Integrative and Comparative Biology

Integrative and Comparative Biology, volume 56, number 6, pp. 1271–1284

doi:10.1093/icb/icw128 Society for Integrative and Comparative Biology

SYMPOSIUM

From Teeth to Baleen and Raptorial to Bulk Filter Feeding in

Mysticete Cetaceans: The Role of Paleontological, Genetic, and
Geochemical Data in Feeding Evolution and Ecology

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Annalisa Berta,1,* Agnese Lanzetti,* Eric G. Ekdale*,† and Thomas A. Deméré†
*Department of Biology, San Diego State University, San Diego, CA 92182, USA; †Department of Paleontology, San
Diego Natural History Museum, San Diego, CA 92101, USA
From the symposium ‘‘Functional (Secondary) Adaptation to an Aquatic Life in Vertebrates’’ presented at the
International Congress of Vertebrate Morphology (ICVM11), June 29–July 3, 2016 at Washington DC.
1
E-mail: aberta@mail.sdsu.edu

Synopsis The origin of baleen and filter feeding in mysticete cetaceans occurred sometime between approximately 34
and 24 million years ago and represents a major macroevolutionary shift in cetacean morphology (teeth to baleen) and
ecology (raptorial to filter feeding). We explore this dramatic change in feeding strategy by employing a diversity of tools
and approaches: morphology, molecules, development, and stable isotopes from the geological record. Adaptations for
raptorial feeding in extinct toothed mysticetes provide the phylogenetic context for evaluating morphological apomor-
phies preserved in the skeletons of stem and crown edentulous mysticetes. In this light, the presence of novel vascular
structures on the palates of certain Oligocene toothed mysticetes is interpreted as the earliest evidence of baleen and
points to an intermediate condition between an ancestral condition with teeth only and a derived condition with baleen
only. Supporting this step-wise evolutionary hypothesis, evidence from stable isotopes show how changes in dental
chemistry in early toothed mysticetes tracked the changes in diet and environment. Recent discoveries also demonstrate
how this transition was made possible by radical changes in cranial ontogeny. In addition, genetic mutations and the
possession of dental pseudogenes in extant baleen whales support a toothed ancestry for mysticetes. Molecular and
morphological data also document the dramatic developmental shifts that take place in extant fetal baleen whales, in
skull development, resorption of a fetal dentition and growth of baleen. The mechanisms involved in this complex
evolutionary transition that entails multiple, integrated aspects of anatomy and ecology are only beginning to be under-
stood, and future work will further clarify the processes underlying this macroevolutionary pattern.

Introduction genes, as well as deciduous tooth buds that form early

Mysticetes (baleen whales) include the largest animals
to have ever lived on Earth. Extant postnatal mysti-
cetes lack mineralized teeth, in contrast to the condi-
tion in the majority of their odontocete (toothed
whale) evolutionary cousins, and instead are unique
among mammals in their possession of baleen, a neo-
morphic palatal keratinous structure employed during
bulk filter feeding. The evolution of baleen represents
a major macroevolutionary shift in cetacean morphol-
ogy and ecology. Although living mysticetes are eden-
tulous, there is both genetic and ontogenetic evidence
of a toothed ancestry for baleen whales represented by
the presence of functional and non-functional tooth
in fetal development. The geological record (i.e., fos-
sils and stable isotopes) allows us to test the hypoth-
esis of a toothed ancestry for mysticetes using
historical data directly, and an integration of morpho-
logical, molecular, developmental, paleontological, and
geochemical data elucidates the transition from ances-
tral raptorial feeding using teeth to bulk filter feeding
using baleen.
Anatomy and feeding in extant
mysticetes
The key innovation of the unique filter feeding phys-
iology of mysticetes is baleen, which functions as a

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1272
Skimming
Suctioning
Feeding pits
Fig. 1 Mysticete feeding types (from Berta et al. 2015b).
natural sieve to trap prey items during bulk feeding
(Pivorunas 1979; Werth 2001, 2004, 2013). Baleen is
composed of keratin (Fudge et al. 2009; Szewciw et
al. 2010) and consists of a serially arranged row of
keratinous laminae and bristles that grow as a pair of
subparallel longitudinal racks from the right and left
lateral margins of the palate (Williamson 1973;
Werth 2001; Young et al. 2015). Individual baleen
laminae are roughly triangular in shape and are di-
visible into main plates, minor plates, and individual
bristles. The main and minor plates consist of a cen-
tral, medullary layer of keratin tubules enmeshed in
an amorphous keratin matrix. On either side of the
medullary layer is a cortical layer of amorphous ker-
atin. Each rack of baleen is deeply rooted within
vascularized gingival tissues (Utrecht 1965). Baleen
consists proximally of living tissue that receives
blood from the superior alveolar arteries (Ekdale et
al. 2015), and distally of the dead and cornified
tissue that extends into the oral cavity. As baleen
grows in the mouth, the lingual border of the
plates is abraded and frayed to expose the bristles
(Werth et al. 2016). The free bristles on one
lamina overlap with the bristles of adjacent laminae
to form a dense, brush-like mat—the baleen filter.
A. Berta et al.
Lunging
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Engulfing
All extant mysticetes share four fundamental func-
tional components related to bulk feeding: a large
head and mouth, rostral bones that are rather loosely
articulated with the braincase and with each other,
an elastic mandibular symphysis, and baleen. All of
those features help to either filter food from water
(e.g., baleen), or to expand the oral cavity to facili-
tate an intake of large volumes of water.
Morphological variations in these general mysticete
features as exhibited by living baleen whales include
further enlargements of the oral cavities, which can
be viewed as adaptations for different strategies of
bulk filter feeding (Fig. 1), including continuous
ram or skim feeding in balaenids (bowhead and
right whales) and presumably neobalaenids (pygmy
right whale), intermittent ram or engulfment/lunge
feeding in balaenopterids (rorquals and humpback
whales), and suction feeding in eschrichtiids (gray
whales) (see Supplementary Material).
One outstanding question in the acquisition of prey
by mysticetes is how baleen whales detect and locate
their food. Our understanding of prey detection in
odontocete cetaceans suggests that biosonar (‘‘echolo-
cation’’) employing high frequency and ultrasonic
sounds is a primary mechanism (e.g., Ketten 2004;
Filter feeding in mysticete cetaceans
Nachtigall et al. 2007). However, mysticetes are likely
sensitive to low and perhaps infrasonic frequencies
(Houser et al. 2001; Erbe 2002; Parks et al. 2007) and
lack echolocation capabilities. Likewise, the eyes of
extant cetaceans are not particularly adapted for en-
hanced visual acuity (Mass and Supin 1997; Buono et
al. 2012; Rodrigues et al. 2014, 2015); however, en-
hanced visual acuity may have been characteristic of
some early diverging extinct mysticetes as hypothesized
by Fitzgerald (2006) and quantified by Marx (2011). By
contrast with extinct mysticetes, molecular evidence
suggests that the cone-specific phototransduction cas-
cade was inactivated in the Oligocene in the ancestry of
balaenopteroids (Springer et al. 2016a), which suggests
that acuity was sacrificed for sensitivity in this rod
monochromatic lineage. Although vibrissae have been
examined in detail for gray and bowhead whales (Berta
et al. 2015a; Drake et al. 2015), the extent to which the
rostral vibrissae of baleen whales serve as mechanore-
ceptors during feeding (e.g., detection of water move-
ment or prey movement) is unclear.
Cetaceans in general have experienced a reduction of
olfactory receptor genes through pseudogenization, but
mysticetes have retained some functionality of olfactory
ability (Kishida et al. 2007; Thewissen et al. 2011; Berta
et al. 2015b). Anatomical evidence indicates that fossil
and modern mysticetes retain distinct olfactory bulbs
and a cribriform plate (Cave 1988; Pihlström 2008),
and bowhead whales in particular have a well-
developed sense of smell relative to other cetaceans
(Thewissen et al. 2011; Kishida and Thewissen 2012).
Baleen whales have been observed to orient themselves
downwind of odor plumes produced by plankton, per-
haps also using vibrissae around the blowhole to deter-
mine the direction of the wind (Drake et al. 2015). In
addition, structures typically associated with the vom-
eronasal organ, namely a fleshy incisive papilla and
paired nasopalatine ducts or pits, have been observed
in several mysticete species (Lillie 1910; Schulte 1916;
Quay and Mitchell 1971; Berta et al. 2015a). The vom-
eronasal organ is usually associated with detection of
pheromones in terrestrial mammals (Keverne 1999),
although it may also possess other chemoreception
functions that overlap with the primary olfactory
system (Trinh and Strom 2003). Further detailed stud-
ies using histology of the nasal and palatal tissues of
mysticetes, as well as behavioral studies, are needed to
fully assess and test hypotheses of olfactory and vom-
eronasal chemosensory functions in baleen whales.
Ontogeny and genes
The ontogenetic development of structures related to
feeding in mysticetes has been revealed through
1273
comparative anatomical studies of fetal specimens
(e.g., Ridewood 1923; Dissel-Scherft and Vervoort
1954; Karlsen 1962; Tomilin 1967; Slijper 1976;
Fudge et al. 2009). Although neonate, juvenile, and
adult mysticetes are edentulous, tooth buds develop
in both the upper and lower jaws in utero. However,
the teeth are resorbed completely and the baleen ap-
paratus begins to develop before birth. In the minke
whale (Balaenoptera acutorostrata), the developing
teeth pass through three of the typical mammalian
stages (bud, cap, bell), but they never erupt and
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eventually are reabsorbed (Ishikawa and Amasaki
1995; Ishikawa et al. 1999; Davit-Beal et al. 2009).
Ongoing research by the present authors aims to
analyze a large sample of prenatal specimens of mul-
tiple mysticete species to image the developing tooth
buds, as well as determine the timing of the tooth to
baleen transition during ontogeny. Preliminary re-
sults from our research indicate that a 63.5 cm long
humpback fetus (Megaptera novaeangliae – SDNHM
25552) has tooth buds within alveolar grooves in
each jaw (20–23 per maxilla, 17–19 per dentary,
74–84 total; Supplementary Fig. S2). By comparing
total length of this fetus with published growth data
(Tomilin 1967; Hampe et al. 2015), we estimate that
the teeth are retained in the humpback to near the
mid-point of gestation (Fig. 2). However, there is no
evidence that baleen development had begun in this
individual, and so the relative timing of the two
events cannot be determined. In a comparative
study of minke whale fetuses, Ishikawa and
Amasaki (1995) concluded that tooth resorption
was in progress as initial baleen proteins were pre-
sent in the gums, suggesting at least some overlap in
the occurrence of tooth buds and developing baleen.
Degrading teeth and developing baleen were never
observed in the same specimen by those authors,
but the duration between total tooth reabsorption
and presence of baleen, if presence of both organs
is separated in time during mysticete ontogeny, is
likely very short. A preliminary growth curve for
minke whales that we construct here using published
data (Tomilin 1967; Ivashin and Mikhalev 1978;
Ishikawa and Amasaki 1995) suggests that tooth
reabsorption and baleen development occur close
to the last third of the gestation period, when the
fetus is about 1 m in total length (half the birth size,
2.1–2.7 m, Tomilin 1967). Because gestation times
and body lengths differ among mysticete species
(Tomilin 1967), more developmental data are
needed to determine the relative timing of tooth re-
sorption and baleen development for most mysticete
species.
1274 A. Berta et al.

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Fig. 2 Growth curves of humpback (M. novaeangliae) and minke (B. acutorostrata) whale species, with annotations on the presence of
teeth and baleen. Total length of fetuses of M. novaeangliae (diamonds) derived from Hampe et al. (2015), Tomilin (1967) and direct
collection of AL. Age of fetuses at different lengths, total gestation time and length at birth from Tomilin (1967). Total length of fetuses
of B. acutorostrata (circles) derived from Ishikawa and Amasaki (1995). Total length at birth and total gestation time from Tomilin (1967)
and Ivashin and Mikhalev (1978). Since these authors did not report a table correlating total length and age of the fetuses, the gestation
time was approximated using the growth curve formula proposed for this species by Ivashin and Mikhalev (1978). Length at birth is an
average (*).

Given that mysticetes possess tooth buds at some
ontogenetic stages, it is no surprise that they retain
functional tooth-related genes from their toothed an-
cestors. Several molecular studies investigated puta-
tive enamel and tooth-related genes in mysticetes
(Deméré et al. 2008; McKnight and Fisher 2009;
Meredith et al. 2009, 2011, 2013, Springer et al.
2016b), thereby providing a better understanding of
the functions and importance of these gene regions
(Fig. 3). A review of those data reveals that loss of
enamel specifically and teeth in general was a step-
wise process during mysticete evolution that was
accomplished via different pathways in different mys-
ticete lineages.
Certain genes associated with teeth/tooth formation
in mammals (WDR72, SLC24A4, FAM83H) have been
found to be mostly conserved in at least three mysticete
species, implying that they might serve other important
functions in development (Springer et al. 2016b).
Similarly, the DPP region of the dentin-related DSPP
(dentin sialophosphoprotein) gene has been found to
be conserved at least in the bowhead whale, while it has
accumulated mutations in toothless xenarthrans
(McKnight and Fisher 2009). Genes in the enamel
matrix proteins domain (AMBN, AMEL) acquired
inactivating mutations in different exons in all lineages
of toothless amniotes, including baleen whales
(Meredith et al. 2013), but the mutations accumulated
in different exons among different mysticete species.
Another gene of the same domain, ENAM, was found
to have become a pseudogene in crown mysticetes, even
if the inactivating mutations are not shared among the
genera that were analyzed. Another putative enamel-
specific gene (C4orf26; Meredith et al. 2011) was
also found to have a complex evolutionary history—
balaenids retain most of the sequence with inactivating
mutations, while most but not all balaenopteroid spe-
cies lack the gene completely (Springer et al. 2016b).
The blue whale (Balaenoptera musculus) possesses the
gene, but it is inactivated by mutations different from
those of Balaenidae. The most parsimonious hypothesis
to explain the various genetic patterns suggests that the
different mutations are a result of ancestral polymor-
phisms and that some of them have been lost indepen-
dently in the extant species (Meredith et al. 2009). In
contrast, MMP20 (matrix metalloproteinase) that is
Filter feeding in mysticete cetaceans 1275

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Fig. 3 Phylogeny of extant mysticete species, with tooth and enamel related gene inactivation mapped onto tree. The symbols
correspond to the first shared inactivation of the gene among the species for which sequences are available. Gene C4orf26 presents
three independent inactivations: white stars indicate a shared gene deletion, light gray and dark gray stars signal two different
inactivating mutations. The retention of the inactivated gene in B. musculus possibly indicates retention of ancestral polymorphism
among rorquals for C4orf26 (Springer et al. 2016b). Tree topology after Gatesy et al. (2013) and McGowen et al. (2009). Data for
AMEL, AMBN, and ENAM from Deméré et al. (2008), Meredith et al. (2010, 2013), MMP20 from Meredith et al. (2010), C4orf26 from
Springer et al. (2016b).

involved in tooth mineralization and also has pleiotro-
pic effects on other organs, has the same inactivating
mutation in all mysticetes, suggesting that the gene lost
functionality only once in the common ancestor of
Mysticeti. It should also be noted that the occurrence
of this shared mutation implies that enamel was lost
once in the common ancestor of crown Mysticeti
rather than independently in different lineages.
Most of the current genetic research into the loss
of teeth in mysticetes has focused on genes related to
tooth development, but the genetic basis for devel-
opment of the baleen apparatus itself is unclear.
Given the tissue’s keratinous composition, baleen
genes are likely to have originated from hair genes
that are expressed in the mouth of these mammals
that have lost the body hair cover (Pivorunas 1979).
It has been hypothesized that an acceleration in ex-
pression of genes of the WNT family during devel-
opment can explain both the hair loss and the
growth of baleen in mysticetes (Park et al. 2015).
Future investigations into the genetic basis of
baleen development will be necessary to more fully
understand the tooth to baleen transition in
mysticetes.
Integrating neontological and paleonto-
logical data
The fossil record of mysticetes provides direct ana-
tomical evidence for the tooth to baleen transition
suggested by developmental patterns in extant fetal
specimens. This record spans approximately 35 mil-
lion years of Earth history from near the Eocene–
Oligocene boundary to the Recent (Fig. 4), and
mysticete fossils are well documented across a
nearly worldwide distribution. The Oligocene por-
tion of this record includes specimens of toothed
mysticetes from the North and South Pacific
(Fitzgerald 2006, 2010; Deméré and Berta 2008;
Marx et al. 2015; Fordyce and Marx 2016) and
stem edentulous mysticetes from the Southeastern
United States, Japan, and New Zealand (Sanders
and Barnes 2002; Okazaki 2012; Boessenecker and
Fordyce 2015a, 2015b, 2015c; Tsai and Fordyce,
1276 A. Berta et al.

2 Odontoceti

1 4 Mammalodontidae†

3 6 Aetiocetidae†

5 8 Eomysticetidae†

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Neobalaenidae
7

10

11 Balaenidae
9

stem Thalassotherii†

13 Cetotheriidae†
12

15 Eschrichtiidae

14

16 Balaenopteridae
Eocene Oligocene Miocene Plio.
40 30 20 10 0
(Millions of Years) Pleistocene Holocene

Feeding Regimes
suction-aided raptorial feeding baleen-aided raptorial feeding bulk lter feeding
skim lter feeding lateral suction lter feeding engulfment/ lunge lter feeding

Fig. 4 Cladogram of Cetacea with associated feeding strategies in extinct and extant mysticetes. Relationships based on a strict consensus of
cladograms presented by Boessenecker and Fordyce (2015b). Stratigraphic ranges were downloaded from the Paleobiology Database (paleo-
biodb.org) on June 9, 2016 by searching for geologic strata through the taxonomic name search form for members of each terminal taxon named
on the cladogram. Illustrations of whales by C. Buell. (1) Cetacea: 28–59% olfactory genes non-functional. (2) Odontoceti: 74–100% olfactory
receptor genes non-functional; biosonar (‘‘echolocation’’). (3) Mysticeti: broad rostrum; thin lateral margins of maxilla; small, wide teeth with
denticles; diastemata in upper jaw. (4) Mammalodontidae: enlarged forward facing eyes (enhanced visual acuity?). (5)
Aetiocetidae þ Chaeomysticeti: small lateral nutrient foramina (presence of baleen-like structure); mandibular symphysis unfused. (6)
Aetiocetidae: enlarged forward facing eyes (enhanced visual acuity?). (7) Chaeomysticeti: low 13C in bones (feeding at low trophic level); reduction
of postnatal dentition; long, flattened rostrum; premaxilla/maxilla kinesis; elaborate lateral nutrient foramina; reduced function of tooth and
enamel genes. (8) Eomysticetidae: vestigial anterior dentition. (9) Crown Mysticeti: definitive presence of baleen/postnatal teeth absent; anterior
extension of occipital shield; lateral bowing of dentaries; reduced function of tooth and enamel genes. (10) Balaenoidea: arching of rostrum; long
baleen; subrostral gap. (11) Balaenidae: extreme arching of rostrum. (12) Thalassotherii: anteriorly convergent baleen racks; indistinct/concave
glenoid fossa; loss of C4orf tooth genes (?) (13) Cetotheriidae: reduced gaping of mouth; semi-synovial jaw joint. (14) Balenopteroidea: loss of C4orf tooth
genes. (15) Eschrichtiidae: slight arching of rostrum; short, coarse baleen; semi-synovial jaw joint; few, short throat grooves. (16) Balaenopteridae:
synovial jaw joint lost; tongue reduced and flaccid; ventral throat pouch; mandibular sense organ; elongation and multiplication of throat grooves.

2015). Given the presence of functional adult teeth The earliest known stem toothed mysticete is
in toothed mysticetes, the genomes of these early Llanocetus denticrenatus from the latest Eocene
mysticetes certainly retained functional tooth and (34 Ma) of Antarctica. However, description of
enamel genes. only a partial dentary and dentition of this
Filter feeding in mysticete cetaceans
important fossil are available, while the skull remains
undescribed. A similar problem involves a series of
undescribed archaeocete-like toothed mysticetes from
the Oligocene (30–26 Ma) of South Carolina, United
States that are based on well-preserved skulls, mandi-
bles, and postcrania. As a consequence, the earliest
well-described stem toothed mysticetes are represented
by fossils from the Oligocene (28–24 Ma) of
Australia and New Zealand—Janjucetus hunderi,
Mammalodon colliveri, and Mammalodon hakataramea
(Fitzgerald 2006, 2010, 2011; Fordyce and Marx 2016).
Collectively, these taxa form a monophyletic group,
the Mammalodontidae (node 4, Fig. 4). Janjucetus,
like its basilosaurid archaeocete ancestors, possessed
firmly closed/fused rostral sutures and a rugose bony
mandibular symphysis indicating that the rostrum and
lower jaw were each internally immobile (akinetic).
The upper and lower dentitions of both Janjucetus
and Mammalodon are characterized by heavily
ridged enamel on both labial and lingual surfaces,
double rooted postcanine teeth, and for Janjucetus
multiple accessory denticles on P2–M2 and p2–m3
(Fitzgerald 2006, 2010). Diastemata occur between
the upper teeth whereas the lower teeth are more
closely appressed. Notably, the upper and lower
teeth have strongly emergent crowns, with the roots
well exposed above the alveolar margin of the rostrum
and mandible, and suggesting well-developed gingival
tissue. Dental wear among mammalodontids is vari-
able, with Janjucetus displaying evidence of cheek
tooth vertical shearing during occlusion (Fitzgerald
2006) and Mammalodon displaying crown-to-crown
apical occlusion (Fitzgerald 2010). In the latter case,
apical dental wear (at least in the holotype specimen)
is so extreme that the cheek tooth crowns are nearly
completed abraded off, suggesting advanced ontoge-
netic age or perhaps pathology.
The palates of mammalodontids lack lateral fo-
ramina and sulci, which in later diverging mysticetes
serve as osteological correlates of baleen, but the in-
creased rostral width in mammalodontids has been
hypothesized to represent an initial step in enlarge-
ment of the oral cavity (Fitzgerald 2011), which in
turn was carried to a further stage in later diverging
mysticetes. Overall, morphological features of the
skull, rostrum, dentition, mandible, and sternum
suggest that mammalodontids likely were specialized
for raptorial feeding (Janjucetus) or suction feeding
(Mammalodon) on primarily single prey items such
as fish and perhaps squid (Fitzgerald 2010), as op-
posed to the bulk filter-feeding mysticetes of today’s
oceans.
Contemporaneous with mammalodontids of the
Southern Hemisphere were aetiocetids from the
1277
Northern Hemisphere, which represent a monophy-
letic lineage of toothed mysticetes known from
Oligocene rocks (31–24 Ma) on both sides of the
North Pacific (node 6, Fig. 4) and often described as
bridging the morphological gap between stem
toothed and stem baleen-bearing mysticetes (e.g.,
Deméré and Berta 2008). Aetiocetids include five
genera and numerous species: Aetiocetus,
Chonecetus, Ashorocetus, Fucaia, and Morawanocetus,
all of which have skulls with closed rostral sutures
between maxilla and premaxilla, maxilla and vomer,
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maxilla and frontal, and premaxilla and frontal as
seen in archaeocetes and mammalodontids.
Importantly, however, aetiocetids possess an unfused
mandibular symphysis as seen in edentulous, baleen-
bearing mysticetes. This anatomical pattern indicates
that aetiocetids had a kinetic lower jaw, but a rigid,
akinetic rostrum. In addition, tiny foramina and as-
sociated sulci on the palate just medial to the teeth
in Aetiocetus, Fucaia, and Morawanocetus and lateral
to a pair of well-defined major palatine foramina and
sulci, are hypothesized to be homologous with the
lateral palatal foramina and sulci in extant mysticetes
that transmit blood vessels that nourish baleen
(Supplementary Fig. S3; see also Deméré and Berta
2008). Confirmation that baleen receives the majority
of blood from the superior alveolar artery and its
associated branches that pass through lateral nutrient
foramina in an extant gray whale was recently re-
ported (Ekdale et al. 2015), and the foramina have
been used to infer the presence of baleen in aetioce-
tids and other extinct mysticete taxa. If aetiocetids
possessed baleen or a baleen-like organ, the structure
of that organ is unknown. The proto-baleen may
have merely consisted of short keratin papillae or
bristles arranged along the lateral portion of the
palate just medial to the teeth and not fully formed
baleen plates.
The homology of the lateral palatal foramina in
aetiocetids and extant mysticetes, however, has yet
to be determined conclusively. Some researchers
have suggested that aetiocetids likely did not possess
proto-baleen (e.g., Marx et al. 2015), but rather these
workers interpret the palate vascularization, emergent
teeth, and unfused mandibular symphysis of aetioce-
tids as being related to a specialized raptorial suction
feeding strategy that utilized enlarged gum tissues to
overcome the lateral positive pressure effects of suc-
tion feeding. These workers also propose a monophy-
letic toothed mysticete grouping of mammalodontids
and aetiocetids—a relationship suggesting that an
elastic mandibular symphysis evolved twice (or was
lost in mammalodontids), and that baleen (if present
in aetiocetids) also evolved twice (or was lost in
1278
mammalodontids). These contrasting interpretations
of aetiocetid phylogeny and function underscore the
important role that this transitional group plays in
reconstructing early mysticete evolution and how the
anatomical features of purely suction-aided raptorial
feeders could be co-opted in a step-wise fashion for
bulk filter feeding in later diverging edentulous
mysticetes.
Whether or not baleen was present, aetiocetid teeth
display a clear and interesting dichotomy between
species of Morowanocetus and Fucaia with distinctly
heterodont dentitions with caniniform, single-rooted
anterior teeth (I1–3, C), and closely-spaced, strongly
denticulate, single- and/or double-rooted postcanine
teeth (Barnes et al. 1995; Marx et al. 2016) and species
of Aetiocetus with weakly heterodont dentitions with
caniniform, single-rooted anterior teeth (I1–3, C), and
widely-spaced, very weakly denticulate, single-rooted
postcanine teeth (Deméré and Berta 2008). The post-
canine dentitions of Morowanocetus and Fucaia lack
diastemata and consist of relatively large, laterally
compressed crowns with strong lingual and labial
enamel ridges in Morowanocetus and only lingual
enamel ridges in Fucaia. In contrast, species of
Aetiocetus have distinct diastemata in both the upper
and lower jaws and only the lingual surfaces of the
relatively small and laterally compressed postcanine
teeth possess fine enamel ridges. In addition, all post-
canine teeth have emergent crowns and surprisingly
shallow alveoli. This unique combination of cranial,
rostral, mandibular, and dental features suggests that
aetiocetids were the first mysticetes to possess man-
dibular kinesis and specialized palate vascularization
and that some form of proto-baleen was present as
a rudimentary oral filter to complement the more
traditional raptorial suction feeding strategy of earlier
diverging toothed mysticetes (Deméré and Berta
2008).
The earliest functionally edentulous mysticetes
(stem Chaeomysticeti; node 7, Fig. 4) are represented
by several extinct lineages. Most are members of
Eomysticetidae (node 8, Fig. 4) known from the
Oligocene (29–27 Ma) of Japan and North
America, as well as a Southern Hemisphere clade
that includes Matapanui, Tohoraata, Tokarahia, and
Waharoa reported from the Oligocene (27–25 Ma)
of New Zealand (Boessenecker and Fordyce 2015a,
2015b, 2015c, 2016a,b). Rostral kinesis in Waharoa
was intermediate between akinetic stem toothed mys-
ticetes (and archaeocetes) and fully kinetic crown
chaeomysticetes. In particular, the premaxilla–maxilla
suture is unfused suggesting a largely open suture,
while the elongate and corrugated nasofrontal and
premaxilla-nasofrontal sutures indicate a somewhat
A. Berta et al.
more rigid rostrum in Waharoa ruwhenua than in
crown mysticetes. The palatal morphology of
Waharoa is also intermediate between toothed and
crown mysticetes. Unlike basal toothed mysticetes
(e.g., Janjucetus and Mammalodon) but similar to
aetiocetids (e.g., species of Aetiocetus), the palate of
Waharoa has lateral palatal vascular features; how-
ever, the palatal foramina and sulci are larger and
more numerous than in aetiocetids. Waharoa differs
from extant mysticetes in having lateral nutrient fo-
ramina and sulci confined to the posterior two-thirds
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of the palate. Some eomysticetids (e.g., Yamatocetus
and Waharoa) also possess an alveolar groove on the
elongated maxilla and more distinct individual alve-
oli on the premaxilla and anterior tip of the mandi-
ble. Putative adult teeth have been reported in at
least one eomysticetid (i.e., Tokarahia), but their
size and shallow alveoli suggest that they may have
not been functional. Nonetheless, the reduction of
postnatal teeth in these mysticetes indicates reduced
function of tooth and enamel genes by the Oligocene
(Fig. 4).
The mandible of Waharoa and other eomysticetids
possessed a distinct symphyseal groove and smooth
symphyseal surface, indicating well-developed man-
dibular kinesis. There was also a large mandibular
foramen and correspondingly thin pan bone, features
used by some workers to indicate that these stem
chaeomysticetes were unable to lunge feed like
extant balaenopterids, but may have employed a ru-
dimentary type of skim feeding reminiscent of extant
right whales (Boessenecker and Fordyce 2015b). The
enlarged, elongate temporal fossa of Wahoroa and
other eomysticetids together with a large coronoid
process indicates the presence of large temporalis
muscles, which may have acted to stabilize the man-
dible during skim feeding so that a unidirectional
flow of water was directed through the oral cavity
(Boessenecker and Fordyce 2015b). Although the
exact form of filter feeding employed by eomystice-
tids is unknown, the absence of a functional adult
dentition and the presence of baleen (interpreted
from lateral nutrient foramina) and both rostral
and mandibular kinesis indicate that eomysticetids
were the earliest mysticetes capable of baleen-assisted
bulk filter feeding.
In concert with changes in morphology at this
stage of mysticete evolution, there is geochemical ev-
idence to suggest a major shift in diet and feeding
physiology between stem mysticetes and chaeomysti-
cetes. Results of a stable isotope study (Clementz
et al. 2014) revealed that the bones of toothed mam-
malodontids and odontocetes carry similar 13C
values, which indicates that the earliest mysticetes
Filter feeding in mysticete cetaceans
were feeding at the same trophic level as toothed
whales and likely were not filter feeding or feeding
low in the food chain as in extant mysticetes. In
contrast 13C values for eomysticetids and stem balae-
nopteroids are lower and significantly different from
those of toothed mammalodontids or odontocetes,
suggesting that the earliest edentulous mysticetes
may have specialized on a diet of zooplankton sim-
ilar to extant mysticetes (Supplementary Fig. S4).
Although aetiocetids were not included within the
isotopic analyses, the results of those analyses pro-
vide additional evidence that the transition from
teeth to baleen is coincident with a shift from rap-
torial to bulk filter feeding. It is no coincidence that
an isotopic signature suggesting feeding at a low tro-
phic level coincides with major anatomical adapta-
tions for bulk filter feeding, such as baleen, flattening
of the rostrum, and rostral kinesis to allow for ex-
pansion of the oral cavity that are observed in the
earliest chaeomysticetes.
The evolution of bulk feeding would have allowed
large consumers to take advantage of short but reg-
ular bursts of an abundant food supply and appears
to have been largely driven by tectonic and oceano-
graphic changes in continental and oceanic configu-
rations, changes in global and regional ocean
circulation patterns, and changes in the latitudinal
position of centers of oceanic primary productivity.
These global changes that began with the final
breakup of Gondwana during the late Eocene re-
sulted in creation of a circum-polar sea in the
Southern Hemisphere (the Southern Ocean) and iso-
lation of the Antarctic continent at the South Pole.
These new conditions, in turn, were responsible for
growth of the Antarctic ice sheet and initiation of
Southern Hemisphere glaciation and a global drop
in sea level at the Eocene–Oligocene boundary ap-
proximately 34 million years ago (Prothero and
Ivany 2003). Establishment of the Southern Ocean
and growth of the Antarctic ice sheet together with
other factors combined to alter the fundamental
structure of the world’s oceans, which became
more thermally stratified and marked by increased
tropics-to-polar thermal gradients. Cold surface
waters flowing north from Antarctica encountered
warmer subantarctic waters to create a major zone
of mixing, downwelling, and upwelling—the
Antarctic Convergence—with very high primary pro-
ductivity. It is in this setting that the earliest eden-
tulous mysticetes are thought to have begun the
impressive adaptive radiation to exploit this rich bio-
mass as bulk filter-feeding mesopredators.
Some recent research has suggested that modern
rorqual-like bulk filter feeding evolved near the
1279
divergence of chaeomysticetes. That hypothesis is
based on fossils of Horopeta umarere from the late
Oligocene (27–25 Ma) of New Zealand (Tsai and
Fordyce 2015). Horopeta is known from a partial skull
that is missing anatomically important parts of the basi-
cranium, squamosal, and rostrum. The mandibles are
fragmentary and bioeroded, but preserve just enough of
the horizontal rami and coronoid processes to distin-
guish them from eomysticetids. Tsai and Fordyce
(2015) used only equivocal mandibular features (a
slightly laterally bowed horizontal ramus and a poster-
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olaterally deflected and broken coronoid process) to
propose that H. umarere was an engulfment feeder
such as extant balaenopterids, but the hypothesis does
not consider all of the other anatomical features that are
critical to successful engulfment feeding, such as a non-
synovial, fibrocartilaginous temporomandibular joint,
a medially buttressed mandibular neck, and a robust
and posteriorly-directed mandibular condyle.
Within crown Mysticeti (defined as the least inclusive
crown clade containing Balaenidae, Neobalaenidae,
Eschrichtiidae, and Balaenopteridae; node 9, Fig. 4) are
several extinct lineages whose membership varies de-
pending upon which phylogenetic study is examined
(e.g., Boessenecker and Fordyce 2015a, 2015b, 2015c;
Gol’din and Steeman 2015; Marx and Fordyce 2015;
Bisconti and Bosselaers 2016; Marx et al. 2016).
Postnatal teeth that have erupted are not described for
any member of crown Mysticeti, and the most recent
common ancestor of the clade may have experienced
further reduction of tooth and enamel genes. Most
recent phylogenies based on morphology recognize a
fundamental dichotomy between a balaenoid clade
(balaenids þ neobalaenids; node 10, Fig. 4) and a thalas-
sotherian clade (Boessenecker and Fordyce 2016) (node
12, Fig. 4). Genetic and total evidence phylogenies re-
cover a closer relationship between neobalaenids and
balaenopteroids (e.g., McGowen et al. 2009; Fordyce
and Marx 2012). The taxonomic dichotomy of crown
mysticetes reflects an early divergence event that was
completed by at least the early Miocene (20–18 Ma)
and established the morphological division between ob-
ligate skim feeders with narrow, arched rostra (balae-
noids) and a more diverse array of generalized and
specialized filter feeders with relatively flat and broad
rostra (thalassotherians). This later group, the
Thalassotherii (Bisconti et al. 2013), underwent dramatic
taxonomic and functional diversification throughout
the Neogene (23–2.6 Ma) and Quaternary (2.6 Ma
to present), possibly beginning as early as the latest
Paleogene (25 Ma). Two discrete thalassotherian line-
ages, however, are consistently recognized in most recent
studies and include Cetotheriidae (node 13, Fig. 4) and
Balaenopteroidea (node 14, Fig. 4) consisting of
1280
eschrichtiids (node 15, Fig. 4) and balaenopterids (node
16, Fig. 4). A third group is more problematic, but in
general consists of a group of stem thalassotherians that,
depending on the study examined, represents either an
unnamed monophyletic group (Boessenecker and
Fordyce 2015a, 2015b, 2015c) or a paraphyletic group
(Marx and Fordyce 2015; Marx et al. 2016). In either
case, this problematic assemblage referred to here as
stem thalassotherians lack the synapomorphies of
cetotheriids and balaenopteroids.
As expected in such a taxonomically diverse clade,
crown mysticetes display a considerable degree of
morphological diversity (disparity) that has been in-
terpreted to represent several functional modes and
feeding strategies for extinct taxa. Fossil balaenids
pose a special challenge because of the significant
temporal gap that separates the earliest recognized
balaenid, Morenocetus parvus (early Miocene [20–
18 Ma] of Argentina) from the next youngest balae-
nid, Eubalaena shinshuensis (late Miocene [6 Ma] of
Japan). In spite of this gap, it appears that very early
in their evolutionary history, balaenids evolved fea-
tures associated with skim feeding (e.g., narrow and
dorsally arched rostra, narrow and laterally elongate
supraorbital processes, anteriorly placed supraoccipi-
tal that overlaps the parietals and frontals, and pos-
terior rostral elements that minimally contact
the frontals). In light of the early appearance of the
balaenid morphotype and in consideration of the
deep divergence of balaenids and thalassotherians
(Fig. 4) from their common ancestor, it may be jus-
tified to consider balaenids as living fossils. Until
only recently, the neobalaenid lineage was monotypic
with the only known member being the living pygmy
right whale Caperea marginata. However, the discov-
ery and description of Miocaperea pulchra, an extinct
neobalaenid from the late Miocene (7.5 Ma) of
Peru, reveals that this lineage is much older, al-
though with a 7 million year temporal gap.
Interestingly, Miocaperea is morphologically very
similar to living Caperea and possesses many of the
distinctive autapomorphies of the extant species.
Recently, one research group has proposed a novel
hypothesis suggesting that C. marginata is actually a
living member of the Cetotheriidae (Fordyce and
Marx 2012; Marx and Fordyce 2015). This hypothesis
is based on an unusual assessment of cranial, petro-
tympanic, and mandibular morphological characters
that questionably represent homologous character
states between cetotheriids and Caperea. However,
in this scenario the substantial balaenid features of
Caperea have to be viewed as resulting from conver-
gence including many features (e.g., dorsally arched
rostrum; long, slender, and numerous baleen
A. Berta et al.
laminae; extremely telescoped supraoccipital, and re-
duced coronoid process) related to the continuous
ram feeding behavior of Caperea. In addition, the
hypothesis suggests that continuous ram feeding
evolved independently within a single lineage of the
cetotheriid clade, a clade that only contains suction
feeding mysticetes. Clearly, neobalaenids are an ex-
tremely autapomorphic group, but few independent
research groups have been able to replicate this
unique phylogenetic placement of Caperea as a
cetotheriid. One exception is the study by Gol’din
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and Steeman (2015), although their phylogenetic
matrix was based in part on the matrix of Fordyce
and Marx (2012).
As mentioned, extinct thalassotherians were taxo-
nomically and morphologically diverse. As such, they
likely displayed a variety of filter-feeding strategies.
Some, such as the speciose cetotheriid lineage appear
to have employed a specialized type of suction feeding
(Gol’din and Startsev 2014; El Adli and Deméré 2015).
Probably the best studied cetotheriids are species of
Herpetocetus, known from the late Miocene and
Pliocene (6.4–2.5 Ma) of the North Pacific and
North Atlantic surviving into the Pleistocene in the
North Pacific, and species of Cetotherium, known
from the late Miocene (11–10 Ma) of Ukraine.
Herpetocetus morrowi described from the late Pliocene
of Southern California had a unique jaw joint that
would have restricted opening of the mouth to less
than 458 (El Adli et al. 2014). This feature, coupled
with the characteristic kinetic rostrum of Herpetocetus
(and closely related Piscobalaena) suggests that these
long-snouted cetotheriids were able to generate con-
centrated oral suction pressure to draw prey-laden
water into their mouths similar to the extant gray
whale Eschrichtius robustus. However, unlike E. robus-
tus, Herpetocetus had a relatively flat palate with a low
palatal keel and anteromedially-oriented glenoid fossa,
as well as a posteriorly elongated mandibular angular
process. These anatomical features and limited gape
suggest that Herpetocetus (and Piscobalaena) likely pos-
sessed numerous, but very short baleen laminae along
the lateral margins of its elongate palate. Cetotherium
riabinini described from the late Miocene of Southern
Ukraine is probably the most anatomically complete
species of Cetotherium. Like that of Herpetocetus, the
rostrum of Cetotherium is elongate; however, also de-
cidedly narrower and more triangular in dorsal view
(Gol’din and Startsev 2014). Intra-rostral sutures are
open and a high degree of rostral kinesis has been pro-
posed for this species. In addition, the mandible lacks
the uniquely elongated angular process and small and
posterolaterally directed mandibular condyle of
Herpetocetus. The postcranial skeleton also displays a
Filter feeding in mysticete cetaceans
high percentage of pachyosteosclerotic bone. A func-
tional analysis of C. riabinini suggests that this Eastern
Paratethyan cetotheriid was primarily a benthic suction
feeder intermediate between continuous suction fee-
ders such as Herpetocetus and intermittent suction fee-
ders such as Eschrichtus (Gol’din and Startsev 2014).
Extant thalassotherians form the clade
Balaenopteroidea (node 14, Fig. 4) that includes
living and fossil members of Eschrichtiidae (gray
whales; node 15, Fig. 4) and Balaenopteridae (rorquals;
node 16, Fig. 4). All extant balaenopteroids lack the
enamel-specific C4orf genes indicating that those
genes were absent in the most recent common ancestor
of eschrichtiids and balaenopterids near the Oligocene/
Miocene boundary. However, those genes may have
been lost in part or in total much earlier in the most
recent common ancestor of Thalassotherii (Fig. 4).
Although there is only one living eschrichtiid (E.
robustus), the two early Pliocene (5–3.5 Ma) taxa
have been described: Gricetoides aurorae from
Eastern North America (Whitmore and Kaltenbach
2008) and Eschrichtioides gastaldii from Italy
(Bisconti, 2008), as well as several Pleistocene fossils
that can be assigned to the genus Eschrichtius (Barnes
and McLeod 1984; Ishishima et al. 2006; Tsai and
Boessenecker 2015). The stem eschrichtiid, E. gastal-
dii, possesses several skull and mandibular features
that appear to be associated with the suction feeding
strategy of living gray whales. These include: a short
and steeply sloping occipital shield, low but distinct
occipital tuberosities, robust and posteriorly directed
paroccipital processes, short and robust zygomatic
process of the squamosal, posterodorsally oriented
mandibular condyle, enlarged angular process of
mandible, low coronoid process, and a post-coronoid
elevation. Together, these features suggest an in-
creased reliance on the masseter, digastricus, and
pterygoid muscles in providing greater precision
and control during lateral and medial rotation of
the mandible along its long axis (alpha rotation),
and a reduced reliance on the temporalis muscle
and a reduced degree of mandibular abduction
(delta rotation), functional adaptations noted in E.
robustus (El Adli and Deméré 2015). A partial
eschrichtiid skeleton from the early Pleistocene-late
Pliocene of Japan appears to represent the earliest
record of the genus Eschrichtius. Although there is
no mandible and the skull is incomplete and lacks
the frontals and rostrum, the cranium preserves fea-
tures commonly associated with E. robustus (e.g.,
short and steeply sloping occipital shield with dis-
tinct occipital tuberosities and robust and posteriorly
directed paroccipital processes) and possibly
1281
correlated with an increased reliance on the neck
musculature.
Balaenopteridae is the most specious group of crown
thalassotherians with 8 or 9 living members and at least
13 described extinct taxa. The balaenopterid fossil
record extends into the late Miocene (12–10 Ma)
and appears to contain several recognizable lineages.
A basal lineage consisting of Miocene and Pliocene
species from Italy and California (Plesiobalaenoptera
quarantellii, ‘‘Balaenoptera’’ ryani, Cetotheriophanes
capellinii) is characterized by skulls with elongate inter-
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orbital regions exposing the parietal and the frontal and
lacking any overlap between posterior rostral bones
and anterior cranial bones. The mandibles have a dis-
tinctly bowed horizontal ramus, a low but well-devel-
oped coronoid process, a small and dorsally placed
mandibular foramen, a large angular process, and a
weakly developed subcondylar furrow. Together these
features suggest an intermediate condition between
stem thalassotherians and crown balaenopterids in
which the lower jaw was able to undergo some degree
of alpha rotation during which the laterally bowed
ramus produced limited lateral expansion of the
mouth but not to the degree seen in modern rorquals.
A more advanced stage of cranial telescoping is seen in
a group of balaenopterids consisting of
Parabalaenoptera baulinensis, Archaebalaenoptera cas-
triarquati, Fragilicetus velponi, Protororqualus cuvieri,
‘‘Megaptera’’ miocaena, ‘‘Megaptera’’ hubachi, and
‘‘Balaenoptera’’ siberi. Although several of these
Miocene and Pliocene taxa were originally assigned
to living genera (Balaenoptera and Megaptera), the
short exposure of the parietal and frontal on the
vertex, the short overlap of anterior cranial and poste-
rior rostral bones, and the retention of a large squamo-
sal fossa indicate otherwise. Features of the mandible,
however, appear to closely approach those in derived
balaenopterids, especially enlargement of the coronoid
process, greater lateral bowing of the ramus, a reduced
angular process, and a deep subcondylar furrow. These
features suggest a greater degree of mandibular alpha
rotation and lateral expansion of the mouth during
initial delta rotation; actions that are fundamental to
the advanced lunge feeding behavior seen in living ror-
quals. A third balaenopterid lineage is represented by a
late Pliocene (3.5–2.5 Ma) species from California,
Balaenoptera bertae (Boessenecker 2013). Unlike
other extinct rorquals, this species can be assigned to
Balaenoptera, as it possesses a modern stage of cranial
telescoping and configuration of the squamosal (e.g.,
possession of a squamosal crease and very reduced
squamosal fossa). Although there is no mandible
known for B. bertae, it likely possessed features charac-
teristic of the living lunge feeding fin whales.
1282
Conclusions
The evolution of baleen assisted bulk filter feeding
from tooth assisted raptorial feeding is one of the
greatest and best documented macroevolutionary
transitions in vertebrate history. All extant mysticetes
are edentulous in adulthood, but ontogenetic evi-
dence of tooth buds in fetuses and genetic evidence
of both functional and non-functional tooth and
enamel related genes in the mysticete genome indi-
cate that all toothless baleen whales are descended
from toothed ancestors. Observations from the
fossil record confirm the toothed ancestry of mysti-
cetes, and the fossil record showcases the step-wise
transition from raptorial to bulk filter feeding. The
rostrum is broadened in the earliest toothed mysti-
cetes (mammalodontids), followed by a loss of fusion
at the mandibular symphysis and presence of a
baleen-like structure in the toothed aetiocetids. A
complete loss of functional teeth in adulthood in
eomysticetids coincides with a flattened and kinetic
rostrum, both of which increase the size of the oral
cavity to allow large volumes of prey-laden water
into the mouth. In addition, geochemical evidence
of a diet rich in zooplankton coincides with morpho-
logical changes that are hypothesized to signify the
transition from raptorial single prey feeding to bulk
filter feeding near the Eocene–Oligocene boundary.
The evolution of bulk filter feeding led the way for a
rapid radiation of the diverse feeding strategies that
are observed in extant mysticetes, as well as potential
unique behaviors that have been hypothesized for
cetotheriids. Through continued discoveries and de-
scriptions of important fossils, detailed anatomical
studies of mysticete fetuses, and further investiga-
tions of the genetic bases of tooth and baleen devel-
opment, the grand narrative of baleen evolution will
continue to unfold.
Supplementary Data
Supplementary Data available at ICB online.
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