeny are extinct.
Molecular and morphological contributions
to the problem of the phylogenetic position of Cetacea are congruent in nesting
Cetacea within ungulates, or the grandorder
Ungulata (McKenna and Bell, 1997). Ungulata (sensu McKenna and Bell, 1997) is diverse and includes several extinct clades
besides Artiodactyla, Cete (which includes
Cetacea), and Perissodactyla (Table 1). In
this study (see below) Žve orders comprise
the ingroup: Artiodactyla, Perissodactyla,
Procreodi, Cete, and “Condylarthra.” Most
(89%) of the genera in these orders are extinct (McKenna and Bell, 1997). Maximally,
a phylogenetic study based on extant taxa
alone can access no more than 11% of genera
in the ingroup. At present, larger moleculebased phylogenies (Gatesy, 1997) have sampled only 1% of ingroup genera. Even the
present study, which includes 37 ingroup
taxa, almost triple that of Gatesy (1997),
uses only 3% of relevant genera. Since the
aim of this analysis is to recover deep splits
between mammalian orders such as Artiodactyla, Perissodactyla, and Cetacea, sampling exhaustively within the ingroup may
not be essential if the most primitive members of a clade can be sampled. It is not,
however, likely that extant mammals are
primitive members of the clades in question, because both molecular and morphological estimates indicate that the splits
between mammalian orders are ancient
(Novacek, 1992b; Kumar and Hedges, 1998),
and their extant members have had much
time to evolve homoplasies.
TABLE 1. Estimate (derived from McKenna and
Bell, 1997) of the extinction in the ingroup in this analysis and other recent molecule-based phylogenetic analyses of the position of Cetacea within Mammalia (e.g.,
Gatesy, 1997, and references therein). Shown are the
number of extinct and extant genera from Žve orders
that make up the ingroup. This estimate of the number of ingroup taxa is conservative because the ingroup may include all genera within Ungulata (see
McKenna and Bell, 1997) (i.e., Tubulidenatata, Arctostylopida, Litopterna, Notoungulata, Astrapotheria, Xenungulata, Pyrotheria, and Urantotheria) and because
it is highly unlikely that the fossil record has preserved
all ingroup taxa.
Taxon
Artiodactyla
Perissodactyla
Cete
“Condylarthra”
Procreodi
Total
Extinct genera
Extant genera
589 (86%)
236 (97.5%)
243 (86%)
59 (100%)
29 (100%)
94 (14%)
6 (2.5%)
39 (14%)
0
0
1156 (89%)
139 (11%)
The problem of looking at only a few taxa,
particularly only a few extant mammalian
taxa, is that because mammalian orders have
ancient splits (long terminal branches) separated by short internodes (Novacek et al.,
1998), sampling of the extant taxa alone risks
reinforcing an inconsistent branching pattern attributable to long-branch attraction
(Felsenstein, 1978). Adding fossils to a data
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
matrix has been argued to be one way to expose and overturn a long-branch attraction
problem (Gauthier et al., 1988). The study
of Gauthier et al., 1988, and others of seed
plants (Doyle and Donoghue, 1987) and eutherians (Novacek, 1992a), all show that parsimony analysis of a matrix of morphological data for extant taxa alone results in a
tree that is incongruent with results of a parsimony analysis of a more complete matrix
(extant + extinct taxa) of the same characters. Interestingly, none of these empirical
analyses has shown that the tree based on
extant taxa alone was simply a pruned version of the tree based on the more complete
matrix. The assumption that the tree resulting from more taxa is the most robust is
implicit in this methodology and is logical,
because there is no justiŽcation for excluding ingroup taxa. Each study performed experiments in which fossil taxa were deleted
and parsimony analyses run to investigate
changes to the tree topology (Donoghue
et al., 1989). Drawing on independent evidence from simulations where the true tree
is known, Huelsenbeck (1991) recognized
that such deletion/restoration experiments
are one of the few means of testing whether
fossils have a signiŽcant effect on tree topology. Inclusion of fossil taxa is particularly
important when studying the relationships
of taxa separated by large stretches of time
because fossils aid in the identiŽcation of homoplasies that might otherwise go unrecognized (Doyle and Donoghue, 1987; Huelsenbeck, 1991). Essentially, fossils may break up
long branches.
Fossil taxa are particularly likely to
break up long branches in the radiation
of cetaceans and other ungulates. Morphological and molecular evidence argues that
the splits among Cetacea, Artiodactyla, and
Perissodactyla are > 50 million years old.
A fossil-based estimate for the divergence
of Cetacea from Artiodactyla is early Paleocene or very Late Cretaceous (~ 65 million
years ago; Gingerich and Uhen, 1998); for
Perissodactyla and Artiodactyla, Late Cretaceous (Novacek, 1992b; but see also Novacek et al., 1998). A molecule-based estimate for the divergence of Cetacea from
Artiodactyla is ~ 58 million years ago, and
463
that for Cetacea + Artiodactyla from Perissodactyla is ~ 83 million years ago (Kumar
and Hedges, 1998). Thus, by all estimates of
divergence, the split under consideration is
ancient and hence vulnerable to long-branch
attraction problems. Mesonychians, which
range from early Paleocene through late
Eocene (McKenna and Bell, 1997), are fossils
that meet two phylogenetically signiŽcant
criteria (Huelsenbeck, 1991): They are relatively complete, and they have a time of appearance relatively close to that of Cetacea.
Many of the diverse array of exinct artiodactyls, perissodactyls, and “condylarths”
known fulŽll similar criteria.
Other studies have reinforced the importance of taxonomic sampling. Wheeler
(1992) demonstrated on the basis of computer simulations that accuracy of cladograms is more affected by number of taxa
included than by model of evolution, number of characters (speciŽcally, length of nucleotide sequences), or rate of evolution. Although Kim (1996) argued that adding taxa
does not always increase phylogenetic accuracy, Graybeal (1998) recognized that many
of the taxa added in his study did not break
up long branches. She found that phylogenetic accuracy improved as the number
of taxa increased, even if simultaneously
the number of characters decreased. Importantly, the taxa added speciŽcally broke up
long branches, and she emphasized that it is
the addition of such taxa that improves phylogenetic accuracy, a result consistent with
paleontological studies.
We follow the methods of Doyle and
Donoghue (1987) and Gauthier et al. (1988)
and use deletion/restoration experiments
with fossil taxa to examine the effect of extinction on tree topology. Indeed, investigation of the morphological (again, primarily
osteological) signal alone is one of the few
ways to maximize the empirical effect of extinct clades on tree topology. If tree topology
changes on addition of morphological data
from fossil taxa, one hypothesis explaining
this result is that it would also happen if
molecular data were accessible for all extinct
ingroup taxa. Obviously, we cannot test this
hypothesis empirically because of missing
data. However, the operational reality faced
464
SYSTEMATIC BIOLOGY
by total evidence analyses is that extinction
creates a data partition that can inuence results and obscure phylogenetic signals. Because osteology can be studied across extinct and extant organisms, its signal alone
deserves consideration, for its potential to
offer an important perspective on relationships not apparent from neontological data.
Data Collection
Scoring all extant and extinct ungulate
genera, particularly Artiodactyla, Perissodactyla, Cetacea, Mesonychia, and archaic
ungulates, was an unrealistic point of departure because, as noted above, some of
these taxa are highly diverse. From among
the clades mentioned above we chose 37
genera to form the ingroup (Appendix 1),
primarily following principles outlined by
Hillis (1998:5 [methods 3 and 4]), and assumed that each of these genera is monophyletic on the basis of the morphological similarity of the species within it. The
ingroup consists primarily of fossil genera known from relatively complete specimens, chosen both because we believe they
are representative of forms close to the
basal morphotype of various extant ungulate clades and because they are representative of the diversity of ungulate clades
argued to be closest to Cetacea (Gentry
and Hooker, 1988; Prothero et al., 1988;
McKenna and Bell, 1997). We did not sample
extensively within paenungulates because
molecular and morphological phylogenies
described above do not argue for a close
relationship between Artiodactyla, Cetacea,
and paenungulates . We did, however, include several taxa that have been argued
on the basis of cladistic analysis (Thewissen and Domning, 1992) to be among the
most primitive members of the paenungulate clade (i.e., Meniscotherium, Phenacodus;
see Appendix 1, “archaic ungulates”). Other
paenungulates are assumed to be nested
among the taxa sampled.
The artiodactyl sample includes the
oldest member of this order, Diacodexis
(Rose, 1982); an entelodont, Archaeotherium;
an anthracothere, “Elomeryx”; an oreodontoid, Agriochoerus; a camelid, Poebrotherium; and several extant forms: Sus (pig),
VOL. 48
Hippopotamus, Hexaprotodon (= Choeropsis,
pygmy hippotamus), Ovis (sheep), Tragulus (chevrotain), and Camelus (camel)
(McKenna and Bell, 1997). The taxonomy
of anthracotheres is much in need of revision, and we place “Elomeryx” in quotes
because we have also used specimens attributed to Bothriodon (Ancodus) to score
the morphology of “Elomeryx”; these taxa
appear to be very similar, are from similar deposits, and may be synonyms. Our
sample of perissodactyls includes Equus
(horse), an extinct equid, Hyracotherium,
and an extinct tapiroid, Heptodon. All relatively complete genera of mesonychians
are included in our analysis, as well as
a number of extinct cetaceans—Pakicetus,
Ambulocetus, and Remingtonocetus, among
others—and two extant cetaceans: odontocete Tursiops (bottle-nosed dolphin) and
a mysticete Balaenoptera (rorqual whale).
Several relevant taxa, collectively described
as “archaic ungulates” (see below and
Appendix 1) or “condylarths,” were also
included.
One genus for which the assumption
of monophyly remains controversial is Pakicetus. We follow Thewissen and Hussain
(1998) as to which specimens constitute
Pakicetus. These authors caution that some
of these identiŽcations remain poorly substantiated. Where possible, original specimens were examined, but character coding was supplemented from the literature
when original specimens were unavailable
(Appendix 1).
Ordinal-level relationships of mammals
are incompletely resolved (Novacek, 1992b),
making outgroup choice ambiguous in
a study of this kind examining variation across more than four orders. In
Novacek’s (1992b) tree, the node below our ingroup (Artiodactyla, Perissodactyla, and Cetacea) is “Condylarthra,”
a paraphyletic assemblage of primitive,
herbivorous-omnivorous, placental mammals loosely allied with ungulates (Carroll, 1988). Although “Condylarthra” is not
speciŽcally designated as an outgroup in
our analysis, our tree contains a number of “condylarths”: Arctocyon, Hyposodus,
Meniscotherium, Phenacodus, triisodontines,
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
and mesonychians (Carroll, 1988), which effectively polarize characters within Artiodactyla, Perissodactyla, and Cetacea. The
sister taxon of “Condylarthra” is an unresolved polytomy consisting of archontans,
glires, carnivorans, and insectivorans (Novacek, 1992b). We chose one outgroup from
this assemblage, the insectivoran Leptictis,
and two others at still lower nodes on the
mammalian tree: the primitive eutherian
Asioryctes and the extant marsupial Didelphis. We decided against using Tubulidentata as an outgroup, despite the hypothesized proximity of this order to our ingroup
(Novacek, 1992b), because the highly derived dentition of tubulidentates would be
useless for polarizing dental characters in
the ingroup.
Our matrix heavily emphasizes osteological characters. We scored 123 morphological characters; 33 basicranial, 9 other cranial,
45 dental, 29 postcranial, and 7 soft morphological characters (Appendix 2). The amount
of missing data for a given taxon ranged
from 2% to 75% (average 29%; Appendix 3).
Most (88, or 72%) of the characters were binary, and 35 (28%) were multistate. Multistate characters were treated in two ways: (1)
all unordered, or (2) 24 of the 35 multistate
characters ordered (20% of the total number of characters, 68% of multistate characters); these characters are speciŽed in Appendices 2 and 3. Ordering was sequential
as follows: 0 « 1 « 2 « 3. Multistate characters were not ordered if we did not hypothesize a hierarchical transformation for
that character.
Treatment of multistate characters as ordered or unordered constitutes an assumption about evolutionary process (Hauser
and Presch, 1991; Wilkinson, 1992; Barriel
and Tassy, 1993; Slowinski, 1993) that must
be faced a priori in cladistic analysis. Unordered multistate characters assume that
one character state can transform directly
into any other character state without passing through an intermediate character state.
Ordered multistate characters assume that
transformations do pass through such an intermediate stage. Wilkinson (1992) argued
that ordering certain characters is a logical extension of Hennig’s auxiliary principle
465
and “explains the similarity between a subset of the character states in terms of synapomorphy” (Wilkinson, 1992:380). Slowinski
(1993) demonstrated that neither ordering
nor unordering necessarily increases taxonomic congruence, one measure of phylogenetic accuracy. He concluded that either
way of treating multistate characters is valid
(Slowinski, 1993:163) and proposed ordering as favorable if a transformation series
describes morphoclinal variation. The characters treated as ordered here capture hierarchical morphological change, and we argue
that treating these characters as unordered
would constitute a loss of information important for reconstructing this phylogeny.
Certain characters discussed as important
for substantiating the monophyly of Artiodactyla were not included in our study if we
could not score them in a consistent fashion
(e.g., the relative expansion of the pars facialis of the lacrimal bone). We excluded one
soft morphological character, relative elongation of the blastocyst (Thewissen, 1994;
Geisler and Luo, 1998), because it has not
been described in sufŽcient detail for many
of the extant taxa in question. The hypocone
of artiodactyls has been described as nonhomologous to the hypocones of various of
the ungulates (Prothero et al., 1988). This
cusp is thought to develop from the metaconule in Artiodactyla and from the lingual
cingulum in many other ungulates (Hunter
and Jernvall, 1995). Instead of assuming a
priori that the hypocones are nonhomologous, we scored both the metaconule and
the hypocone on the basis of position on
the tooth: the hypocone being the cusp in
the distolingual corner of the upper molar,
and the metaconule being the cusp positioned more labially or anterolabially on a
diagonal line between the metacone and the
protocone.
Outgroup taxa do not necessarily have
state 0 for every character (Appendix 3) for
two reasons: (1) we use several genera rather
than a hypothetical ancestor as an outgroup,
and there is morphological variation among
the outgroups; and (2) certain ordered characters (e.g., character 46) branch in two directions from the hypothesized primitive
state, which is most easily coded by desig-
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VOL. 48
SYSTEMATIC BIOLOGY
nating the primitive state as 1 and the derived states as 0 and 2.
Character Independence
An assumption of parsimony analysis is
that the characters used in a phylogenetic
analysis (homology statements) are independent. As discussed by Kluge and Wolf
(1993) independence in phylogenetic analysis must be addressed in two forms: (1) logical independence of characters, and (2) concurrent origin of the characters. The most
egregious violation of the assumption of independence is to score redundant characters, that is, those that fail the test of logical independence. Farris (1983:20) describes
an example of two characters that are not
logically independent as scoring “tarsal segments and twice that number” separately.
We strive not to include duplications of this
nature in our data matrix.
The second criterion for independence,
concurrent origin, is much more difŽcult
to verify (Kluge and Wolf, 1993), particularly for fossil taxa. Rejection of the
hypothesis that two synapomorphies
evolved independently requires knowledge
of tokogenetic relationships that “even our
best-supported phylogenetic propositions
do not provide” (Kluge and Wolf, 1993:192).
Numerous biological processes (e.g., genetic, selective, developmental) may contribute to the non-independence of different
characters. However, as Kluge and Wolf
(1993:192) contend, “the actual processes
responsible for nonindependent evolution
cannot be read from even the most detailed
patterns of organism relationship.” We interpret this to mean that similar distribution
of character states in two or more characters is not necessarily indicative of the nonindependence of those characters. Hence,
to dismiss covarying characters without
exquisite knowledge of tokogenetic relationships risks an a priori dismissal of phylogenetic signal (character congruence).
We, therefore, include all logically independent characters in our analysis, even
two characters that appear to covary exactly (i.e., characters 81 and 82). Exact covariance does not seem sufŽcient reason to
combine two characters in the matrix. These
characters cannot be scored for all taxa in
the matrix, and thus it is quite possible that
the exact covariance may disappear as our
knowledge of the fossil record improves.
Secondly, we are studying taxa whose origin is separated by millions of years, making it very likely that we have not discovered, and have not scored, all relevant forms.
Although in certain cases characters may
appear to have been acquired at the same
node (i.e., covary exactly), this may be a byproduct of extinction, fossilization, and the
scale of the analysis, not evidence of the nonindependence of the synapomorphies. This
paper contains references to basicranial,
cranial, dental, postcranial, and soft morphological data partitions. These partitions
are, however, simply constructs to organize
information and are not meant at present to
convey any knowledge of biologically based
character-relatedness.
Phylogenetic Analyses
The matrix was compiled in MacClade
3.07 (Maddison and Maddison, 1992) and
analyzed by using either the heuristic
or branch-and-bound search algorithms in
PAUP 3.1.1 (Swofford, 1993), depending on
the size of the character-taxon matrix in
a particular run. Once trees were found
in PAUP, character distributions were analyzed in MacClade. Because of the large size
of the data set, a branch-and-bound analysis
in PAUP was possible only in runs that excluded all fossils (runs 3 and 4; see below).
All other searches were heuristic with the
following settings: addition sequence random; number of replications = 1,000; treebisection and reconnection (TBR) branchswapping performed; MULPARS option in
effect; steepest descent option not in effect; branches having maximum length 0
collapsed to yield polytomies; trees unrooted; uninformative characters excluded;
and multistate taxa interpreted as polymorphism. Trees were rooted with Didelphis as
outgroup. All tree lengths reported are calculated in PAUP 3.1.1 (Swofford, 1993).
The character-taxon matrix was subject to
maximum parsimony analysis under the following parameters: run 1, certain multistate
characters ordered (Appendices 2 and 3);
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
run 2, all multistate characters unordered;
run 3, extant taxa only, and certain multistate
characters ordered; run 4, extant taxa only,
and all multistate characters unordered; run
5, certain multistate characters ordered, and
evidence from Thewissen et al. (1998) included; run 6, all multistate characters unordered, and evidence from Thewissen et al.
(1998) included. Runs 3 and 4 with extant
taxa only were constructed to mimic taxon
sampling available in molecular analyses,
thereby testing the effect of fossils on tree
topology.
On the basis of available data, we tested
the hypothesis that the morphology of the
cetacean astragalus is central to establishing
artiodactyl monophyly (Milinkovitch and
Thewissen, 1997; Luckett and Hong, 1998)
by adding in runs 5 and 6 new data on
what are described as astragali of primitive
cetaceans (Thewissen et al., 1998). The characters described by Thewissen et al. (1998)
are found on two specimens, neither of
which is associated with diagnostic cetacean
material. For this reason, we treat these data
with particular caution. These specimens
potentially provide data on three characters
that are missing data in our initial matrix: the
navicular facet (character 104), the sustentacular facet (character 105), and the lateral
process (character 107). (The cetacean conditions for the astragalar canal [character 103]
and the proximal astragalus [character 109],
are known for Ambulocetus [Thewissen et al.,
1996].) On the basis of the new bones, we
coded character 104 as a new state 3, at
(in Pakicetus); character 105 as state 0, narrow (in Pakicetus); and character 107 as state
1, absent (in Ambulocetus). The bone described by Thewissen et al. (1998) appears
to introduce new variability to character 105
not orignally reected in our coding regime.
Where our matrix emphasizes width of this
character, Thewissen et al. (1998) emphasize
length. This character is very likely in need
of more detailed description in the future to
accommodate the variation in the ingroup.
We calculated decay values (Bremer, 1988)
for nodes in the consensus trees from runs
1 and 2 by conducting heuristic searches
(with 100 replications, using TBR branchswapping and random addition) in PAUP
467
3.1.1 (Swofford, 1993) and using constraint
trees to Žnd trees that do not contain a
particular clade in question. The difference in length between these trees and our
most-parsimonious tree equals the decay
index for each node. We emphasize that
the decay values are estimates because all
searches are heuristic. Estimated bootstrap
values (Felsenstein, 1985) were calculated in
PAUP* 4.0b1 (Swofford, 1998) for the unordered and ordered trees by using heuristic searches (1,000 replications) with simple addition and TBR branch-swapping,
and including groups compatible with the
50% majority rule consensus. Optimization of characters was performed by using
both ACCTRAN and DELTRAN options in
PAUP 3.1.1. Finally, to compare the topology
found in one of the more densely sampled
molecule-based analyses (Gatesy, 1997) with
the morphology-based results here, we used
a backbone constraint tree in PAUP* 4.061
to search for the most-parsimonious morphological tree under this molecular topological constraint. This exercise provided an
estimate of whether or not forcing the topology generated on the basis of molecular data
alone substantially increased the length of
the tree based on morphology alone. This experiment was performed on the matrix with
ordered characters only.
RESULTS
Run 1, in which 20% of the total number of characters (69% of multistate characters) were ordered (Fig. 2, Appendices 2
and 3), produced two most-parsimonious
trees of 536 steps each, the strict consensus of which supported monophyly of each
the following clades: Artiodactyla, Perissodactyla, Mesonychia, Mesonychidae, and
Cetacea. The sister taxon of Cetacea is
Mesonychia (Hapalodectidae and Mesonychidae), and the sister group to the cetaceanmesonychyian clade is the triisodontine
arctocyonid, Andrewsarchus. Among clades
with extant members, Artiodactyla is more
closely related to the mesonychian-cetacean
clade than is Perissodactyla. Within Artiodactyla, Sus, the hippopotamids, the entelodont, and the anthracothere are more
468
SYSTEMATIC BIOLOGY
VOL. 48
FIGURE 2. Strict consensus of two most-parsimonious trees of 536 steps each from run 1 (CI = 0.384, RI = 0.696,
HI = 0.698, RC = 0.267), 20% of total characters ordered (68% of multistate characters) (Appendices 2 and 3).
Artiodactyla (A), Cetacea (C), Mesonychidae (D), Mesonychia (M), and Perissodactyla (P) are each monophyletic.
Table 2 describes synapomorphies found with ACCTRAN and DELTRAN optimization at nodes marked with
letters. Extant taxa = bold, extinct taxa = y. Numbers above branches are estimated decay values; numbers below
branches are estimated bootstrap support.
closely related to each other than any is to
the ruminant clade, which consists of Ovis,
Tragulus, Camelus, and Poebrotherium. Meniscotherium, Phenacodus, and Hyopsodus form
a monophyletic clade with Perissodactyla.
The ingroup overall is not monophyletic;
the “condylarth” Arctocyon falls outside of
a clade that includes the insectivoran Lep-
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
tictis. The data are not strong enough to
unite the two triisodontine arctocyonids Andrewsarchus and Eoconodon as monophyletic,
or even to draw Eoconodon into the ingroup,
where it is hypothesized to belong based on
current taxonomy (McKenna and Bell, 1997).
Estimated decay indices indicate that the
monophyly of Artiodactyla is more strongly
supported than either the sister taxon relationship between Mesonychia and Cetacea
or the clade Artiodactyla + (Andrewsarchus
+ (Mesonychia + Cetacea))).
Run 2 (all characters unordered; Fig. 3)
resulted in 36 most-parsimonious trees of
505 steps each, the strict consensus of which
supports monophyly of each of the following clades: Artiodactyla, Perissodactyla, and
Cetacea. The sister taxon of Cetacea is now
the mesonychian Hapalodectes, the polarity
within Mesonychidae has reversed in comparison with Figure 2, and both Mesonychia and Mesonychidae are paraphyletic
with respect to Cetacea. Two results occur
in all most-parsimonious trees, as in run
1: Poebrotherium and Camelus form a clade
with the ruminants (Tragulus and Ovis), and
Hyopsodus, Phenacodus, and Meniscotherium
form a clade with Perissodactyla (Fig. 2).
The tree topology within Artiodactyla is relatively similar to that found in run 1, except
that the oreodontoid Agriochoerus joins the
ruminant clade.
Removing all fossils from the charactertaxon matrix and treating certain characters as ordered (run 3; Fig. 4a-c) recovers
three most-parsimonious trees of 173 steps
each, the strict consensus of which is a paraphyletic Artiodactyla with internal relationships of the ingroup poorly resolved.
The three most-parsimonious trees (Fig. 4)
support a cetacean sister group relationship
with Ovis or with Ovis + (Camelus + Tragulus). Running extant taxa only with all multistate characters unordered (run 4; Fig. 4d-e)
resulted in two most-parsimonious trees of
150 steps each, again with a paraphyletic Artiodactyla and Cetacea nested inside as the
sister taxon of either hippopotamids or hippopotamids + Sus.
The backbone constraint tree (Fig. 5b),
which forced the most-parsimonious solution for the morphological matrix congruent
469
with one topology generated on the basis
of molecules (Gatesy, 1997), was 551 steps,
15 steps longer than the most-parsimonious
tree that was based on our morphological matrix with certain multistate characters ordered (Fig. 2). Under this constraint,
mesonychians are still the sister taxon of
Cetacea, and this entire clade falls inside Artiodactyla.
Optimizations
Synapomorphies for the tree found in
run 1 (certain characters ordered) calculated with both ACCTRAN and DELTRAN
optimization algorithms (Table 2) are described below. Such synapomorphies describe the strongest support for particular
nodes because they persist whether parallelism or reversals are favored. The clade
including Perissodactyla + (Artiodactyla +
(Andrewsarchus + (Mesonychia + Cetacea)))
is supported by four such synapomorphies
(Table 2; Fig. 2: node a), which come from
basicranial, dental, and postcranial partitions of the data matrix. Artiodactyla +
(Andrewsarchus + (Mesonychia + Cetacea))
is supported by 12 synapomorphies (Fig. 2:
node b) from basicranial, cranial, postcranial, and soft-morphological partitons of
the data matrix. Mesonychia + Cetacea,
however, is supported by only two synapomorphies (Fig. 2: node d). This is due
in large part to the fragmentary nature of Andrewsarchus, the outgroup to
this clade, which makes polarity calculations ambiguous. Cetacea is one of
the more strongly supported nodes with
15 synapomorphies from basicranial, cranial, and dental data (Fig. 2: node e).
Mesonychia (Hapalodectes + Mesonychidae)
(Fig. 2: node f), by contrast, is supported
by three dental synapomorphies, and
Mesonychidae by four synapomorphies,
from basicranial, cranial, and dental data
partitions (Fig. 2: node g). Artiodactyla
(Fig. 2: node j) is supported by 8 synapomorphies from basicranial, dental, and postcranial partitions of the data matrix. Perissodactyla, and clades that include stem
taxa leading to it, are well-supported
nodes with several synapomorphies each
(Table 2).
470
SYSTEMATIC BIOLOGY
VOL. 48
FIGURE 3. Strict consensus of 36 most-parsimonious trees, 505 steps each (CI = 0.406, RI = 0.694, HI = 0.679,
RC = 0.282), all characters unordered (run 2). Artiodactyla (A), Cetacea (C), and Perissodactyla (P) are each
monophyletic; Mesonychidae (“D”), and Mesonychia (“M”) are paraphyletic. Numbers above branches represent estimated decay values, numbers below branches represent estimated bootstrap support, branches without
bootstrap values are nodes recovered in < 5% of bootstrap replicates . Extant taxa are in bold; extinct taxa = y.
Unequivocal synapomorphies supporting artiodactyl monophyly in all 36 trees are the following: 27. Alisphenoid
canal, present (1) ® absent (0); 32. Post-temporal canal, present (0) ® absent (1); 86. dp4 , resembles M1 (0) ®
six-cusped (1); 92. Entepicondyle, wide (0) ® narrow (1); 93. Entepicondylar foramen, present (0) ® absent (1); 96.
Proximal radius, two fossae (1) ® three fossae (2); 105. Sustentaculum, narrow (0) ® wide (1); 107. Lateral process
of astragalus, present (0) ® absent (1); 109. Proximal astragalus, at (0) ® deeply grooved (2). The unequivocal
synapomorphies supporting Hapalodectes + Cetacea are these: 37. Lacrimal tubercle, present (1) ® absent (0); 60.
M3 , absent (3) ® equal to M2 in size (1); 83. Reentrant grooves, distal (2) ® proximal (0); and 95. Olecranon
process, deep (1) ® shallow (0).
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
471
Because removal of extinct taxa from the
data matrix changed the topology of the
tree (compare Figs. 2 and 4a-c, or Figs.
3 and 4d-e), we examined which of the
characters speciŽcally supporting the sister taxon relationship with Cetacea were
acting as homologies in the cladograms of
extant taxa alone (Fig. 4) but were homoplasies when the fossils were included. (Figs.
2 and 3; Table 2). These characters, listed
in the caption to Figure 4, came from the
cranial, postcranial, or soft-morphological
data partitions.
Addition of Astragalar Data from Thewissen
et al. (1998)
When the data from Thewissen et al.
(1998) are incorporated into the matrix (runs
5 and 6), cetaceans are scored as having one
character that was shown above (Table 2) to
be a synapomorphy for Artiodactyla: character 107, lateral process of the astragalus
absent. Adding these characters to the matrix with certain multistate characters ordered (run 5) results in 2 trees of 539 steps
each with a topology no different from that
of Figure 2. Adding these characters to the
matrix with all multistate characters unordered results in a concensus tree no different from that found in Figure 3; that is,
the new data do not change the toplogies
of the trees.
D ISCUSSION
Results of these parsimony analyses show
that on the basis of 123 morphological
characters (116 osteological and 7 soft morFIGURE 4. Results of parsimony analyses with all extinct taxa removed from the data matrix (Appendix 3).
(a-c) The three most-parsimonious trees of 173 steps each (CI = 0.618, RI = 0.590, HI = 0.422, RC = 0.365), based on
the matrix with 20% of multistate characters ordered (Appendices 2 and 3) (run 3); Cetacea is the sister taxon of
Ovis in (a) and (b) or Ovis + (Camelus + Tragulus) in (c). Synapomorphies supporting the sister taxon relationship
between Cetacea and other taxa found with both ACCTRAN and DELTRAN algorithms are as follows: Tree a-1.
Subarcuate fossa, present (0) ® absent (1); 15. Articulation of ectotympanic to squamosal, broad (0) ® absent
(3); and 16. Exoccipital-ectotympanic contact, present (1) ® absent (0); tree b-1 and 15; tree c-26. Foramen ovale,
medial, posterior wall formed by petrosal (2) ® anterior, posterior wall formed by alisphenoid (0); 94. Length
of olecranon process, long (1) ® short (0); 113. Second metatarsal, unreduced (0) ® highly reduced (2); and 114.
Fifth metatarsal, unreduced (0) ® highly reduced (2). (d and e) The two most-parsimonious trees of 150 steps
each (run 4) (CI = 0.660, RI = 0.617, HI = 0.387, RC = 0.407), based on the matrix with all multistate characters
unordered. Synapomorphies supporting Cetacea as the sister taxon of Sus + (Hippopotamus + Hexaprotodon) (tree
d) are these: 7. Mastoid, exposed (0) ® not exposed (1); 23. Postglenoid foramen, present, enclosed by squamosal
(0) ® absent (2). The following support Cetacea as the sister taxon of Hippopotamus + Hexaprotodon (tree e): 1.
Subarcuate fossa: present (0) ® absent (1); 15. Articulation of ectotympanic to squamosal: broad (0) ® absent (3);
121. Hair: abundant (0) ® absent (1); and 122. Sebaceous glands: present (0) ® absent (1).
472
SYSTEMATIC BIOLOGY
FIGURE 5. Comparison of backbone constraint tree
to molecule-based tree, both addressing the question
of artiodactyl monophyly. (a) pruned tree from Gatesy
(1997) used as the constraint; (b) strict consensus of nine
most-parsimonious trees of 551 steps each resulting
from a heuristic search using the tree from (a) as a backbone constraint and the matrix with certain multistate
characters ordered. Extant taxa are in bold. Cetacea
(C), Mesonychidae (D), Mesonychia (M), and Perissodactyla (P) are each monophyletic, “A” = Artiodactyla
here is monophyletic only if Cetacea are included.
VOL. 48
phological) from 10 extant and 30 extinct
taxa, Artiodactyla is more closely related
to Cetacea than is Perissodactyla. This conclusion is supported when certain multistate characters (20% of the total data set)
are treated as ordered, when all multistate
characters are treated as unordered, and
when we exclude fossils from the analysis. We believe that results of runs with
certain multistate characters ordered better
reect hierarchical morphoclinal transformations and relationships between different
character states (Wilkinson, 1992; Slowinski, 1993), that are important to reconstructing phylogeny. With certain characters ordered, the sister taxon of Cetacea is
a monophyletic Mesonychia, as has been argued on the basis of dental characters alone
(O’Leary, 1998a). The triisodontine arctocyonid Andrewsarchus is the stem taxon to this
cetacean-mesonychian clade, and a monophyletic Artiodactyla is the sister taxon to
that clade (Fig. 2). This tree also supports
traditional groupings within Artiodactyla
(Gentry and Hooker, 1988): a ruminantcamel clade and a hippopotamid-suid clade,
each with extinct relatives. That Cetacea is
more closely related to Artiodactyla than
to Perissodactyla corroborates the conclusions of virtually all molecule-based phylogenetic analyses of this question noted in
the introduction, as well as several exclusively morphological descriptions or analyses (Gingerich et al., 1990; Novacek, 1992b;
Thewissen and Hussain, 1993; Geisler and
O’Leary, 1997; Geisler and Luo, 1998), but
is incongruent with conclusions of several
other morphological analyses (Novacek and
Wyss, 1986; Wible, 1987; Prothero et al., 1988;
Novacek, 1989; Prothero, 1993; Thewissen,
1994).
When all multistate characters are treated
as unordered, the strict consensus of
36 most-parsimonious trees also has a
monophyletic Artiodactyla, but Mesonychia, Mesonychidae, and triisodontine
arctocyonids are paraphyletic. Other nodes
at which this tree is congruent with that
from the run with certain multistate
characters ordered are these: monophyly
of Perissodactyla, the order of stem taxa
leading to Perissodactyla (Meniscotherium,
Phenacodus, Hyopsodus), a clade including
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
473
TABLE 2. Character optimizations for particular nodes in the two most-parsimonious trees from run 2 (certain
multistate characters ordered, Fig. 2). Character state transformations were calculated by using both ACCTRAN
and DELTRAN algorithms in PAUP 3.1.1. Complete character state descriptions are given in Appendix 2. Indicated
are transformations found with (A) ACCTRAN only, (D) DELTRAN only, or (A/D) ACCTRAN and DELTRAN
(in bold).
Node
a
b
c
Character
A 2. Tegmen tympani
A/D 11. Ectotympanic
A/D 60. M3 equal to M2
A 95. Olecranon fossa
A/D 97. Distal radius
A/D 115. Distal phalanges
A/D 16. Exoccipital-ectotympanic
contact
A/D 17. Sigmoid process
A 20. Squamosal part of external
auditory meatus
A/D 37. Lacrimal tubercle
A 56. M1 -M2 hypocone
A 58. Paraconule on M2
A 59. Metaconule on M2
A/D 92. Entepicondyle
A 93. Entepicondylar foramen
A/D 99. Manus
A/D 104. Navicular facet
A/D 108. Pes
A/D 112. First metatarsal
A/D 118. Lumen
A/D 119. Stomach lumen
A/D 120. Cavernous tissue of penis
A/D 123. Lung bronchi
D 20. Squamosal part of external
auditory meatus
A 22. Internal carotid foramen
A/D 23. Post-glenoid foramen
A 25. Position of foramen for ramus
superior of stapedial artery
A 26. Foramen ovale
A 30. Foramen rotundum
A 31. Mastoid foramen
A 33. Preglenoid process
A 52. M2 metacone
D 56. M1 -M2 hypocone
A/D 57. Trigon basin
A 71. M2 paraconid
A 73. M3 paraconid
A 78. Protoconid
A 83. Reentrant grooves
A 94. Olecranon process
A 95. Olecranon fossa
A 98. Centrale
A 116. Distal phalanges
A 121. Hair
A 122. Sebaceous glands
Transformation
(0) Uninated ® (1) inated
(0) Ring ! (1) bulla
(2) Smaller than M2 ! (1) equal
(0) Shallow ® (1) deep
(0) Single, concave fossa ! (1) scaphoid
and lunate fossae
(0) Curved ! (1) straight
(0) Absent ! (1) present
(0) Absent ! (1) present
(0) Absent ® (1) deep groove
(1) Present ! (0) absent
(1) Present ® (0) absent
(1) Present ® (0) absent
(1) Present ® (0) absent
(0) Wide ! (1) narrow
(0) Present ® (1) absent
(0) Mesaxonic ! (1) paraxonic
(0) Convex ! (1) saddle-shaped
(0) Mesaxonic ! (1) paraxonic.
(1) Reduced ! (2) highly reduced
(0) Unilocular ! (1) plurilocular
(0) Absent ! (1) present
(0) Abundant ! (1) sparse
(0) Two ! (1) three
(0) Absent ® (1) deep groove
(0) Absent ® (1) present
(0) Enclosed by squamosal ! (1) medial to
petrosal/squamosal suture
(0) In petrosal/squamosal suture ® (1) anterolateral
to epitympanic recess
(1) Medial ® (0) anterior
(0) Absent ® (1) present
(0) Present ® (1) absent
(0) Absent ® (1) present
(0) Subequal to paracone ® (1) half the size of
paracone
(1) Present ® (0) absent
(0) Broad ! (1) narrow
(0) Present ® (1) absent
(0) Present ® (1) absent
(0) Subequal to height of talonid ® (1) twice
height of talonid
(1) Absent ® (0) proximal
(0) Short ® (1) long
(1) Deep ® (0) shallow
(1) Absent ® (0) present
(0) Compressed ® (1) broad
(0) Abundant ® (1) absent
(0) Present ® (1) absent
(continued on next page)
474
TABLE 2.
Node
d
e
VOL. 48
SYSTEMATIC BIOLOGY
Character
D 2. Tegmen tymapani
D 31. Mastoid foramen
A 45. Embrasure pits
D 52. M2 metacone
A 54. Lingual cingulum on M2
A/D 57. Trigon basin
D 73. M3 paraconid
D 83. Reentrant grooves
A/D 84. Talonid basins
A/D 85. M3 hypoconulid
D 94. Olecranon process
D 116. Distal phalanges
A 3. Anterior process of petrosal
A 4. Tensor tympani fossa
D 4. Tensor tympani fossa
A 5. Sulcus for internal caroid
artery
A/D 6. Proximal stapedial artery
sulcus
A/D 7. Mastoid process external
exposure
D 9. Facial nerve sulcus
A 9. Facial nerve sulcus
A/D 12. Pachyosteosclerotic
involucrum
A/D 15. Articulation of ectotympanic
bulla to squamosal
A/D 24. Foramen for ramus superior
of stapedial artery
D 26. Foramen ovale
A/D 27. Alisphenoid canal
A 33. Preglenoid process
A 35. Postorbital bar
A 44. Premaxillae
A/D 48. P4 protocone
A/D 49. P4 paracone
A 52. M2 metacone
A/D 67. Lingual cingulid
A/D 68. M1 paraconid
A/D 70. M2 paraconid
A 72. M3 paraconid
A/D 74. M1 metaconid
A/D 75. M2 metaconid
A 76. M3 metaconid
A/D 87. Elongate shearing facets
A 91. Scapular spine
A 96. Proximal radius
(Continued)
Transformation
(0) Uninated ® (1) inated
(0) Present ® (1) absent
(0) Absent ® (1) present
(0) Sub-equal to paracone ® (1) half size of
paracone
(0) Present ® (1) absent
(1) Narrow ! (2) very narrow
(0) Present ® (1) absent
(1) Absent ® (0) proximal
(0) Basined ! (1) reduced
(0) Long ! (2) absent
(0) Short ® (1) long
(0) Compressed ® (1) broad
(0) Absent ® (1) present
(1) Circular pit, no groove ® (2) circular pit,
deep groove
(0) Elongate fossa ® (2) circular pit, deep groove
(0) Present ® (1) absent
(0) Present ! (1) absent
(0) Present ! (1) absent
(0) Absent ® (2) anterior wall = mastoid process
(3) Anterior wall formed by meatal tube ® (2)
anterior wall formed by mastoid process
(0) Absent ! (1) present
(0) Broad ! (1) circular facet
(0) Present ! (1) absent
(1) Medial to glenoid fossa, posterior wall =
alisphenoid ® (0) anterior to glenoid fossa,
posterior wall formed by alisphenoid
(1) Present ! (0) absent
(1) Present ® (0) absent
(0) Absent ® (1) present, almost complete
(0) Short ® (1) elongate
(0) Present ! (1) absent
(0) Equal to height of M1 paracone ! (1) twice height
of M1 paracone
(1) Half the size of the paracone ® (2) highly
reduced
(0) Absent ! (1) present
(0) Present ! (1) absent
(0) Present ! (1) absent
(0) Present ® (1) absent
(0) Present ! (1) absent
(0) Present ! (1) absent
(0) Present ® (1) absent
(0) Absent ! (1) present
(0) Acromion overhangs glenoid ® (2) acromion
does not overhang glenoid
(1) Two fossae ® (0) one fossa
(continued on next page)
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
TABLE 2.
Node
f
g
Character
A 14. Median furrow of tympanic bulla
A 19. Ectotympanic part of meatal tube
D 30. Foramen rotundum
D 33. Preglenoid process
A 41. Mandibular condyle height
A/D 50. P4 metacone
A/D 53. M1 parastyle
D 54. Lingual cingulum
A/D 69. M1 paracristid position
D 71. M2 paracristid position
A 90. Number of sacrals
A 93. Entepicondylar foramen
D 4. Tensor tympani fossa
A 9. Facial nerve sulcus
A 22. Internal carotid foramen
A/D 23. Post-glenoid foramen
D 25. Foramen for ramus superior of
stapedial artery
D 26. Foramen ovale
h
i
A/D 29. Posterior opening
of alisphenoid canal
A 37. Lacrimal tubercle
D 41. Height of mandibular condyle
A 45. Embrasure pits
A/D 60. M3 size
A/D 83. Reentrant grooves
A/D 95. Olecranon fossa
D 2. Tegmen tympani
A 14. Median furrow of tympanic bulla
A 41. Condyle
D 58. Paraconule on M2
D 59. Metaconule on M2
A/D 65. P3 metaconid
A/D 66. P4 metaconid
A/D 77. M1 -M2 hypoconulid
D 78. Protoconid
D 90. Number of sacral vertebrae
D 95. Olecranon fossa
A/D 106. Astragalar-cuboid contact
A 4. Fossa for tensor tympani
D 5. Transpromontorial sulcus for
internal carotid artery
D 6. Proximal stapedial artery
D 53. M1 parastyle
A/D 79. Protoloph
A 90. Number of sacral vertebrae
A 91. Scapular spine
A/D 92. Entepicondyle
A/D 93. Entepicondylar foramen
A/D 103. Astragalar canal
A/D 104. Navicular facet of
astragalus
475
(Continued)
Transformation
(1) Median notch ® (0) absent
(1) Short ® (2) long
(0) Absent ® (1) present
(0) Absent ® (1) present
(1) Even with dentition ® (0) below dentition
(0) Absent ! (1) present
(0) Absent ! (2) strong
(0) Absent ® (1) present
(0) Lingual ! (1) anterior
(0) Lingual ® (1) anterior
(2) Four ® (1) two or three
(1) Absent ® (0) present
(0) Elongate fossa ® (1) circular pit
(3) Anterior wall formed by meatal tube ® (1)
anterior wall formed by squamosal
(1) Present ® (0) absent
(1) Present ! (2) absent
(0) In petrosal/squamosal suture ® (1)
anterolateral to epitympanic recess
(1) Medial to glenoid fossa, posterior wall formed by
alisphenoid ® (0) anterior to glenoid fossa
(0) Separated from foramen ovale ! (1) in a
recess with the foramen ovale
(0) Absent ® (1) present
(1) Even with dentition ® (0) below dentition
(1) Present ® (0) absent
(1) Equal to M2 ! (2) small
(0) Proximal ! (2) distal
(0) Shallow ! (1) deep
(0) Uninated ® (1) inated
(1) Median notch ® (2) anteroposterior furrow
(1) Even with dentition ® (2) superior to dentition
(0) Absent ® (1) present
(0) Absent ® (1) present
(0) Absent ! (1) present
(0) Absent ! (1) present
(0) Absent ! (1) present
(1) Twice height of talonid ! (0) subequal to
height of talonid
(1) Two or three ® (2) four
(0) Shallow ® (1) deep
(1) Present ! (0) absent
(0) Elongate fossa ® (1) circular pit
(0) Present ® (1) absent
(0) Present ® (1) absent
(0) Absent ® (1) weak
(0) Absent ! (1) present
(2) Four ® (3) Žve or six
(0) Large acromion ® (1) small acromion
(0) Wide ! (1) narrow
(0) Present ! (1) absent
(0) Present ! (1) absent
(0) Convex ! (1) saddle-shaped
(continued on next page)
476
TABLE 2.
Node
j
VOL. 48
SYSTEMATIC BIOLOGY
(Continued)
Character
A/D 109. Proximal astragalus
A/D 112. First metatarsal
A/D 114. Fifth metatarsal
A 2. Tegmen tympani
D 4. Tensor tympani fossa
A/D 27. Alisphenoid canal
A/D 32. Post-temporal canal
A/D 36. Frontal and maxillary
contact
D 78. Protoconid
A/D 86. dp4
A 91. Acromion
D 93. Entepicondylar foramen
D 95. Olecranon fossa
A/D 96. Proximal radius
D 98. Centrale
A/D 101. Third trochanter
A/D 104. Navicular facet of
astragalus
A/D 105. Sustentacular width
A 106. Astragalar-cuboid contact
A/D 107. Lateral process of
astragalus
A 109. Proximal astragalus
camels and ruminants, and one including
hippopotamids, Sus, and fossil relatives.
Milinkovitch and Thewissen (1997) argued that determination of the sister group
of Cetacea hinges strongly on the recovery of an astragalus of a primitive cetacean
(e.g., Pakicetus, Ambulocetus). Two fragmentary astragali argued to be cetaceans on the
basis of faunal data have recently been described (Thewissen et al., 1998). These bones
are not, however, associated with diagnostic cetacean material, and we treat their impact on the phylogeny of Cetacea with some
caution. The new fossils are extremely fragmentary, and we have concluded that these
bones introduce new and possibly autapomorphic character states not previously recognized. Addition of these new fossils does
not change the tree topology or the number of trees found whether multistate characters are treated as ordered or unordered.
These bones have been described as exhibiting more similarities to artiodactyls than
to mesonychians (Thewissen et al., 1998);
nonetheless, the invariance of our result may
Transformation
(1) Grooved ! (2) deeply grooved
(1) Reduced ! (2) highly reduced
(1) Reduced ! (2) highly reduced
(1) Inated ® (0) uninated
(0) Elongate fossa ® (1) circular pit
(1) Present ! (0) absent
(0) Present ! (1) absent
(0) Absent ! (1) present
(1) Twice height of talonid ® (0) subequal to
height of talonid
(0) Resembles M1 ! (1) six-cusped
(0) Large ® (1) small
(0) Present ® (1) absent
(0) Shallow ® (1) deep
(1) Two fossae ! (2) three fossae
(0) Present ® (1) absent
(0) Present ! (1) highly reduced
(1) Saddle-shaped ! (2) trochleated
(0) Narrow ! (1) wide
(1) Small ® (2) large
(0) Present ! (1) absent
(0) Flat ®
(2) deeply grooved
be related to the fact that artiodactyl monophyly is supported by basicranial, dental, and postcranial synapomorphies, not
simply synapomorphies based on ankle
morphology.
As found in other phylogenetic analyses (Gauthier et al., 1988), removing fossils
from an analysis does not simply result
in a pruned version of the tree generated
from the matrix with extinct and extant taxa,
but instead results in a tree with a different
topology. When all extinct taxa are removed
from the character-taxon matrix, mimicking the taxon sampling of many molecular analyses, we consistently recover artiodactyl paraphyly with Cetacea as the sister
taxon of Ovis, a clade including Ovis +
(Camelus + Tragulus), hippopotamids, or hippopotamids + Sus. Characters supporting
these sister taxon relationships with Cetacea
come from a variety of anatomical systems
and are interpreted as homoplasies in the
more complete matrix that includes extant
and extinct taxa. Interestingly, artiodactyl
paraphyly is also the result found in most
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
molecule-based analyses of the phylogenetic position of cetaceans, studies that cannot sample extinct taxa. The topology supported in the molecule-based analysis of
Gatesy (1997) would increase the length of
the most-parsimonious tree based on our
matrix by 15 steps, a substantial number in
a tree based on only 123 characters.
Given a conservative estimate that 89% of
the ingroup genera relevant to the phylogenetic position of Cetacea are extinct, we propose that analysis of a morphology-based,
largely osteological, phylogenetic signal is
particularly important, because extinct taxa
can be maximally effective in such an analysis. We cannot test the effect of most molecular data on tree topology, because they are
not available for mesonychians, triisodontine arctocyonids, other “condylarths,” lepticitids, basal artiodactyls, or basal perissodactyls. These extinct taxa may have even
more information on branching sequences
and character transformation than do extant
taxa, because by virtue of their antiquity the
extinct taxa have had less time to evolve
homoplasies.
The stem taxa that we have added
here, mesonychians—“condylarths,” triisodontines, and basal artiodactyls and
perissodactyls—introduce so much data on
character transformation that they overturn nodes supported in most-parsimonious
trees that are based on extant taxa alone
(Figs. 2–4). These stem taxa simultaneously
introduce substantial homoplasy: The consistency index (CI) for the trees based on extant taxa alone (Fig. 4a-c) is 0.618, whereas
that for the more complete matrix (extant
+ extinct) taxa (Fig. 2) is 0.391. Adding ingroup taxa to a phylogenetic problem, as we
have done, typically increases homoplasy
(Sanderson and Donoghue, 1989), something that may affect the bootstrap and decay values of the Žnal tree. Strict comparisons between decay and bootstrap values
found in this study and those in moleculebased studies are not a means of assessing relative robustness of the different phylogenetic hypotheses they support because
the trees are derived from different characters and taxa. Values presented here for
the decay and bootstrap are lower than
477
those found in a molecule-based analysis
of Gatesy (1997), which supports a sister
taxon relationship between hippopotamids
and cetaceans, not artiodactyl monophyly. It
has been shown elsewhere that addition of
an extra ingroup taxon with homoplasies to
a parsimony analysis can reduce the stability of the ingroup (i.e., make it decay faster)
(Novacek, 1991). However, if that taxon is
part of the ingroup, it simultaneously contributes to an increase in understanding of
character transformation and relationships.
Given such effects, Novacek (1991:347) argued that “cladistic results are not uniformly
amenable to evaluation by simple measures
of the stability of their components.” Such
measures include the bootstrap and decay
indices. Novacek (1991) argued further that
addition of stem taxa may elucidate character transformation at the price of destabilizing certain nodes.
In an important effort to synthesize information on differing molecular and morphological hypotheses of cetacean origins,
Gatesy et al. (1996) proposed three hypotheses of relationship incorporating extinct and extant taxa: (1) cetaceans and
mesonychians are derived artiodactyls; (2)
cetaceans are derived artiodactyls and the
sister group of hippopotamids, and mesonychians are a separate clade outside of Artiodactyla; and (3) Artiodactyla is monophyletic and mesonychians are the sister
taxon of cetaceans. On the basis of all the
morphological evidence presented here, neither mesonychians nor cetaceans are derived artiodactyls (hypotheses 1 and 2),
making hypothesis 3 the best explanation
of the morphological data. Hypothesis 3
renders as homoplasies the six morphological and behavioral synapomorphies of
hippopotamids and cetaceans proposed by
Gatesy et al. (1996). These include absence
of hair, aquatic habitat, and underwater
vocalization.
These results suggest future avenues of
investigation likely to impact the phylogenetic position of Cetacea. The triisodontine arctocyonid Andrewsarchus does not
have the close relationship to Cetacea proposed by Prothero et al. (1988), but instead
falls outside of a mesonychian-cetacean
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SYSTEMATIC BIOLOGY
clade largely on the basis of dental evidence, as argued by O’Leary (1998a) . Andrewsarchus forms part of a paraphyletic
grouping with Eoconodon, but expanded
investigation of the triisodontine arctocyonids, a relatively primitive and poorly
known group, is necessary before the paraphyly of this group should be recognized
by taxonomic changes. In particular, knowledge of such features as the morphology
of the distal phalanges of Hapalodectes and
Eoconodon will be important for establishing their positions within ungulates. The result that the insectivoran Leptictis, an outgroup taxon, falls closer to our ingroup than
does the primitive “condylarth” Arctocyon
also warrants further testing and may be
an artifact of including only one insectivoran. It is not clear that the hypocone in all
members of Artiodactyla is derived from
the metaconule, because both the hypocone
and the metaconule are present together
in the clade comprising Archaeotherium,
“Elomeryx,” and Sus (Appendix 3). Phylogenetic analyses focusing on the relationships within Cetacea (Uhen, 1996) do not
support the positions of Basilosaurus and
Dorudon found in this analysis but instead
place Dorudon closer to extant cetaceans. Because the aim of this study is to resolve more
basal nodes in the ungulate tree, we suspect
that the addition of more characters or more
basilosaurid cetaceans to this matrix may
result in the topology supported in Uhen
(1996).
Results based on the data set with certain multistate characters ordered (Fig. 2)
require that cetaceans diverged by the
middle Paleocene (Torrejonian), the time
of appearance of the oldest mesonychian,
Dissacus, a result also supported by other
phylogenetic analyses (Geisler and Luo,
1998; O’Leary, 1998a). This tree topology
speciŽes the existence of a cetacean ghost
lineage ~ 10 million years long that remains to be discovered, something also
suggested by the large number of synapomorphies uniting cetaceans (Table 2; Fig. 2:
node e). This estimate of the time of origin of Cetacea is greater than likelihoodbased estimates (Gingerich and Uhen,
1998), which place the origin of Cetacea
in the Eocene, much closer to the Žrst
appearance of archaeocetes in the fossil
record.
As emphasized by the count of extinct
and extant taxa relevant to the question of
the position of Cetacea within Mammalia
(Table 1), this analysis only begins to sample the diverse array of taxa likely to impact
the position of Cetacea within Mammalia.
Besides numerous extinct artiodactyls and
perissodactyls, 12 other mesonychian genera and Žve other triisodontine genera,
known from fragmentary remains, are likely
to affect the relationships presented here
(McKenna and Bell, 1997). Furthermore,
located either within the ungulate clade or
as stem taxa to it are 65 other “condylarth” genera (McKenna and Bell, 1997),
many of which are also poorly known
and have not been scored here. Other critical taxa include the pakicetid Nalacetus,
which has been argued to have the most
primitive dental morphology of any known
cetacean (O’Leary, 1998a; Thewissen and
Hussain, 1998); Chriacus (Rose, 1996), which
exhibits modiŽcations of the postcranial
skeleton that suggest a link between arctocyonid “condylarths” and basal artiodactyls;
Microclaenodon, a triisodontine arctocyonid,
which is the Žrst outgroup to Mesonychia
on the basis of dental evidence (O’Leary,
1998a), but which is known from little other
material; and Sinonyx (Zhou et al., 1995), a
mesonychian from the Paleocene of Asia,
which is well-preserved postcranially but
remains undescribed. Discovery and description of material of these key fossils will
be crucial for testing the stability of the tree
topologies presented here.
ACKNOWLEDGMENTS
We acknowledge the generosity of many colleagues
who provided helpful discussion and access to specimens, including undescribed fossil material: P. D. Gingerich, R. E. Heinrich, E. Heizmann, L. T. Holbrook,
S. G. Lucas, W. P. Luckett, D. Lunde, Z. Luo, R. D. E.
MacPhee, P. J. Makovicky, M. C. McKenna, M. J. Novacek, K. D. Rose, A. E. Sanders, N. B. Simmons, and
J. G. M. Thewissen. We are particularly grateful to J. G.
M. Thewissen for unpublished data on Ambulocetus, to
M. D. Uhen for assisting with the coding of Dorudon,
to L. B. Nash for preparing Figure 1, and to C. Heezy
who provided data on the postorbital bars of several
1999
O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
ungulates. M. J. Novacek, C. F. Ross, and D. M. Sabatini
generously allowed us to conduct hours of phylogenetic analysis on their computers. R. J. Asher, J. Gatesy,
G. J. P. Naylor, M. J. Novacek, C. F. Ross, N. B. Simmons,
J. B. Slowinski, and W. C. Wheeler read and greatly improved earlier versions of the manuscript.
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Received 29 April 1998; accepted 14 August 1998
Associate Editor: G. Naylor
APPENDIX 1.
SPECIMENS AND LITERATURE REFERENCES USED
TO C OMPILE THE C HARACTER -T AXON MATRIX
FOR PARSIMONY ANALYSIS
Data on the deciduous fourth premolar throughout
matrix are from Luckett and Hong (1998). AMNH-M
= Department of Mammalogy, AMNH-VP, Department of Vertebrate Paleontology, American Museum
of Natural History, New York; ChM PV = Charleston
Museum, Charleston, South Carolina; GSP-UM = Geological Survey of Pakistan/University of Michigan,
Ann Arbor; H-GSP = Howard University/Geological
Survey of Pakistan, Washington, D.C.; IVPP = Institute
of Vertebrate Paleontology and Paleoanthropology, Bei-
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SYSTEMATIC BIOLOGY
jing, China; MCZ = Museum of Comparative Zoology,
Harvard University, Cambridge, Massachusetts;
NMMNH = New Mexico Museum of Natural History, Albuquerque; USGS = Johns Hopkins University/United States Geological Survey (now at the
Smithsonian Institution, Washington, D.C.); USNM =
National Museum of Natural History, Smithsonian Institution, Washington, D.C.; YPM = Yale Peabody Museum, New Haven, Connecticut; YPM-PU, Princeton
University collection (now at Yale Peabody Museum).
Archaic Ungulates
Andrewsarchus.—AMNH-VP 20135; Chow (1959).
Arctocyon.—AMNH-VP 55900 (cast) , 55901 (cast),
55902; Russell (1964).
Eoconodon.—AMNH-VP 764, 774, 3177, 3181, 3187,
3280, 4052, 16329, 16341; Matthew (1897, 1937).
Hyopsodus.—AMNH-VP 1, 39, 1717, 10977, 10979,
11330, 11349, 11350, 11363, 11393, 11415, 11899; Gazin
(1968); Thewissen and Domning (1992).
Meniscotherium.—AMNH-VP 2560, 4414, 4426, 4434,
4447, 48083, 48126, 48129, 48555; Gazin (1965); Cifelli
(1982); Williamson and Lucas (1992).
Phenacodus.—AMNH-VP, 2961, 4370, 4378, 4403,
15262, 15266, 15268, 15271, 15275, 15279, 15284, 15286,
117195; Thewissen (1990); O’Leary and Rose (1995b).
Artiodactyla
Agriochoerus.—AMNH-VP 685, 1349, 1355, 7407,
7409, 9808, 9811, 38843, 38932, 95324, 95332, 99275.
Archaeotherium.—AMNH-VP 39127, 39455.
Camelus.—AMNH-M 2911, 14109, 35463, 35563,
69405, 80227, 90433; Smuts and Bezuidenhout (1987);
Langer (1988 [based on condition in Llama]).
Diacodexis.—AMNH-VP 16141; USGS 2352; Rose
(1982, 1985); Russell et al. (1983); Thewissen et al. (1983);
Thewissen and Hussain (1990); Thewissen (1994).
“Elomeryx”-(includes specimens attributed to Bothriodon).—AMNH-VP 579, 582, 583, 1242, 1245, 1259, 1483,
10041, 12461, 39015, 101668; Scott (1894).
Hexaprotodon.—AMNH-M 2423, 54265, 81899, 89626,
146848, 146849, 148452, 185383, 202423; Vaughan (1986);
Langer (1988); Sokolov (1982).
Hippopotamus.—AMNH-M 15898, 24282, 24284,
24285, 24289, 53773, 54248, 80813, 81856, 130247, 176118;
Vaughan (1986); Langer (1988); Sokolov (1982).
Ovis.—AMNH-M 6231, 6239, 10074, 14515, 15584,
35520, 53598, 88702, 100012, 100072, 146547; Sisson and
Grossman (1953); Langer (1988); Sokolov (1982).
Poebrotherium.—AMNH-VP 8955, 39085, 42240,
42248, 42249, 42261, 42272, 42276, 42281, 42284, 42292,
47003, 47008, 47052, 47103, 47182, 47284, 47317, 47324,
47333, 47077, 47907, 63701, 63704, 63712, 63713, 97103.
Sus.—AMNH-M 20871, 69422, 69442, 100260,
235190, 235192, 236144, 238325, 238331; Sisson and
Grossman (1953); Langer (1988); Sokolov (1982).
Tragulus.—AMNH-M 10101, 14137, 14139, 34252,
32645, 53602, 53609, 60759, 90101, 90193, 102091, 102176,
106552, 240913; Langer (1988); Sokolov (1982).
Balaenoptera.—AMNH-M 28274, 84870, 148407,
219212, 219220; Daudt (1898); Muller (1898); Sokolov
(1982); Gaskin (1978).
Basilosaurus.—AMNH-VP 14381, 129577 (cast); GSPUM 97507; Kellogg (1936).
Cross Whale.—ChM PV 5401; Geisler et al. (1996).
Dorudon.—Uhen (1996, 1998).
Pakicetus.—GSP-UM 084 (cast); H-GSP 96231, 96386,
96431, 18410, 18570, 96505; Gingerich and Russell
(1981, 1990); Thewissen and Hussain (1993); Thewissen
(1994); Thewissen and Hussain (1998).
Protocetus.—Fraas (1904).
Remingtonocetus.—GSP-UM 3009, 3054, 3057; Kumar
and Sahni (1986); Gingerich et al. (1995).
Tursiops.—AMNH-M 120920, 184930, 212554; Daudt
(1898 [based on condition in other odontocetes]);
Muller (1898 [based on condition in other odontocetes]);
Langer (1988).
Mesonychidae
Ankalagon.—AMNH-VP 776, 777, 2454; NMMNH
16309.
Dissacus.—AMNH-VP 3356, 3357, 3359, 3360, 3361,
15996, 39276, 55925 (cast); IVPP 4266 (cast); YPM-PU
16159; O’Leary and Rose (1995a, 1995b).
Harpagolestes.—AMNH-VP 1878, 1892, 1945, 2308,
26267, 26300, 26301; USNM 14708, 14915; Wortman
(1901); Peterson (1931); West (1981); Zhou et al. (1995).
Mongolestes.—AMNH-VP 26064, 26065.
Mongolonyx.—AMNH-VP 26661, 26662.
Mesonyx.—AMNH-VP 1716, 5021, 11552, 12641,
12643 (cast), 19204, 122122; Scott (1888); O’Leary and
Rose (1995b).
Pachyaena.—AMNH-VP 72, 75, 1522, 2823, 2959,
4262, 15224, 15228, 15728, 15730, 16154; USGS 7185;
YPM 50000; YPM-PU 14708; O’Leary and Rose (1995a,
1995b); Rose and O’Leary (1995).
Sinonyx.—VPP V10760 (skull and lower dentition);
Zhou et al. (1995).
Synoplotherium.—AMNH-VP 19203,
122122; Wortman (1901).
Hapalodectidae
Hapalodectes.—AMNH-VP 78, 12781, 14748 (cast),
128561, 17558, 20172, 80802 (cast); IVPP 5254 (cast);
USGS 275 (cast), 9628, 10293 (cast); Guthrie (1967); Szalay (1969a); Ting and Li (1987); Zhou and Gingerich
(1991); O’Leary (1998b).
Perissodactyla
Equus.—AMNH-M 1244C, KMM 99; AMNH-VP 113
(VP), LA 118; Sisson and Grossman (1953); Vaughan
(1986); Langer (1988).
Heptodon.—AMNH-VP 294, 4855, 4858, 14865, 14884,
16861, 141881; Radinsky (1965).
Hyracotherium.—AMNH-VP 55267, 55268, 55269,
96274, 96277, 96284, 96298, 129209; Kitts (1956); MacFadden (1992); Rose (1990); Thewissen and Domning
(1992).
Cetacea
Ambulocetus.—H-GSP 18507; Thewissen et al. (1996);
Thewissen pers. comm. (pelvis data).
Outgroups
Asioryctes.—Kielan-Jaworowska (1977, 1981).
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
Didelphis.—AMNH-M 7310, 14335, 70089, 180358,
217701, 219212, 219220, 240517, 242660; Bremer (1904);
McCrady (1940); Vaughan (1986); Langer (1988).
Leptictis.—AMNH-VP 1413a, 5346, 38920, 39444,
90256, 96766; MCZ 19678; USNM 336367; Novacek
(1980, 1986).
APPENDIX 2. CHARACTERS AND CHARACTER
STATES FOR PARSIMONY ANALYSIS
Multistate characters treated as ordered are speciŽed below. The character-taxon matrix is presented in
Appendix 3.
Basicranial Characters
1. Subarcuate fossa.—Present (0); absent (1) (Novacek,
1986).
2. Shape of tegmen tympani (ordered).—Uninated,
forms thin lamina lateral to facial nerve canal (0);
inated, forms barrel-shaped ossiŽcation lateral to
the facial nerve canal (1); hyperinated, transverse
width greater than or equal to width of promontorium (2) (modiŽed from Cifelli, 1982; Geisler and
Luo, 1998).
3. Anterior process of petrosal.—Absent (0); present, anterior edge of tegmen tympani extending far anterior to edge of pars cochlearis (1) (Luo and Marsh,
1996; Geisler and Luo, 1998).
4. Fossa for tensor tympani muscle.—Shallow, anteroposteriorly elongate fossa (0); circular pit, no groove (1);
circular pit with deep tubular anterior groove (2);
long narrow groove between tegmen tympani and
promontorium (3) (Luo and Marsh, 1996; Geisler
and Luo, 1998).
5. Transpromontorial sulcus for internal carotid artery.—
Present, forms anteroposterior groove on promontorium, medial to fenestrae rotunda and ovalis (0);
absent (1) (Cifelli, 1982; Thewissen and Domning,
1992).
6. Sulcus on promontorium for proximal stapedial artery.—
Present, forms a groove that branches from the
transpromontorial sulcus anteromedial to the fenestra rotunda and extends to the medial edge of the
fenestra vestibuli (0); absent (1) (Cifelli, 1982; Wible,
1987; Thewissen and Domning, 1992).
7. Mastoid process of petrosal.—Exposed externally on
posterior face of braincase as a triangle between
lambdoidal crest of the squamosal dorsolaterally,
the exoccipital ventrally, and the supraoccipital medially (0); not exposed posteriorly, lambdoidal crest
of squamosal in continuous contact with exoccipital
and supraoccipita l (1).
8. Stylomastoid foramen.—Complete, ectotympanic
contacts tympanohyal laterally and petrosal medially, in some cases ectotympanic separated from
petrosal by a narrow (< 1 mm) Žssure (0); incomplete, ectotympanic does not contact the petrosal
either anterior or posterior to the fenestra rotunda,
medial side of foramen open (1) (modiŽed from
Geisler and Luo, 1998).
9. Facial nerve sulcus distal to stylomastoid foramen.—
Absent (0); present, anterior wall of sulcus formed
by squamosal (1); present, anterior wall formed by
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
485
mastoid process of petrosal (2); anterior wall formed
by meatal tube of ectotympanic (3) (modiŽed from
Geisler and Luo, 1996, 1998). Some taxa coded as
polymorphic for this character are not truly polymorphic, and the character state is simply ambiguous, but certain states can be eliminated from the
list of possibilities.
Articulation of pars cochlearis with basisphenoid/basioccipital.—Present (0); absent (1) (Thewissen and
Domning, 1992).
Ectotympanic.—Simple ring, no bulla formation (0);
medial edge expanded into bulla (1) (derived from
Novacek, 1977; MacPhee, 1981; Geisler and Luo,
1998).
Pachyosteosclerotic involucrum of bulla.—Absent (0);
present (1) (Thewissen, 1994).
Lateral furrow of tympanic bulla.—Absent (0); present,
forms a groove on the lateral surface of the ectotympanic bulla anterior to the base of the sigmoid
process or meatal tube (1) (Geisler and Luo, 1998).
Median furrow of tympanic bulla for tympanohyal
(ordered).—Absent (0); median notch on posterior
rim of bulla (1); prominent anteroposteriorly oriented furrow splits the ventral surface of the bulla
into medial and lateral halves (2) (Geisler and Luo,
1998).
Articulation of ectotympanic bulla to squamosal
(ordered).—Broad articulation with medial base of
postglenoid process (0); circular facet on short entoglenoid process (1); contact with a crest of the entoglenoid process (2); contact absent (3) (Geisler and
Luo, 1998).
Contact between exoccipital and ectotympanic bulla.—
Absent (0); present (1) (Geisler and Luo, 1998).
Sigmoid process (= anterior crus of tympanic ring).—
Absent (0); present, forms transverse plate that
projects laterally from the anterior crus of the ectotympanic ring and forms the anterior wall of the external auditory meatus (1) (modiŽed from Thewissen, 1994; Geisler and Luo, 1998).
Sigmoid process shape.—Thin and transverse plate
(0); broad and aring, base of the sigmoid process
forms dorsoventral ridge on lateral surface of ectotympanic bulla (1) (Geisler and Luo, 1998).
Ectotympanic part of the meatal tube (ordered).—
Absent (0); present but short, length of tube < 30%
maximum width of bulla (1); present and long,
length > 60% maximum width of bulla (2) (Geisler
and Luo, 1998).
Squamosal portion of external auditory meatus.—
Absent or shallow, depth < 25% of transverse length
(0); deep groove, depth > 35% of transverse length
(1).
Basioccipital crests (falcate processes).—Absent (0);
present, forming ventrolaterall y aring basioccipital processes (1) (derived from Barnes, 1984; modiŽed from Thewissen, 1994).
Internal carotid foramen.—Absent or conuent with
the piriform fenestra (0); present at basisphenoid/basioccipital suture with lateral wall of foramen formed by both these bones and thus separated from the piriform fenestra (1) (Geisler and
Luo, 1998).
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SYSTEMATIC BIOLOGY
23. Postglenoid foramen (ordered).—Present, enclosed
by squamosal, immediately posterior to postglenoid process (0); present, medial to petrosal/squamosal suture (if bulla present, a secondary ventral opening between bulla and
squamosal may form) (1); absent (2) (Novacek,
1986; Geisler and Luo, 1998).
24. Foramen for ramus superior of stapedial artery.—
Present (0); absent (1) (modiŽed from Novacek,
1986; Thewissen and Domning, 1992).
25. Position of foramen for ramus superior of stapedial
artery.—In petrosal/squamosal suture on dorsolateral edge of epitympanic recesss (0); anterolateral to
epitympanic recess (1) (modiŽed from Geisler and
Luo, 1998). Cannot be scored for taxa that lack a foramen for the ramus superior of the stapedial artery.
26. Foramen ovale.—Anterior to glenoid fossa, posterior
wall formed by alisphenoid (0); medial to glenoid
fossa, posterior wall formed by alisphenoid (1); medial to glenoid fossa, posterior wall formed by petrosal (2); posterior to glenoid fossa (3).
27. Alisphenoid canal (alar canal).—Absent (0); present
(1) (Novacek, 1986; Thewissen and Domning, 1992).
28. Anterior opening of alisphenoid canal.—Within sphenorbital Žssure, cannot be distinguished from sphenorbital Žssure in lateral view (0); posterior to sphenorbital Žssure (1) (Novacek, 1982; Thewissen and
Domning, 1992).
29. Posterior opening of alisphenoid canal.—Wellseparated from foramen ovale (0); within a deep
groove or recess with the foramen ovale (1) (derived from Zhou et al., 1995).
30. Foramen rotundum.—Absent, maxillary division of
trigeminal nerve exits skull through sphenorbital
Žssure (0); present (1) (Novacek, 1986; Thewissen
and Domning, 1992).
31. Mastoid foramen.—Present, skull in posterior view
(0); absent (1) (deŽnition of structure follows
MacPhee, 1994).
32. Post-temporal canal (for arteria diploetica magna,
also called pericranial foramen).—Present, occurs
at petrosal/squamosal suture with skull in posterior view, the canal continuing within the petrosal/squamosal suture (0); absent (1) (Wible, 1990;
MacPhee, 1994).
33. Preglenoid process.—Absent (0); present, forms transverse, ventrally projecting ridge at anterior edge of
glenoid fossa (1) (modiŽed from Thewissen, 1994).
Cranial Characters
34. Supraorbital process.—Absent, region over orbit does
not project laterally from sagittal plane (0); present,
laterally elongate and tabular (1) (derived from
Barnes, 1984).
35. Postorbital bar (ordered).—Absent (0); present and
almost complete (1); present and complete (2).
36. Contact of frontal and maxilla in orbit.—Absent (0);
present (1).
37. Lacrimal tubercle.—Absent (0); present, situated on
anterior edge of orbit adjacent to the lacrimal foramen (1) (Novacek, 1986).
38. Palatine Žssure.—Small (0); large (1).
39. Posterior margin of external nares (ordered).—
Anterior to or over the canines, or at anterior edge of
premaxilla if canine not present (0); between P1 and
P2 (1); posterior to P2 (2) (Geisler and Luo, 1998).
40. Mandibular foramen.—Small, maximum height of
opening # 25% the height of the mandible at M3 (0);
large, continuous with a large posterior fossa, maximum height $ 50% the height of the mandible at
M3 (1) (modiŽed from Thewissen, 1994; Geisler and
Luo, 1998).
41. Height of mandibular condyle relative to dentition
(ordered).—Below level of the dentition (0); even
with superior aspect of dentition (1); substantially
superior to dentition (2).
42. Angle of dentary.—Distal end at same level as ventral edge of dentary below molars (0); forms distinct ange that projects posteroventrally well below ventral edge of dentary (1) (modiŽed from Gentry and Hooker, 1988).
Dental Characters
43. Upper incisors.—Present (0); absent (1).
44. Premaxillae.—Short with incisors arranged in transverse arc (0); elongate, incisors aligned longitudinally with intervening diastemata (1) (modiŽed
from Prothero et al., 1988; Thewissen, 1994).
45. Embrasure pits on palate.—Absent (0); present (1)
(modiŽed from Thewissen, 1994).
46. P1 (ordered).—Absent (0); present, one-rooted (1);
present, two-rooted (2) (Zhou et al., 1995).
47. P3 roots.—Three (0); two (1) (Zhou et al., 1995).
48. P4 protocone.—Present (0); absent (1) (Thewissen,
1994).
49. P4 paracone.—Equal or subequal to height of paracone of M1 (0); greater than twice the height of M1
paracone (1) (Thewissen, 1994).
50. P4 metacone.—Absent (0); present (1) (Thewissen,
1994).
51. Stylar shelf.—Present (0); absent (1).
52. M2 metacone (ordered).—Distinct cusp, sub-equal to
paracone (0); distinct cusp approximately half the
size of the paracone (1); highly reduced, indistinct
from paracone (2) (Zhou et al., 1995).
53. M1 parastyle (ordered).—Absent (0); weak (1); moderate to strong (2) (O’Leary, 1998a) .
54. Lingual cingulum on M2 .—Present (0); absent (1)
(O’Leary, 1998a).
55. Ectocingula.—Present (0); absent (1) (O’Leary,
1998a).
56. M1 -M2 hypocone.—Absent (0); present (1) (Thewissen and Domning, 1992; O’Leary, 1998a).
57. Trigon basin (ordered).—Broad (0); somewhat narrow (1); very narrow (2) (modiŽed from Thewissen,
1994; O’Leary, 1998).
58. Paraconule on M2 .—Absent (0); present (1) (O’Leary,
1998a).
59. Metaconule on M2 .—Absent (0); present (1) (O’Leary,
1998a).
60. M3 size (ordered).—Present, larger than M2
(0); present, approximately equal to M2
(1);
present,
small,
maximum
mesiodistal length than < 60% the length of M2
(2); absent (3) (modiŽed from Zhou et al.,
1995).
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
487
61. Lower canines.—Approximately twice as large as in- 85. M3 hypoconulid.—Long, protrudes as separate discisors or larger (0); subequal in size to incisors, well
tal lobe (0); short, does not protrude substantially
separated from postcanine teeth (1).
beyond rest of talonid (1); absent (2) (Thewissen,
1994).
62. Lower incisors.—Small and vertical (0); tusk-like (1).
63. Lower canine cross-section shape.—Oval (0); triangu- 86. dp4 .—Resembles M1 (0); six-cusped, additional
neomorphic cusp on paracristid (1) (Gentry and
lar (1) (Gentry and Hooker, 1988).
Hooker, 1988; Luckett and Hong, 1998).
64. P1 .—Present (0); absent (1) (Zhou et al., 1995).
65. P3 metaconid.—Absent (0); present (1) (Thewissen 87. Elongate shearing facets on lower molars extending below the gum line.—Absent (0); present (1).
and Domning, 1992).
66. P4 metaconid.—Absent (0); present (1) (Thewissen
and Domning, 1992).
Postcranial Characters
67. Lingual cingulid on lower molars.—Poorly deŽned or 88. Cervical vertebrae.—Long, length of centrum greater
absent (0); continuous from mesial to distal extreme
than or equal to the centra of the anterior thoracics
(1) (O’Leary, 1998a).
(0); short, length shorter than centra of anterior tho68. M1 paraconid.—Present (0); absent (1) (derived from
racics (1); very long (2) (derived from Gingerich et
O’Leary, 1998a) .
al., 1995).
69. M1 paraconid/paracristid position.—Cusp lingual or 89. Articulation between sacral vertebrae and ilium of
paracristid winding lingually (or both) (0); cusp
pelvis (ordered).—Broad area of articulation beanterior or paracristid (or both) straight mesiodistween pelvis and S1 and sometimes S2 (0); narrow
tally, sometimes poorly developed (1) (derived from
articulation of pelvis with end of transverse process
O’Leary, 1998a) .
of S1 (1); articulation absent (2) (Geisler and Luo,
70. M2 paraconid.—Present (0); absent (1) (derived from
1998).
O’Leary, 1998a) .
90. Number of sacral vertebrae (ordered).—One (0); two
71. M2 paraconid/paracristid position.—Cusp lingual or
or three (1); four (2); Žve or six (3); cannot be scored
paracristid (or both) winding lingually (0); cusp anfor taxa that lack an articulation between the verteterior or paracristid (or both) straight mesiodistally,
bral column and the ilium (Thewissen and Domnsometimes poorly developed (1) (O’Leary, 1998a) .
ing, 1992; Gingerich et al., 1995).
72. M3 paraconid.—Present (0); absent (1) (O’Leary, 91. Scapular spine.—Bears large acromion pro1998a).
cess that overhangs glenoid fossa (0); scapu73. M3 paraconid/paracristid position.—Cusp lingual or
lar spine with acromion process small or abparacristid winding lingually (or both) (0); cusp ansent, does not encroach upon glenoid fossa (1);
terior or paracristid (or both) straight mesiodistally,
acromion process large, directed anteriorly and
sometimes poorly developed (1) (O’Leary, 1998a) .
does not encroach upon the glenoid fossa (2)
74. M1 metaconid.—Present, forms distinct cusp (0); ab(O’Leary and Rose, 1995b; Geisler and Luo,
sent or occasionally present as swelling on lingual
1998).
side of protoconid (1) (Thewissen, 1994; Zhou et al., 92. Entepicondyle of humerus.—Wide, $ 50% width of ul1995).
nar and radial articular facets (0); narrow, # 25%
75. M2 metaconid.—Present, forms distinct cusp (0); abwidth of ulnar and radial articular facets (1) (desent or occasionally present as swelling on lingual
rived from O’Leary and Rose, 1995b; Geisler and
side of protoconid (1) (modiŽed from Zhou et al.,
Luo, 1998).
1995).
93. Entepicondylar foramen.—Present (0); absent (1)
76. M3 metaconid.—Present, forms distinct cusp (0); ab(Thewissen and Domning, 1992).
sent or occasionally present as swelling on lingual 94. Length of olecranon process.—Short, < 10% total ulside of protoconid (1) (modiŽed from Zhou et al.,
nar length (0); long, > 20% total ulnar length (1)
1995).
(derived from O’Leary and Rose, 1995b).
77. M1 -M2 hypoconulid.—Absent (0); present (1) (The- 95. Olecranon fossa.—Shallow (0); deep, sometimes perwisen, 1994).
forate (1) (modiŽed from O’Leary and Rose, 1995b).
78. Molar protoconid.—Subequal to height of talonid 96. Proximal end of radius.—Single fossa for trochlea and
(0); closer to twice height of talonid or greater (1)
capitulum of humerus (0); two fossae, one for the ca(O’Leary, 1998a).
pitulum and one for the medial edge of trochlea (1);
79. Protoloph.—Absent (0); present (1).
three fossae, same as (1) but with additional fossa
80. Metaloph.—Absent (0); present (1).
for the lateral lip of the humeral articular surface (2)
81. Metalophid formation on anterior aspect of lower teeth
(O’Leary and Rose, 1995b; Geisler and Luo, 1998).
(between protoconid and metaconid).—Absent (0); 97. Distal articular surface of radius.—Single concave
present (1).
fossa (0); split into scaphoid and lunate fossae (1);
82. Hypolophid formation on posterior aspect of lower teeth
convex to at, distinct facets (2) (derived from
(between entoconid and hypoconid).—Absent (0);
O’Leary and Rose, 1995b).
present (1) (Thewissen and Domning, 1992).
98. Centrale.—Present (0); (1) absent (Thewissen, 1994).
83. Reentrant grooves.—Proximal (0); absent (1); distal 99. Manus.—Mesaxonic, axis of symmetry passes along
(2) (Thewissen, 1994; O’Leary, 1998a).
center of digit 3 (0); paraxonic, axis of symmetry
84. Molar talonid.—Basined, or slightly basined,
passes between digits three and four (1).
hypoconid and entoconid present (0); reduced (1) 100. Height of greater trochanter of femur (ordered).—
(modiŽed from Thewissen, 1994).
Inferior to head of femur (0); approximately equal to
488
101.
102.
103.
104.
105.
106.
107.
108.
109.
110.
111.
112.
VOL. 48
SYSTEMATIC BIOLOGY
head of femur (1); above head of femur (2) (derived
from O’Leary and Rose, 1995b).
Third trochanter of femur (ordered).—Present (0);
highly reduced (1); absent (2) (derived from O’Leary
and Rose, 1995b).
Patellar articular surface on femur.—Wide (0); narrow
(1).
Astragalar canal.—Present (0); absent (1) (derived
from Shoshani, 1986).
Navicular facet of astragalus (ordered) (see Fig. 1).—
Convex (0); saddle-shaped (1); trochleated (2) (modiŽed from Thewissen and Domning, 1992; O’Leary
and Rose, 1995b).
Sustentacular width.—Narrow, # 50% width of the
astragalus (0); wide, $ 70% width of the astragalus
(1) (Geisler and Luo, 1998).
Contact of distal astragalus with cuboid (ordered)
(see Fig. 1).—Absent (0); present but small, contact
# 30% of the width of the distal articular surface (1);
present and large, contact $ 40% of the articular surface (2) (O’Leary and Rose, 1995b; Geisler and Luo,
1998).
Lateral process of astragalus.—Present (0); absent (1)
(Schaeffer, 1956).
Pes (ordered).—Mesaxonic, axis of symmetry of foot
passes along center of digit three (0); paraxonic, axis
lies between digits three and four (1); mesaxonic,
axis passes along center of digit four (2) (derived
from Gingerich et al., 1990; Thewissen, 1994; our
interpretation of this character differs from that of
these previous authors).
Proximal astragalus (ordered).—Nearly at to
slightly concave (0); grooved, depth of trochlea
< 25% width of trochlea (1); deeply grooved, depth
of trochlea > 30% width of trochlea (2) (derived
from Schaeffer, 1947; O’Leary and Rose, 1995b).
Cuboid and navicular.—Unfused (0); fused (1) (Webb
and Taylor, 1980).
Proximal fusion of third and fourth metatarsals.—
Absent (0); present (1).
First metatarsal (ordered).—Unreduced, length >
50% length of third metatarsal (0); reduced, length
< 50% length of third metatarsal (1); highly reduced
in form of nodule or small splint or absent (2).
113. Second metatarsal (ordered).—Unreduced, length
$ 50% length of third metatarsal (0); reduced, length
# 50% length of third metatarsal (1); highly reduced in form of nodule, small splint or completely
absent (2).
114. Fifth metatarsal (ordered).—Unreduced, length
$ 50% length of third metatarsal (0); reduced,
length # 50% length of third metatarsal (1); highly
reduced in form of nodule or small splint or
absent (2).
115. Ventral border of distal phalanges.—Curved inferiorly
(0); straight (1) (derived from MacLeod and Rose,
1993).
116. Distal phalanges in dorsal view.—Phalanx compressed transversely (0); broad transversely, each
phalanx bilaterally symmetrical with central anteroposterior axis (1); broad transversely, each phalanx
asymmetrical (2) (derived from MacLeod and Rose,
1993).
Soft Tissue Characters
117. Stomach epithelium.—Nonglandular (stratiŽed squamous epithelium) (0); composite (nonglandular
and glandular mucosa) (1); discoglandular (small
patches of glandular epithelium surrounded by
nonglandular mucosa) (2); glandular (mucosa with
glands) (3) (derived from Langer, 1988).
118. Lumen.—Unilocular (stomach with simple chamber only) (0); plurilocular (lumen of stomach subdivided by folds into two or more chambers) (1)
(derived from Langer, 1988).
119. Diverticulation of stomach lumen (blind tubes or sacs
branching from the main gastric lumen).—Absent
(0); present (1) (derived from Langer, 1988).
120. Cavernous tissue of penis.—Abundant (0); sparse (1)
(derived from Slijper, 1936; Thewissen, 1994).
121. Hair.—Abundant to common on body (0); almost
completely absent (1) (Gatesy, 1997).
122. Sebaceous glands.—Present (0); absent (1) (Gatesy,
1997).
123. Primary bronchi of lung.—Two (0); three (1) (Thewissen, 1994).
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O’LEARY AND GEISLER—PHYLOGENY OF CETACEA
489
APPENDIX 3. Data matrix of 123 characters for 40 taxa. ? = missing data; n = inapplicable character; character
states described in Appendix 2. Polymorphic characters as follows: states 0 and 1 = 5; 0 and 2 = 6; 0 and 3 = 7;
1 and 2 = 8; 2 and 3 = 9; earliest appearance of the genus (McKenna and Bell, 1997) (E. = early; M. = middle; L.
= late; Cret. = Cretaceous; Pal. = Paleocene; Eoc. = Eocene; Mioc. = Miocene; Pleist. = Pleistocene), and percent
missing data listed at end of matrix. Characters in bold are treated as ordered in certain analyses, extant taxa in
bold. The matrix is available at http://www.herbaria. harvard.edu/treebase/ under the accession number S387.
(continued on next page)
490
SYSTEMATIC BIOLOGY
APPENDIX 3.
(Continued)
VOL. 48