THE ANATOMICAL RECORD 295:615–631 (2012)
Inner Ear Evolution in Primates
Through the Cenozoic: Implications for
the Evolution of Hearing
MARK N. COLEMAN1* AND DOUG M. BOYER2
Department of Anatomy, Midwestern University, Glendale, Arizona 85308
Department of Anthropology and Archaeology, Brooklyn College, Brooklyn,
New York 11210
Mammals are unique in being the only group of amniotes that can
hear sounds in the upper frequency range (>12 kHz), yet details about
the evolutionary development of hearing patterns remain poorly understood. In this study, we used high resolution X-ray computed tomography
to investigate several functionally relevant auditory structures of the
inner ear in a sample of 21 fossil primate species (60 Ma to recent times)
and 25 species of living euarchontans (primates, tree shrews, and flying
lemurs). The structures examined include the length of the cochlea, development of bony spiral lamina and area of the oval window (or stapedial
footplate when present). Using these measurements we predicted aspects
of low-frequency and high-frequency sensitivity and show that hearing
patterns in primates likely evolved in several stages through the first
half of the Cenozoic. These results provide temporal boundaries for the
development of hearing patterns in extant lineages and strongly suggest
that the ancestral euarchontan hearing pattern was characterized by
good high-frequency hearing but relatively poor low-frequency sensitivity.
They also show that haplorhines are unique among primates (extant or
extinct) in having relatively longer cochleae and increased low-frequency
sensitivity. We combined these results with additional, older paleontological evidence to put these findings in a broader evolutionary context. Anat
C 2012 Wiley Periodicals, Inc.
Rec, 295:615–631, 2012. V
Key words: primate hearing; hearing evolution; low-frequency
hearing; high-frequency hearing; cochlea; oval
window; stapedial footplate; secondary bony
One of the most unique features of auditory perception in mammals is the ability to hear sounds above 12
kHz (Fay, 1988). Snakes and turtles are relatively insensitive to airborne sounds and can rarely hear sounds
above 2 kHz (Fig. 1). Lizards and crocodilians show
slightly better sensitivity but are still limited to frequencies below 4–8 kHz. Most birds can hear sounds up to
around 10 kHz although some predatory birds such as
barn owls can hear sounds as high as 12 kHz (Konishi,
1973). In contrast, most mammals have an upper frequency limit of hearing that ranges from 30 to 60 kHz
and some bats and aquatic mammals are able to detect
acoustic signals above 100 kHz (Fig. 1). Humans (upper
C 2012 WILEY PERIODICALS, INC.
limit 18 kHz), elephants (Elephas maximus—upper
limit 11 kHz), and naked mole rats (Hetercephalus
glaber—upper limit 12 kHz) present a few exceptions
Grant sponsor: National Science Foundation, Evolving Earth
Foundation, American Society of Mammalogists, Midwestern
University, Stony Brook University; Grant numbers: NSF BCS0408035, NSF BCS-0622544, NSF BCS-0100825.
*Correspondence to: Mark N. Coleman, Department of
Anatomy, Midwestern University, 19555 N. 59th Ave., Glendale,
AZ 85308, USA. E-mail: [email protected]
Received 20 September 2011; Accepted 2 December 2011.
Published online 27 January 2012 in Wiley Online Library
COLEMAN AND BOYER
Fig. 1. Hearing sensitivity for various groups of terrestrial vertebrates. Nonmammalian vertebrates show reduced hearing sensitivity,
particularly at frequencies above 10 kHz compared with most mammals that have heightened overall sensitivity and can hear sounds in
the high-frequency range (>12 kHz). Number in parentheses represents number of species used to derive group averages. Mean audiograms for snakes, turtles, lizards, crocodiles, and birds taken from
Dooling et al. (2000). Opossum audiogram based on average values
for Didelphis virginiana (Ravizza et al., 1969a; Ravizza and Masterton,
1972), Marmosa elegans, Monodelphis domestica (Frost and Masterton, 1994). Ungulate audiogram based on average values for Bos Taurus, Equus caballus (Heffner and Heffner, 1983), Capra hircus, Sus
scrofa (Heffner and Heffner, 1990a), Elephas maximus (Heffner and
Heffner, 1982), Rangifer tarandus (Flydal et al., 2001). Carnivore audiogram based on average values for Canis familiaris (Heffner, 1976), Felis
catus (Heffner and Heffner, 1985b), Mustela nivalis (Heffner and
Heffner, 1985c), Mustela putorius (Kelly et al., 1986), Procyon lotor
(Wollack, 1965). Bat audiogram based on average values for Artibeus
jamaicensis (Heffner et al., 2003), Carollia perspicillata (Koay et al.,
2003), Eptesicus fuscus (Koay et al., 1997), Megaderma lyra (Neuweiler, 1984), Myotis lucifugas (Dalland, 1965), Noctilio leporinus
(Wenstrup, 1984), Phyllostomus hastatus (Koay et al., 2002), Rhinolophus ferrumequinum (Long and Schnitzler, 1975), Rousettus aegyptiacus (Koay et al., 1998). Low-frequency rodent audiogram based on
species with a low-frequency cutoff below 500 Hz and a highfrequency cutoff below 64 kHz: Cavia porcellus (Heffner et al., 1971),
Chinchilla laniger (Heffner and Heffner, 1991), Cynomys leucurus,
Cynomys ludovicianus (Heffner et al., 1994b), Dipodomys merriami
(Webster and Webster, 1972; Heffner and Masterson, 1980), Geomys
bursarius (Heffner and Heffner, 1990b), Heterocephalus glaber (Heffner
and Heffner, 1993), Marmota monax, Mesocricetus auritus, Tamias
striatus (Heffner et al., 2001), Meriones unguiculatis (Ryan, 1976),
Sciurus niger (Jackson et al., 1997), Spalax ehrenbergi (Heffner and
Heffner, 1992). High-frequency rodent audiogram based on species
with a low-frequency cutoff above 500 Hz and a high-frequency cutoff
above 64 kHz: Acomys cahirinus, Phyllotis darwini (Heffner et al.,
2001), Mus musculus, Sigmodon hispidus (Heffner and Masterton,
1980), Neotoma floridana, Onychomys leucogaster (Heffner and
Heffner, 1985a), Rattus norvegicus (Heffner et al., 1994a). Primate
audiogram data and techniques used to extract and interpolate data
from the literature described in Coleman (2009).
to the general mammalian pattern of good highfrequency hearing (Heffner and Heffner, 1982, 1993;
Jackson et al., 1999).
Although it has been argued that the development of
a three-bone ossicular system and coiling (and elongation) of the cochlea were key adaptations that led to
good high-frequency sensitivity (Masterson et al., 1969;
Manley, 1972; Fleischer, 1978; Echteler et al., 1994;
Frost and Masterton, 1994; Fox and Meng, 1997), determining the timing of key events in the evolution of
hearing abilities of mammals has been a topic of debate.
One leading hypothesis on the subject proposes that
primitive mammals shifted to a primarily highfrequency condition soon after acquiring the three-bone
ossicular system (Jurassic) and then gradually (re)developed good low-frequency sensitivity starting in the
Cretaceous and extending through the early part of the
Cenozoic (Masterson et al., 1969; Jerison, 1973; Frost
and Masterton, 1994).
Comparative studies in living mammals have generally supported this hypothesis by showing that
‘‘primitive’’ mammals like opossums and hedgehogs are
characterized by good high-frequency hearing and rela-
tively poor low-frequency sensitivity (Ravizza et al.,
1969a, b; Frost and Masterton, 1994). These animals
also have what is generally considered to be ‘‘ancestral’’
characteristics in ear morphology such as the ‘‘microtype’’ middle ear bone configuration, which seems
particularly well adapted for transmitting highfrequency sounds (Fleischer, 1978; Rosowski, 1992). In
recent years, it has become increasingly possible to use
fossils to investigate evolutionary hearing patterns,
although there are still a few temporal gaps, which have
prevented a comprehensive evaluation of proposed evolutionary sequences.
The incipient development of the three-bone ossicular system during the Late Triassic (roughly 200 Ma),
such as witnessed in fossil mammaliaformes like
Morganucodon, may have resulted in a slight shift toward higher frequencies although these gains were
probably modest since these animals had relatively
large ossicles and short, uncoiled cochleae (Kermack
and Mussett, 1983; Rosowski and Graybeal, 1991;
Rosowski, 1992). Comparative studies have shown that
high-frequency limits are correlated with ossicular
a et al., 1995; Coleman and Colbert, 2010),
INNER EAR EVOLUTION IN PRIMATES
so the relatively large ossicles in Morganucodon likely
placed inertial limitations on how quickly the ear bones
could vibrate, limiting high-frequency transmission
through the middle ear.
The hearing range in early mammals such as multituberculates (late Jurassic – late Eocene) was probably not
that much different from that of living monotremes. Multituberculates such as Lambdopsalis share numerous
similarities to monotremes in middle ear structure such
as the orientation of the ectotympanic bone, the position
of the malleus relative to the incus and the simple morphology of the incus (Meng and Wyss, 1995). Mechanical
analyses of ear function in echidnas (Tachyglossus
aculeatus) suggest that their middle ear bones are
relatively inefficient at transmitting sounds, particular
at higher frequencies (Aitkin and Johnston, 1972). In
addition, multituberculates were similar to extant monotremes in having a relatively short cochlea that curves
laterally but does not complete one full turn (Fox and
Meng, 1997). Auditory brainstem response estimates of
hearing in echidnas (Tachyglossus aculeatus) suggest
that these prototherians, and possibly multituberulates
as well, had a relatively limited hearing range from 1.6
to 13.9 kHz (Mills and Shepherd, 2001).
During the middle to late Jurassic, the ancestors of
crown therians (marsupials and placentals) began developing inner ear structures that likely signal the onset of
heightened high-frequency hearing. The cladotherian
mammals Henkelotherium guimarotae and Dryolestes leiriensis from late Jurassic deposits in Portugal (156–150 Ma)
had relatively short cochleae (2.7–3.3 mm) that completed
about 3/4 of one full turn (270 ) (Ruf et al., 2009; Luo
et al., 2011), similar to multituberculates and monotremes.
However, unlike multituberculates and monotremes, Heneklotherium and Dryolestes demonstrate evidence for
development of primary and secondary bony laminae along
the basal end of the cochlear canal (Ruf et al., 2009; Luo
et al., 2011). Possessing both primary and secondary bony
laminae generally reduces the width of the basilar membrane and also allows this membrane to be more tense
(stiff) along the basal end, both of which help promote the
reception of high-frequencies (Fleischer, 1976). Although
some animals can hear relatively high frequencies without
the presence of a secondary lamina, it is considered a basic
anatomical requirement for the specialized high-frequency
hearing of bats and cetaceans (Bruns, 1980; Ketten, 1992;
Vater et al., 2004).
Although the bony laminae in Heneklotherium and Dryolestes suggest they may have had nascent adaptations for
relatively good high-frequency hearing, additional auditory
characteristics indicate that the overall range and sensitivity of hearing was probably limited in comparison with
extant therians. For one, the presence of a Meckelian
groove in Heneklotherium and Dryolestes suggest that
these taxa had a ‘‘transitional mammalian middle ear’’
that was not as efficient as the ‘‘definitive mammalian
middle ear’’ at transmitting airborne sounds (Meng et al.,
2011). In addition, their relatively short cochleae likely
placed limitations on the range of perceptible frequencies
because there may not have been adequate space on the
basilar membrane to have auditory sensory neurons (hair
cells) devoted to both high- and low-frequency sensitivity.
Complete coiling of the cochlear canal may have been
one strategy for increasing basilar membrane length in
a compact space. The hearing in the first mammals that
had short but coiled cochleae was presumably like marsupials such as opossums (Fig. 1), which have coiled but
relatively short basilar membranes [e.g., 6.4 mm, Monodelphis domestica—(Muller et al., 1993)]. The limited
low-frequency hearing in living opossums is not strictly
related to small body size since even the medium-sized
Didelphis virginiana (4 kg) can hear sounds only down
to about 1 kHz [overall range ¼ 1–68 kHz—(Ravizza
et al., 1969a)]. Furthermore, ‘‘primitive’’ extant placental
mammals such as hedgehogs (Hemiechinus auritus) also
have limited low-frequency sensitivity (500 Hz to
>60 kHz) and a presumably relatively short cochlea as
implied by the fact that their cochleae have only 1 1/2
spiral turns (Lewis et al., 1985).
The oldest known mammal that demonstrates at least
one full coil of the cochlea comes from early Cretaceous
deposits (125–100 Ma) in Mongolia and has been attributed to Prokennalestes trofimovi (Wible et al., 2001).
Younger mammalian specimens from late Cretaceous
deposits in Canada (84–77 Ma) had cochlear canals with
approximately 1 1/4 turns (Meng and Fox, 1995a) and
even younger specimens from the Bug Creek Anthills
locality in Montana (65 Ma) demonstrate cochleae with
1 1/2 turns (Meng and Fox, 1995b). The estimated hearing
for the placental specimens from the Bug Creek Anthills
locality ranged from 1.23 to 87.7 kHz and that of a marsupial from the same site had a range from 1.58 to 73.8 kHz
(Meng and Fox, 1995b). This evidence suggests that therian mammals living around the time of the K-T boundary
were characterized by heightened high-frequency hearing
but relatively poor low-frequency sensitivity.
During the Cenozoic, therians apparently continued
these trends in auditory evolution and developed essentially modern morphologies (and presumably hearing
patterns) by the Miocene. Fleischer (1976) compared the
ear structures in extinct and living cetaceans and concluded that the specialized hearing of odontocetes
related to echolocation evolved during the Oligocene and
was essentially similar to modern patterns by the Miocene. More recently, Coleman et al. (2010) examined the
middle and inner ears of Miocene aged fossil New World
monkeys and predicted that these 20 my old primates
had low- (and possibly high-) frequency sensitivity similar to living monkeys from South America. However,
there is still a paucity of studies that have focused on
reconstructing hearing patterns from the early Cenozoic,
a period that figures prominently in arguments like the
‘‘Masterson hypothesis’’ (Masterson et al., 1969).
The primate fossil record offers an opportunity to begin
to address this problem due to the abundance of specimens
that span the Cenozoic era. In this study, we examined relevant auditory structures in 21 species of extinct primates
and closely related taxa that range in geologic age from 60
Ma until near-modern times. We then compared these
specimens with a sample of extant euarchontans (Fig. 2)
and used predictive equations to estimate the low- and
high-frequency sensitivity of the fossils.
MATERIALS AND METHODS
The fossil specimens examined in this study are given
in Table 1. The actual fossils themselves were not analyzed. Instead, high resolution X-ray computed
tomography (HRXCT) was used to construct digital
COLEMAN AND BOYER
Fig. 2. Basic euarchontan relationships and taxonomic terms.
Euarchonta is a superordinal grouping of primates, dermopterans and
scandentians and their fossil ancestors. Names in parentheses are
common names and those with a dagger (†) indicate an extinct group.
models of auditory structures (see below) that are often
preserved in fossils and that have been found to be functionally relevant. The fossil specimens were scanned at
various institutions and the voxel dimensions for each
specimen are given in Table 1. The geologically oldest
assemblage of fossils belong to the group referred to as
plesiadapiformes, which are now thought to be stem primates with a sister-group relationship to Euprimates
(Bloch et al., 2007). Our sample consisted of six species
of small to medium-sized plesiadapiforms from North
America and Europe that range in age from 60 to 54 Ma.
The next group consisted of three medium-sized fossil
primates from North America and Europe called adapoids that range in age from 50 to 35 Ma. We also
examined two similarly aged (45–35 Ma) small to
medium-sized species of omomyoids from North America and Europe. Our sample included one 45 Ma primate
specimen from China that has been suggested to represent a basal anthropoid‡ (MacPhee et al., 1995). In
addition, we sampled four species of medium-sized
unambiguous fossil anthropoids: one 30 Ma fossil from
Africa and three 20 Ma fossils from South America.
Lastly, we examined five species of extinct large-bodied
subfossil lemurs that come from recent geological deposits in Madagascar (late Pleistocene-Holocene).
Extant Comparative Sample
The main comparative sample analyzed in this study
(Table 2) consisted of a phylogenetically diverse group of
25 species (72 specimens total) of living euarchontans.
This sample included seven species of platyrrhines (New
World monkeys), three species of catarrhines (Old World
monkeys) and four species of Tarsiers, which are collectively referred to as haplorhines (¼ anthropoids þ
tarsiers). In addition, we sampled five species of lorisoids
and two species of lemuroids that belong to the primate
suborder termed strepsirhines. We also examined four
species of nonprimate euarchontans: two species of scandentians (treeshrews) and two species of dermopterans
As with the fossil specimens, HRXCT was used to create digital models of relevant auditory structures. Most
extant specimens were scanned at the University of
Technically, the correct designation for the infraorder consisting
of New World monkeys þ Old World monkeys þ Apes may be Simiiformes (Groves, 2005), but in this article we use the traditional
designation of Anthropoidea to avoid confusion with the recent literature involving this group.
Texas High-Resolution X-ray CT facility (Table 2). These
scans had voxel dimensions measuring 62.5 lm
62.5 lm 68.0 lm and the final images were 16 bit
TIFF files. However, a subset of the extant specimens
was scanned at higher resolutions. These included one
specimen of Tarsius syrichta and two specimens of
Tarsius tarsier (15.0 lm 15.0 lm 15.0 lm), one specimen of Cynocephalus volans (15.0 lm 15.0 lm 15.0
lm), and four specimens of Ptilocercus lowii (24.0 lm
24.0 lm 26.0 lm). Besides the extant specimens that
were analyzed using computed tomography, additional
data on oval window area (or stapedial footplate area)
for 71 primate species were taken from published
reports (Coleman et al., 2010) augmented with previously unpublished data for several species (Appendix 1).
Measuring Auditory Structures
Cochlear length (CL) in fossil and living specimens
was estimated by creating digital endocasts of the inner
ear using HRXCT and measuring the outer circumference of the cochlear canal. Image stacks were imported
into ImageJ 1.35f (NIH) where threshold values were
determined using the half-maximum height protocol
described in Coleman and Colbert (2007). The image
stacks were then loaded into 3D Slicer 2.6 open source
software, where all measurements were taken on three
dimensional digital models. The measurements were
taken by placing markers (fiducials) at the smallest possible intervals along the outer circumference of the
digital cochlear endocast, starting at the distal edge of
the round window and continuing until the approximate
location of the helicotrema. The distance between adjacent fiducial points was then measured and all distances
summed to derive the total length estimate.
The number of cochlear spirals (CS) was counted by
placing a transparent radial grid (divided into one
eighths) over two dimensional images of the cochlear
endocasts in apical view. The measurement was started
from the distal edge of the round window similar to previous studies (West, 1985). The digital cochlear endocasts
were also used to evaluate the potential presence of secondary bony laminae that support the outer edge of the
basilar membrane (all specimens observed appeared to
have primary bony laminae). It should be noted that
because secondary bony laminae are relatively thin and
fragile structures, it may be possible to not detect their
presence (in specimens that possess them) if the voxel
dimensions are too large or if the specimen is damaged.
However, we detected secondary bony laminae in some
specimens that were scanned at the lowest resolution
(62.5 lm 62.5 lm 68.0 lm) of any of the specimens in
our dataset, suggesting it should be possible to distinguish
its presence when adequately developed. The final structure measured using HRXCT was oval window area
(OWA). This structure was estimated by measuring the
major and minor axes (length and width) of the oval window (or stapedial footplate if the stapes was preserved).
These measurements were then used to calculate the area
using the formula for an ellipse.
Predicting Hearing Sensitivity
The predictive equations used to estimate certain parameters of hearing sensitivity in the fossil specimens
TABLE 1. Fossil taxa examined in this study
Bloch & Gingerich (1998)
Silcox et al. (2009)
Kay et al. (2008)
Coleman et al. (2010)
Seiffert, E. (pers. comm.)
MacPhee et al. (1995)
The units for cochlear length (CL) are in millimeters, those for oval window area (OWA) are in millimeters squared, those for body mass (BM) are in grams and
those for voxel dimensions are in microns. CS refers to number of cochlear spirals and SBL refers to the number of spirals of the secondary bony lamina (when
present). BM Ref. refers to references used for body mass estimates. Body mass estimates with an asterisk (*) based on the mean of the smallest and largest species in the genus (because the exact species designation is unknown). Body mass estimate for Tremacebus (**) based on the value for Dolichocebus but reduced to
1,500 g because of the slightly shorter skull length (Kay et al., 2008).
INNER EAR EVOLUTION IN PRIMATES
COLEMAN AND BOYER
TABLE 2. CL estimates for extant taxa examined in this study
2 3/4 – 3
1/2 – 2 7/8
3 – 3 1/8
1/4 – 2 5/8
7/8 – 3 1/8
1/2 – 2 3/4
5/8 – 2 7/8
3/8 – 2 1/2
7/8 – 3 1/8
3/8 – 2 1/2
2 – 2 3/8
1/4 – 2 1/2
7/8 – 3 1/8
2 7/8 – 3
2 7/8 – 3
2 7/8 – 3
1/2 – 3 5/8
5/8 – 3 7/8
3/4 – 3 7/8
2 3/4 – 3
CL units are in millimeters, N represents number of specimens examined and S.D. represents one standard deviation. CS and
SBL abbreviations the same as in Table 1. Body mass (BM) estimates are in grams and are taken from Smith and Jungers
(1997) for primates, from Askay (2000) for tree shrews, and from Myers (2000) for colugos except where noted by asterisks.
Body mass estimates for Nycticebus javanicus (*) based on Nekaris et al. (2008) and those for Tarsius pelengensis based on
mean values for T. bancanus and T. syrichta which have similarly sized skulls as T. pelengensis (unpublished data).
were based on previous research on the functional morphology of the auditory system in living euarchontans
with known hearing abilities (Coleman, 2007; Coleman
and Colbert, 2010). This research found a significant
relationship (r2 ¼ 0.922, P < 0.001) between CL and
sound pressure level at 250 Hz ([email protected]
described by the formula:
y ¼ 2:433ðxÞ þ 83:43
where x ¼ CL in millimeters and y ¼ [email protected]
decibels (relative to 20 lPa). This research also detected
a significant, albeit weaker association (r2 ¼ 0.579, P ¼
0.011) between OWA and sound pressure level at 32 kHz
kHz) described by the formula:
y ¼ 21:467ðxÞ þ 0:297
where x ¼ OWA in millimeters2 and y ¼ [email protected]
decibels. In this study we used [email protected]
Hz as a measure of low-frequency sensitivity and [email protected]
kHz as a
measure of high-frequency sensitivity and predicted
these variables in fossil taxa using the formulae presented above.
In addition to predicting low- and high-frequency sensitivity in individual fossils, CL and OWA were
reconstructed for ancestral nodes and these values were
then used to predict low- and high-frequency sensitivity
at the basal stems leading to haplorhines, strepsirrhines,
and all primates. Ancestral state reconstructions were
performed with Mesquite (1.12) modular system for evolutionary analysis (Maddison and Maddison, 2006), based
on a squared-change parsimony model. Using a relatively
well-resolved phylogeny and character values for terminal
taxa (species), evolutionary programs such as Mesquite
use algorithms to reconstruct values at internal nodes of
a phylogenetic tree (i.e., essentially weighted mean values). Incorporating temporal information (branch length
data) and fossil taxa can greatly increase the confidence
in ancestral reconstructions, particularly toward the base
of a phylogenetic tree (Finarelli and Flynn, 2006).
Phylogenetic Relationships and
The data used to construct the phylogenetic relationships and divergence dates for living euarchontans was
based primarily on Perelman et al. (2011) that used
both molecular evidence and fossil calibration points.
In addition, the split within scandentia (Tupaia from
Ptilocercus) was based on Bininda-Emonds et al. (2007).
The position of fossil New World monkeys (Dolichocebus,
Tremacebus, Homunculus) as stem platyrrhines is based
on analyses presented in Kay et al. (2008) and the designation of Aegyptopithecus as a stem catarrhine is from
Fleagle (1999). The divergence times and relationships
of the subfossil lemurs is based on Godfrey and Jungers
(2003) and Orlando et al. (2008). The designation of omomyoids as stem haplorhines and adapoids as stem
strepsirrhines is based on traditional as well as recent
phylogenetic analyses (Szalay and Delson, 1979; Martin,
1990; Ross et al., 1998; Fleagle, 1999; Seiffert et al.,
INNER EAR EVOLUTION IN PRIMATES
Fig. 3. Relative CL and OWA in extant and fossil taxa. Scatterplots
showing the log of body mass regressed against the log of CL and
OWA. Regression lines based on extant data only. A: Upper black line
¼ haplorhine line (r2 ¼ 0.692, P < 0.001), lower black line ¼ nonhaplorhine line (r2 ¼ 0.742, P < 0.001), light gray line ¼ all taxa line (r2 ¼
0.388, P < 0.001). Extant haplorhines have relatively longer cochlea
than any of the other groups. Note the relatively short cochleae in plesiadapiformes. B: Black line ¼ all taxa (r2 ¼ 0.825, P < 0.001). In this
comparison, haplorhines appear no different than the other groups.
2009). The intragroup relationships and position of plesiadapiforms as sister taxa to Euprimates is based on
Bloch et al. (2007). The taxonomic affinity of the Shanghuang petrosal has been argued to resemble either a
basal anthropoid (MacPhee et al., 1995) or possibly an
omomyoid (Ross and Covert, 2000). Both phylogentic
interpretations are investigated here.
1/2–3; strepsirrhines ¼ 2–2 3/4; dermopterans ¼ 2 1/4–2
7/8; scandentians ¼ 2 3/4 – 3 1/8). In fact, tarsiers have
more spiral turns than almost any other mammal that
has been examined with the exception of a few animals
like guinea pigs that display an average of 4 1/4 turns
(West, 1985). Tarsiers also exhibit a well developed secondary bony lamina that extends along the radial wall
of the cochlear canal for approximately two full spiral
turns (Fig. 4). In contrast, secondary bony laminae were
not identified in any of the anthropoids examined here
(e.g., Saimiri – Fig. 4).
CL values in living strepsirrhines generally cluster
around the nonhaplorhine regression line indicating relatively shorter cochleae compared with tarsiers and
anthropoids (Fig. 3A). Also unlike anthropoids, some of
the strepsirrhines appear to display some indication of a
secondary bony lamina. The lamina is most highly
expressed in Galago senegalensis which shows a depression on the outer surface of the cochlear endocasts
which extends for approximately 1/2 turn (Fig. 4). A secondary spiral (bony) lamina was also identified in
galagos in a previous study by Fleischer (1973). Eulemur
fulvus also shows indications of a secondary bony lamina, although not as distinct as in galagos and it appears
to stretch for only 1/4 – 1/2 turns. Lemur, Nycticebus,
Perodicticus, and Loris could also have short secondary
laminae (1/4 turn) but the current evidence from the
cochlear endocasts does not allow for a conclusive determination. Higher resolution CT scans are needed to
better evaluate the extent of development of this structure in these and other strepsirrhine taxa.
The recently extinct subfossil lemurs show a similar
pattern in CL to their smaller bodied living relatives,
although there is more scatter around the nonhaplorhine
line. Despite their large body mass, most subfossil lemur
cochleae are no longer than New World monkeys like
Aotus and Saimiri that are well over an order of magnitude smaller in body mass (Table 2). Archaeolemur sp.
presents the main exception to this pattern [often called
the ‘‘monkey-lemur’’ because of its post-cranial and
The first results to discuss relate to the association
between CL and body mass in living and recent (i.e.,
subfossil lemurs) taxa. Considering all of the taxonomic
groups together (Fig. 3A—light gray line), there is a significant positive relationship between CL and body mass
(r2 ¼ 0.388, P < 0.001). However, the amount of variation explained (coefficient of determination ¼ r2) is much
higher when extant haplorhines (r2 ¼ 0.692, P < 0.001)
are considered separately from the other extant euarchontans (r2 ¼ 0.742, P < 0.001). This is interpreted to
indicate that the relative length of the cochlea is divided
into two distinct groups (Fig. 3A—dark black lines):
Extant haplorhines have the relatively longest cochleae
while nonhaplorhine taxa generally have relatively
shorter cochleae. There is also a significant positive relationship between body mass and OWA in extant and
recent taxa (r2 ¼ 0.825, P < 0.001). However, in this
comparison haplorhines do not appear to be distinct
from the other euarchontan taxa and are scattered along
both sides of the best fit regression line (Fig. 3B).
Although the phylogenetic relationship of tarsiers
remains debatable (Perelman et al., 2011), this study
reveals that they share certain similarities in cochlear
structure with living anthropoids. For example, tarsiers
have remarkably long cochleae for their body size (20.1–
24.1 mm) and three of the four species investigated fall
above the haplorhine regression line (Fig. 3A). They also
demonstrate a high number of spiral turns (3 1/2–3 7/8),
which is most similar to the catarrhines among the taxa
in our study (catarrhines ¼ 2 7/8–3 1/8; platyrrhines ¼ 2
COLEMAN AND BOYER
Fig. 4. CT cochlear endocast models for representative living
euarchontans (anthropoid, tarsier, strepsirrhine and treeshrew) and
fossil primates (plesiadapiform, adapoid, omomyoid, and the Shanghuang petrosal). All models scaled to approximately the same size.
Note the high number of spiral turns and development of the secondary bony lamina (black arrows) in Tarsius. Also, note the lack of any
evidence of a secondary lamina in squirrel monkeys (Saimiri).
dental similarities to Old World monkeys (Fleagle,
1999)], and had an estimated relative CL more similar
to living haplorhines (Fig. 3A). Subfossil lemurs display
1 7/8–2 5/8 spiral turns of the cochlea and none of the
specimens examined here demonstrated indications of a
secondary bony lamina. Considering OWA, most subfossil lemurs show relatively small values based on body
mass estimates for these species (Fig. 3B). In fact, Megaladapis sp. and Palaeopropithecus sp. had areas that
were approximately half the size of chimpanzees (Pan
troglodytes), which are roughly equivalent in overall
mass. As with CL, Archaeolemur is unusual compared
with the other subfossil lemurs and shows a mean value
for OWA that falls just above the regression line (Fig.
Common treeshrews (Tupaia glis) have the absolutely
(15.0 mm) and relatively shortest cochleae of any extant
species examined (Fig. 3A). Pen-tailed treeshrews (Ptilocercus lowii) actually have slightly longer cochleae and
are somewhat more coiled than common tree-shrews despite being over three times smaller in body mass. These
two species of treeshrews also have among the smallest
values for OWA (Fig. 3B). Tupaia glis displays indications of a secondary bony lamina that is reminiscent of
galagos although it appears to proceed for nearly one
full turn. The secondary lamina is quite evident on the
cochlear endocasts for Ptilocercus lowii and clearly
extends for at least one full turn (Fig. 4). Both genera of
dermopterans (Cynocephalus and Galeopterus) have CL
values that fall very close to the nonhaplorhine line.
What appears to be a thin secondary bony lamina
extends for about 1/2 turn in Cynocephalus volans, but
is not plainly visible on the endocasts of Galeopterus
variegatus. A previous analysis found that Cynocephalus
variegatus (¼ Galeopterus variegatus) had a weakly
developed ridge along the radial wall of the cochlear
canal but that it was structurally different from the secondary lamina of animals like tupaia and galagos and
more similar to the condition (spiral ligament) in
humans (Fleischer, 1973).
Plesiadapiformes, the geologically oldest taxa, had relatively
euarchontans and display values that consistently place
below the nonhaplorhine line (Fig. 3A). Plesiadapis
INNER EAR EVOLUTION IN PRIMATES
cookei had the longest cochlea of any plesiadapiform
examined but still was relatively shorter than any
extant species except common treeshrews. Carpolestes
simpsoni, had the shortest cochlea (8.6 mm – Fig. 3A)
and smallest number of cochlear spirals (1 1/2 turns –
Fig. 4) of any specimen examined, extinct or extant.
Most plesiadapiformes had OWA values that were close
to the best fit regression line although Carpolestes was
relatively smaller than most other taxa (Fig. 3B). Carpolestes also had a clearly developed secondary bony
lamina that extended for at least 1/2 turn (Fig. 4). All of
the remaining plesiadapiformes also appear to have had
a secondary lamina although generally not apparently
as developed as in Carpolestes (i.e., shallower depression
in the endocasts and extending only 1/4–1/2 turns).
In contrast to plesiadapiformes, the geologically
younger adapoids (50–35 Ma) all demonstrate CL values
that are very close to the nonhaplorhine regression line,
similar to most living strepsirrhines. However, the
adapoids we examined were similar to most plesiadapiformes in seemingly possessing a secondary bony lamina
that was about 1/4–1/2 turns long (e.g., Adapis - Fig. 4).
The roughly coeval omomyoids illustrate a mixed pattern with one species showing similarities to adapoids
while the other species resembles plesiadapiformes in
some respects. The smaller and older of the two species,
Omomys carteri (45 Ma), had a relatively short cochlea,
with values falling below the nonhaplorhine line (Fig.
3A), and demonstrably had a secondary lamina that
extended for nearly one full turn (Fig. 4). The larger
bodied and geologically younger Microchoerus (35 Ma),
on the other hand, produced a CL value that fell slightly
above the nonhaplorhine line and had a less developed
(although still visible) secondary lamina that was
approximately 1/4 turn long.
The 45 Ma Shanghuang petrosal, a possible basal
anthropoid, had a short cochlea with relative values similar to most plesiadapiformes (Fig. 3A). In fact, the
Shanghuang petrosal had the second shortest cochlea of
any taxon in our sample (13.3 mm). The cochlear endocast
for this specimen also clearly revealed a secondary bony
lamina that goes at least one full spiral turn (Fig. 4). In
contrast, the 30–20 Ma unambiguous fossil anthropoids
show the longest cochleae of any extinct group examined.
Three of these specimens fall just below the haplorhine
line, while Tremacebus harringtoni actually falls slightly
closer to the nonhaplorhine line (Fig. 3A). However, a previous analysis of Tremacebus suggested that this
specimen may be distorted, reducing its apparent length
(Coleman et al., 2010). Regardless, none of these specimens displayed indications of a secondary bony lamina.
Using the values for CL and OWA, we estimated measures of low-frequency sensitivity ([email protected]
Hz) and highfrequency sensitivity ([email protected]
kHz) for each of the fossil
specimens using the predictive equations presented above
(Table 3). These values are illustrated in Figure 5 along
with the same audiometric parameters for extant anthropoids and strepsirrhines as well as two ‘‘primitive’’ living
placental mammals, treeshrews and hedgehogs.
Carpolestes simpsoni and the Shanghuang petrosal are
both predicted to have had relatively poor low-frequency
sensitivity that was outside the range of living primates
but intermediate between the values for treeshrews and
hedgehogs. Nannodectes, Omomys, and Pronothodectes
were also apparently less sensitive to low-frequency
TABLE 3. Predicted hearing sensitivity in fossils
62.4 (6 12.6)
31.6 (6 11.9)
23.2 (6 13.6)
17.5 (6 12.6)
26.8 (6 14.8)
9.1 (6 13.3)
Low-frequency ([email protected]
Hz) and high-frequency ([email protected]
kHz) sensitivity predictions and 95% confidence intervals
(6) for all extinct taxa investigated in this study. [email protected]
Hz predicted using CL values and [email protected]
using oval window area based on analyses in Coleman and
sounds with predicted values of [email protected]
the values for treeshrews and the upper limits for living
strepsirrhines. On the other side of the auditory spectrum, all of these taxa (in addition to Ignacius) appear
to have had good high-frequency sensitivity, based on
predictions from OWA, that was above the range of any
of the living anthropoids that have had their hearing
tested. In fact, the predicted values of [email protected]
Carpolestes, Shanghuang and Omomys were all below 10
dB SPL. In living primates, there is a significant correlation between [email protected]
kHz and high-frequency cutoff (r
¼ 0.833, P ¼ 0.003), and the few euarchontans that
have [email protected]
kHz values below 10 dB SPL also have a
high-frequency cutoff of 60 kHz or higher (Table 4).
What’s more, all of these taxa apparently had relatively well developed secondary lamina that extended
between 1/2 and one full spiral turn. The expression of
this feature also suggests that these taxa were well
adapted to hear high-frequencies based on the observation that Galago senegalensis and Tupaia glis show
similar development of the secondary lamina (1/2 and
one full turn, respectively) and have among the best
known high-frequency sensitivity of any extant euarchontan. The relationship between secondary laminae
development and good high-frequency sensitivity in primates is further supported by the recent finding that
Tarsius syrichta has a high-frequency cutoff of 75 kHz
(Ramsier et al., 2011), which is the highest of any primate tested, and also demonstrates the greatest
development of secondary laminae among the primates
in our sample (~two full turns – Fig. 4).
Low-frequency sensitivity in Plesiadapis tricuspidens,
P. cookei, Microchoerus, and the three adapoids we investigated appear to have been somewhat better than the
fossil taxa described above. The predicted values of
Hz are below those for treeshrews and are
COLEMAN AND BOYER
Fig. 5. Predicted low-frequency and high-frequency sensitivity for
fossil specimens. Sound pressure level at 250 Hz ([email protected]
used as a proxy for low-frequency sensitivity and sound pressure level
at 32 kHz ([email protected]
kHz) was used as a proxy for high-frequency sensitivity. Predicted values for the fossils are compared with the range of
values for living primates, treeshrews and hedgehogs (gray rectangles). Extant primate and treeshrew audiometric data based on Coleman (2009) and augmented with data for Callithrix jacchus (common
marmosets) from Osmanski and Wang (2011). Audiometric data for
hedgehogs from Ravizza et al. (1969b).
similar to the middle and lower values displayed by living
strepsirrhines but also overlap the upper values for
extant anthropoids. In other words, the estimated values
are toward the middle of the distribution of values in living forms (Fig. 5). Conversely, the predicted [email protected]
for these taxa suggests reduced high-frequency sensitivity
compared with the first group of fossils described and in
this case overlaps the range of values for living anthropoids. P. tricuspidens and Microchoerus produced values
that are found in all three comparative groups of living
taxa, whereas the values for P. cookei and Adapis were
higher than those for treeshrews (indicating less sensitivity) but still within the ranges of extant strepsirrhines
and anthropoids. These predicted values of [email protected]
plus the apparent presence of moderately developed secondary laminae in the fossils (1/4–1/2 turns) suggests an
upper frequency limit (high-frequency cutoff) between
41–58 kHz based on modern analogues (Table 4).
The four species of fossil anthropoids we examined all
produced predicted values of [email protected]
Hz that are similar to those found in living anthropoids but below the
range of strepsirrhines, treeshrews or hedgehogs (Fig.
5). In contrast, the estimated high-frequency sensitivity
for this group was less uniform. The predicted value of
kHz for Aegyptopithecus falls exclusively within
the range for extant anthropoids. In contrast, the value
for Dolichocebus also overlaps the range of values for
strepsirrhines and the value for Homunculus overlaps
the ranges of all three comparative groups. However,
considering the finding that secondary bony laminae
were not detected in any of these fossils (or in living
anthropoids) and the fact that the predicted values were
all encompassed by the range of living anthropoids, suggests a high-frequency cutoff between 34 and 45 kHz for
this group of fossils.
It should be noted that the predictive equation used to
estimate high-frequency sensitivity (based on OWA) has
a higher margin of error than the equation used to predict low-frequency sensitivity (based on CL). However,
these two traits may in fact be interrelated to some
degreee. Although Coleman and Colbert (2010) did not
find a significant relationship between high-frequency
sensitivity and CL, studies from other researchers have
identified such a relationship. Echteler et al. (1994) found
that the high-frequency cutoff in mammals goes up as
basilar membrane length decreases and Kirk and Gosselin-Ildari (2009) found that smaller cochlear volumes are
also related to increased high-frequency sensitivity.
Therefore, the general pattern identified here that the
primates with smaller (shorter) cochleae also had smaller
OWAs strengthens the interpretations for changes in
high-frequency hearing based on oval window area alone.
TABLE 4. Values for [email protected]
kHz and high-frequency
cutoff in living euarchontans with known hearing
Sound pressure level at 32 kHz ([email protected]
kHz) in decibels
and high-frequency cutoff (Hi-Cut) in kilohertz. There is a
significant correlation between [email protected]
kHz and highfrequency cutoff in these euarchontan taxa (r ¼ 0.833,
P ¼ 0.003). Note that taxa with a value of less than 10 dB
for [email protected]
kHz also have a high-frequency cutoff of
60 kHz or higher.
INNER EAR EVOLUTION IN PRIMATES
Fig. 6. Reconstructed sequence of OWA and CL in euarchontans.
The values for OWA and CL in extant and fossil taxa were used to
reconstruct the values at key transitional nodes: (1) basal primates, (2)
basal strepsirrhines, (3) basal haplorhines, and (4) basal anthropoids.
Evolutionary changes in OWA (Fig. 6A) seem to be largely related to
To further investigate evolutionary trends in OWA,
CL and development of the secondary bony lamina, we
changes in body mass whereas variation in CL (Fig. 6B) shows grade
shifts whereby older fossil groups demonstrate relatively shorter cochleae. Asterisks along stems indicate development of the secondary
bony lamina for that clade unless otherwise noted. 1 (*) ¼ absent; 2
(**) ¼ poorly developed; 3 (***) moderate to highly developed.
mapped the values for these characters onto a phylogenetic tree and reconstructed the values for key
transitional points along the tree not represented by fossils (Fig. 6). One major challenge when constructing a
COLEMAN AND BOYER
Fig. 6. Continued.
phylogenetic tree of primates that includes the fossils in
our sample relates to the phylogenetic position of the
Shanghuang petrosal. As briefly described in the Materials and Methods Section, various authors have
suggested that the Shanghuang petrosal could be either
a basal anthropoid (MacPhee et al., 1995) or a member
of the Omomyiformes (Ross and Covert, 2000). As
revealed by our study, the cochlear endocast of the
Shanghuang petrosal is superficially similar to the cochlea of Omomys carteri in several characteristics (Fig. 4).
For example, they both have relatively short cochleae
(Fig. 3A), have a similar number of cochlear spirals (2 3/4
vs. 2 3/8), and both appear to have a secondary bony lamina that extended for about one turn. In addition, both
specimens have similar values for OWA (0.37 mm2 vs.
0.41 mm2). However, they do appear to differ somewhat
INNER EAR EVOLUTION IN PRIMATES
Fig. 7. Low-frequency sensitivity ([email protected]
Hz) and high-frequency
sensitivity ([email protected]
kHz) predictions for basal primates (1), basal
strepsirrhines (2), and basal haplorhines (3), compared with the audio-
grams for living primates and tree shrews (Coleman, 2009), hedgehogs
(Ravizza et al., 1969b), opossums (Ravizza et al., 1969a; Frost and
Masterton, 1994), and echidnas (Mills and Shepherd, 2001).
in the apical height of the cochlear spiral (Fig. 4). Regardless of phylogenetic affinity, the Shanghuang petrosal
likely had hearing capabilities that were very similar to
that of Omomys based on the predictions in sensitivity
presented here. Since the taxonomic identity of the
Shanghuang petrosal remains uncertain, we will tentatively consider it to belong to an Omomyiform although
we will also discuss the implications in the case that it
actually came from a basal anthropoid.
Evolutionary changes in OWA, and presumably highfrequency sensitivity, seem to be largely related to overall increases in body size (Fig. 3B, Fig. 6A). Small
mammals (with small heads) need heightened highfrequency sensitivity to take advantage of spectral cues
that aid in the ability to localize the source of a sound
(Heffner and Heffner, 2010). However, as animals get
larger, there is likely reduced selection to maintain
heightened high-frequency sensitivity for localization purposes. Therefore, if OWA is one of the proximate
mechanisms governing high-frequency sensitivity, then it
makes sense that increases in body size (and head size)
will be paralleled by increases in stapedial footplate size.
In many ways, the loss of secondary bony laminae in
some groups may also reflect this trend toward larger
body size in mammals. This may explain why the large
bodied subfossil lemurs appear to be devoid of secondary
laminae while at least some of the relatively smaller living strepsirrhines (e.g., Galago, Eulemur) apparently
possess such structures. However, the absence or presence of the secondary laminae is not strictly tied to body
size since small-bodied monkeys like tamarins and marmosets apparently lack them while similarly-sized
primates like galagos and lorises possess them (Fig. 6B).
It also does not appear that the development of secondary laminae is directly related to either CL or the
number of cochlear spirals since tarsiers show the greatest expression of laminae development, yet have a high
number of cochlear coils and relatively long cochleae,
similar to most monkeys and apes which lack laminae.
Regardless, the finding that all of the fossils older than
30 Ma in our sample appear to show some development
of a secondary bony lamina (Fig. 6B) supports the notion
that the presence of this structure is the ancestral condition for the cladotherian clade (Ruf et al., 2009).
When examining changes in CL, some interesting
phylogenetic and temporal patterns become evident (Fig.
6B). Note that only the geologically youngest fossils
show CL values that approach those found in living
forms. Although increases in body size through time
have no doubt resulted in overall increases in CL,
changes in body size alone cannot explain these patterns.
plesiadapiform with the longest cochlea (19.0 mm) and
among the largest in body mass (2,059 g) in our sample, still possessed a cochlea that was shorter than a
modern species like an owl monkey (Aotus trivirgatus –
22.4 mm), which is less than half the body mass
(775 g). In addition, the geologically older omomyoid
Omomys had a relatively shorter cochlea than the geologically younger omomyoid Microchoerus (Fig. 3A).
Furthermore, if the Shanghuang petrosal is that of a basal
anthropoid (or basal haplorhine for that matter), then there
is a large difference in relative CL between this 45 Ma
specimen compared with the 30–20 Ma fossil anthropoids
we investigated from Africa and South America.
The reconstructed values at the branch leading to all
primates (1 – Fig. 6) for OWA was 0.66 mm2 and that for
CL was 17.9 mm. These values suggest that basal primates had low-frequency sensitivity that was
intermediate between the mean values for extant strepsirrhines and treeshrews and high-frequency sensitivity
similar to living strepsirrhines (Fig. 7). Considering the
Shanghuang petrosal to belong to a stem anthropoid
only moderately influences these reconstructed values
(0.63 mm2 and 17.5 mm) and consequently does not significantly alter this interpretation. The reconstructed
values at the branch leading to strepsirrhines (2 – Fig.
6) was 0.77 mm2 for OWA and 19.6 mm for CL. These
values suggest slightly less high-frequency sensitivity
but slightly better low-frequency hearing than found in
COLEMAN AND BOYER
living strepsirrhines (Fig. 7). Again, evaluating this pattern with Shanghuang as a basal anthropoid had little
effect on the reconstructed values (0.74 mm2 and 19.3
mm). The reconstructed values at the branch leading to
haplorrhines (3 – Fig. 6) were 0.69 mm2 and 18.7 mm
suggesting both high- and low-frequency sensitivity that
was very similar to the mean for the extant strepsirrhines for which hearing sensitivity has been tested
(Fig. 7). As before, there are only minor changes if
Shanghuang is positioned as a basal anthropoid (0.64
mm2 and 18.1 mm).
In contrast to the minimal influence of the Shanghuang petrosal on the reconstructed values at the
branches labeled 1, 2, 3 discussed above, its phylogenetic
position does significantly alter the interpretations associated with the branch leading to anthropoids (4 –
Fig. 6). If the Shanghuang petrosal was that of an Omomyiform, then the reconstructed values at the branch
labeled 4 were 1.12 mm2 and 24.4 mm for OWA and CL,
respectively. This suggests that the relatively long cochleae characteristic of anthropoids and tarsiers is a
shared derived trait with an origin that likely stretches
back to the diversification of these two groups. However,
if the Shanghuang was actually from a basal anthropoid,
then the values at branch 4 are reconstructed to have
been 0.70 mm2 and 18.2 mm, similar to the inferred values for basal haplorrhines. This scenario implies that
the relatively long cochleae of tarsiers developed independently to that of anthropoids. Regardless of when
anthropoids and tarsiers began to develop their relatively long cochleae, it appears that their early ancestors
(basal haplorhines) were characterized by reduced lowfrequency and increased high-frequency sensitivity compared with modern and more recent species. The earliest
fossil evidence for hearing sensitivity that is on par with
that of living haplorrhines does not appear until 30–20
Ma as witnessed in definitive fossil anthropoids like
Aegyptopithecus and Dolichocebus (Fig. 5).
The pattern of increased cochlear coiling and elongation documented in Cretaceous mammals (see
introduction) is continued in the geologically younger fossil primates examined in this study. Comparable with the
Bug Creek Anthills specimens, Carpolestes simpsoni from
the late Paleocene had about 1 1/2 spiral turns, similar to
living hedgehogs that also display 1 1/2 turns of the cochlea. The predicted low-frequency sensitivity for C.
simpsoni (also similar to the known low-frequency sensitivity of hedgehogs) implies that this animal likely could
not have perceived sounds much below 250 Hz (based on
the traditional low-frequency cutoff of 60 dB). A recent
study of cochlear volume in this specimen also suggests
that C. simpsoni had a hearing range that was shifted toward higher frequencies (Armstrong et al., 2011).
The similarly aged Pronothodectes gaoi (middle-late
Paleocene) and Nannodectes intermedius (late Paleocene) had cochleae that spiraled for 2 1/8–2 3/8 turns
and ranged in length from 14.5–15.6 mm. The slightly
younger Plesiadapis tricuspidens and Plesiadapis cookei
(late Paleocene-early Eocene) had essentially the same
number of spirals (2 1/4–2 3/8) but slightly longer cochleae (17.0–19.0 mm). The three early-late Eocene
adapoids we investigated show a slight increase in cochlear turns (2 1/4–2 5/8) and CL (19.7–20.6) compared
with Plesiadapis spp. The omomyid, Omomys carteri
from the middle Eocene displays 2 3/4 spirals but a rela-
tively short length of 15.4 mm compared with the late
Eocene-early Oligocene Microchoerus sp. that exhibits a
cochlea with 3 1/8 turns and a length of 21 mm. Finally,
the fossil anthropoids in our sample show cochlear
characteristics that are within the range of extant
anthropoids (Table 2). Aegyptopithecus zeuxis (early Oligocene) had 2 7/8 turns (25.7 mm) and fossil
platyrrhines (early Miocene) had 2 3/4–3 1/8 turns (22–
24.5 mm) (Coleman et al., 2010).
Our results provide paleontological evidence that basal primates (late Cretaceous) had good high-frequency
sensitivity but relatively poor low-frequency sensitivity
compared with modern members of the order. Then, they
began to develop good low-frequency sensitivity with
slight decreases in high-frequency sensitivity starting
during the late Paleocene-early Eocene. Finally, essentially modern patterns had evolved by the Oligocene
(30 Ma), although slight modifications to the entire
auditory apparatus appear to have continued through the
early part of the Miocene (Coleman et al., 2010).
These findings, in combination with other studies on
geologically older mammals, are in accordance with the
hypothesis articulated by Masterson et al. (1969) that
mammals went through a period of reduced lowfrequency sensitivity during the evolution of modern
hearing patterns, although the timing of events are different than originally proposed. This purported sequence
of changes in hearing sensitivity has considerable implications for the evolution of vocal communication,
predator-prey interactions and the development of hearing specializations in mammals. For example, the
transition to a primarily high-frequency hearing pattern
was likely paralleled by a shift to higher vocalization frequencies making it improbable that early primates (and
possibly mammals as well) used low-frequency, longrange communication signals like those that are utilized
by many species of primates today. This also raises the
possibility that at least some early primate (and mammalian) vocalizations were above the upper limit of
hearing of contemporaneous nonmammalian predators
(i.e., dinosaurs), resulting in opportunities to exploit new
behavioral and ecological niches and potentially altering
predator-prey dynamics. Furthermore, the ancestral
hearing phase of good high-frequency and poor lowfrequency sensitivity (90–45 Ma) in primates may be
typical of other mammalian orders and would have been
a critical first step toward developing the unique hearing
patterns like those of echolocating bats. In fact, low-frequency sensitivity in many bats is very similar to that
in opossums (Fig. 1) suggesting that the ‘‘specialized’’
hearing of bats may not be that far removed from the
pattern that characterized mammals during the reduced
low-frequency sensitivity phase.
SUMMARY AND FUTURE DIRECTIONS
Plesiadapiformes, the earliest fossil primates for
which we have evidence were characterized by having
small oval window areas and relatively short cochlea
that housed moderate to well-developed secondary bony
laminae. These traits are interpreted to suggest that
these taxa had good high-frequency but relatively poor
INNER EAR EVOLUTION IN PRIMATES
between extant strepsirrhines and primitive living mammals like treeshrews and hedgehogs. Then, with the
origin of haplorrhines and strepsirrhines (Euprimates), primates began to develop relatively longer cochleae and
reduced expression of secondary bony laminae indicating
an increase in low-frequency sensitivity and modest reductions in high-frequency sensitivity. This ‘‘strepsirrhine’’
stage of hearing dates back to at least the Eocene (50
Ma) based on fossil taxa like adapoids but could date well
back into the late Cretaceous based on molecular evidence.
Finally, sometime after the origin of Euprimates, haplorrhines continued the pattern of cochlear elongation
and reduction (or loss) of secondary bony laminae
(except in tarsiers). The African and South American
fossil evidence suggest that this process was completed
by the early Miocene, but the origin of this stage of
primate hearing remains unresolved. Early fossil haplorrhines like Omomys and the Shanghuang petrosal
suggest that haplorrhines and strepsirrhines (and
possibly anthropoids and tarsiers as well) may have developed cochlear elongation independently, relative to the
basal primate condition. Among living haplorrhines, only
tarsiers have developed relatively long cochleae while
still retaining well developed secondary bony laminae—
adaptations that apparently confer both heightened highand low- frequency sensitivity to this unique genus.
Paleontological evidence and comparative studies on
auditory function promise to continue refining our
understanding of hearing evolution. Investigating more
primate specimens from the Eocene and Oligocene will
shed more light on the evolution of the hearing patterns
in primates and help put these findings in a larger theoretical framework. In particular, analyzing the auditory
region of (definitive) basal anthropoids could help us
understand the development of the unique traits of this
group of primates (to which humans belong). It will
also be interesting to begin examining other orders of
mammals (e.g., rodents, carnivores) from the early
Cenozoic to see if similar patterns of auditory evolution
have occurred. Ultimately, this type of information
contributes to a more complete understanding of the
environmental processes that have resulted in the
behavioral and ecological diversity seen among primates,
mammals, and other vertebrate groups.
We thank the following individuals and institutions for
access to fossil CT data: J.I. Bloch (U. Florida) and M.T.
Silcox (U. Winnipeg) – Carpolestes, Ignacius; H.H.
Covert (U. Colorado) – Microchoerus, Omomys; R. Emry
(Smithsonian) – Nannodectes; R.C. Fox (U. Alberta) –
Pronothedectes; P.D. Gingerich (U. Michigan) – P. cookei;
M. Godinot (National d’Histoire Naturelle, Paris) – Adapis, P. tricuspidens; R. F. Kay (Duke U.) – Dolichocebus,
Homunculus, Tremacebus; E.R. Seiffert (Stony Brook U.)
– Aegyptopithecus; E.L. Simons (Duke U.) – Aegyptopithecus, Archaeolemur, Babakotia, Megaladapis, Mesopropithecus, Palaeopropithecus; A. Walker (Pennsylvania
State U.) – Notharctus and Smilodectes (used with permission of the Division of Paleontology, AMNH), Adapis,
P. tricuspidens; K.C. Beard (Carnegie) – Shanghuang petrosal. J. Rossie provided scans for Loris and Saguinus
(NSF BCS-0100825). The following people also helped
with scanning and obtaining CT data: M. Colbert, L. Gordan, T. Ryan, A. Walker, E. Westwig. We would also like to
acknowledge B. Demes, J. Georgi, A. Grossman, C. Heesy,
W. Jungers, J. Rosowski, and C. Ross for helpful discussions and comments about the analysis and early versions
of the manuscript. Lastly, we thank two anonymous
reviewers for useful comments on the manuscript.
Aitkin LM, Johnston BM. 1972. Middle-ear function in a monotreme-echidna (Tachyglossus aculeatus). J Exp Zool 180:245–250.
Armstrong SD, Bloch JI, Houde P, Silcox MT. 2011. Cochlear labyrinth volume in euarchontoglirans: implications for the evolution
of hearing in primates. Anat Rec 294:263–266.
Askay S. 2000. Ptilocercus lowii (On-line). Animal diversity web.
Available at: http://animaldiversity.ummz.umich.edu/site/accounts/
information/Ptilocercus_lowii.html. Accessed 4.10.2010.
Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R,
Grenyer R, Price S, Vos R, Gittleman J, Purvis A. 2007. The
delayed rise of present-day mammals. Nature 446:507–512.
Bloch JI, Gingerich P. 1998. Carpolestes simpsoni, a new species
(Mammalia, Proprimates) from the late Paleocene of the Clark’s
Fork Basin, Wyoming. Contributions from the Museum of Paleontology: The University of Michigan. Vol. 30: p 131–162.
Bloch JI, Silcox MT, Boyer DM, Sargis EJ. 2007. New Paleocene
skeletons and the relationship of plesiadapiforms to crown-clade
primates. PNAS USA 104:1159–1164.
Boyer DM. 2009. New cranial and postcranial remains of late Paleocene plesiadapidae (Plesiadapiformes, Mammalia) from North
America and Europe: descriptions and evolutionary implications.
Anatomy. Stony Brook, New York: Stony Brook University.
Bruns V. 1980. Basilar membrane and its anchoring system in the
cochlea of the greater horseshoe bat. Anat Embryol 161:29–50.
Coleman MN. 2007. The functional morphology and evolution of the
primate auditory system. Anthropology. Stony Brook University,
Stony Brook, New York.
Coleman MN. 2009. What do primates hear? A meta-analysis of all known
nonhuman primate behavioral audiograms. Int J Prim 30:55–91.
Coleman MN, Colbert MW. 2007. Technical note: CT thresholding
protocols for taking measurements on three-dimensional models.
Am J Phys Anth 133:723–725.
Coleman MN, Colbert MW. 2010. Correlations between auditory
structures and hearing sensitivity in non-human primates.
J Morph 271:511–532.
Coleman MN, Kay RF, Colbert MW. 2010. Auditory morphology and
hearing sensitivity in fossil New World monkeys. Anat Rec 293:
Dalland J. 1965. Hearing sensitivity in bats. Science 150:1185–1186.
Dooling R, Lohr B, Dent ML. 2000. Hearing in birds and reptiles.
In: Dooling R, Fay RR, Popper AN, editors. Comparative hearing:
birds and reptiles. Springer-Verlag, New York, pp. 308–359.
Echteler SM, Fay RR, Popper AN. 1994. Structure of the mammalian cochlea. In: Fay RR, Popper AN, editors. Comparative hearing: mammals. New York: Springer-Verlag. pp. 134–171.
Fay RR. 1988. Hearing in Vertebrates: A Psychophysics Data Book.
Hill-Fay Associates, Winnetka, IL.
Finarelli JA, Flynn JJ. 2006. Ancestral state reconstruction of body
size in the caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record. Syst Biol 55:301–313.
Fleagle JG. 1999. Primate adaptation and evolution. San Diego:
Fleischer G. 1973. Studien am Skelett des Geh€
augetiere, einschliesslich des Menschen Mitt 21:131–239.
Fleischer G. 1976. Hearing in extinct cetaceans as determined by
cochlear structure. J Paleontol 50:133–152.
Fleischer G. 1978. Evolutionary principles of the mammalian middle ear. Berlin: Springer-Verlag.
Flydal K, Hermansen A, Enger PS, Reimers E. 2001. Hearing in
reindeer (Rangifer tarandus). J Comp Physiol A 187:265–269.
COLEMAN AND BOYER
Fox RC, Meng J. 1997. An X-radiographic and SEM study of the osseous inner ear of mulituberculates and monotreme (Mammalia):
Implications for mammalian phylogeny and evolution of hearing.
Zool J Linn Soc 121:249–291.
Frost SB, Masterton RB. 1994. Hearing in primitive mammals:
Monodelphis domestica and Marmosa elegans. Hear Res 76:67–72.
Gilbert CC. 2005. Dietary ecospace and the diversity of euprimates during the early and middle eocene. Am J Phys Anthro. 126:237–249.
Godfrey LR, Jungers WL. 2003. Subfossil lemurs. In: Goodman SM,
Benstead JP, editors. The natural history of Madagascar. Chicago:
University of Chicago Press. p 1247–1252.
Groves CP. (2005). Order primates. In: Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. Baltimore: The Johns Hopkins University Press. p 111–184.
Heffner HE. 1976. Hearing in large and small dog (Canis familiaris). J Acoust Soc Am 60:S88.
Heffner HE, Masterton B. 1980. Hearing in glires: domestic rabbit, cotton rat, feral house mouse and kangaroo rat. J Acoust Soc Am 68:
Heffner HE, Heffner RS. 1985a. Hearing in two cricetid rodents:
Wood rat (Neotoma floridana and grasshopper mouse (Onychomys
leucogaster). J Comp Psychol 99:275–288.
Heffner HE, Heffner RS, Contos C, Ott T. 1994a. Audiogram of the
hooded Norway rat. Hear Res 73:244–247.
Heffner RS, Heffner HH, Masterton B. 1971. Behavioral measurements of absolute and frequency difference thresholds in guinea
pig. J Acoust Soc Am 49:1888–1895.
Heffner RS, Heffner HE. 1982. Hearing in the elephant (Elephas
maximus) - Absolute sensitivity, frequency discrimination, and
sound localization. J Comp Physiol Psychol 96:926–944.
Heffner RS, Heffner HE. 1983. Hearing in large mammals - horse
(Equus caballus) and cattle (Bos taurus). Behav Neurosci 97:299–309.
Heffner RS, Heffner HE. 1985b. Hearing range in the domestic cat.
Hear Res 19:85–88.
Heffner RS, Heffner HE. 1985c. Hearing in mammals: the least
weasel. J Mamm 66:745–755.
Heffner RS, Heffner HE. 1990a. Hearing in domestic pigs (Sus
scrofa) and goats (Capra hircus). Hear. Res. 48:231–240.
Heffner RS, Heffner HE. 1990b. Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear Res 46:239–252.
Heffner RS, Heffner HE. 1991. Behavioral hearing range of the
chinchilla. Hear Res 52:13–16.
Heffner RS, Heffner HE. 1992. Hearing and sound localization in
blind mole rats, Spalax ehrenbergi. Hear Res 62:206–216.
Heffner RS, Heffner HE. 1993. Degenerate hearing and sound localization in naked mole rats (Heterocephalus glaber), with an overview of central auditory structures. J Comp Neurol 331:418–433.
Heffner RS, Heffner HE. 2010. Explaining high frequency hearing.
Anat Rec 293:2080–2082.
Heffner RS, Heffner HE, Contos C, Kearns D. 1994b. Hearing in
prairie dogs: transition between surface and subterranian
rodents. Hear Res 73:185–189.
Heffner RS, Koay G, Heffner HE. 2001. Audiograms of five species
of rodents: implications for the evolution of hearing and the perception of pitch. Hear Res 157:138–152.
Heffner RS, Koay G, Heffner HE. 2003. Hearing in American leafnosed bats. III: Artibeus jamaicensis. Hear Res 184:113–122.
a S, Nummela S, Reuter T. 1995. What middle ear parameters tell about impedance matching and high frequency hearing.
Hear Res 85:31–44.
Jackson LL, Heffner HE, Heffner RS. 1997. Audiogram of the fox
squirrel (Sciurus niger). J Comp Psychol 111:100–104.
Jackson LL, Heffner RS, Heffner HE. 1999. Free-field audiogram of the
Japanese macaque (Macaca fuscata). J Acoust Soc Am 106:3017–3023.
Jerison HJ. 1973. Evolution of the brain and intelligence. New
York: Academic Press.
Kay RF, Fleagle JG, Mitchell TRT, Colbert M, Bown T, Powers DW.
2008. The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. J Hum Evol 54:323–382.
Kelly JB, Kavanagh GL, Dalton JCH. 1986. Haring in the ferret
(Mustela putorius) - thresholds for pure tone detection. Hear Res
Kermack KA, Mussett F. 1983. The ear in mammal-like reptiles and
early mammals. Acta Palaeont Pol 28:147–158.
Ketten DR. 1992. The marine mammal ear: specializations for
aquatic audition and echolocation. In: Webster DB, Fay RR, Popper AN, editors. The evolutionary biology of hearing. New York:
Springer-Verlag. p 717–750.
Kirk EC, Gosselin-Ildari AD. 2009. Cochlear labyrinth volume and
hearing abilities in primates. Anat Rec 292:765–776.
Koay G, Bitter KS, Heffner HE, Heffner RS. 2002. Hearing in American leaf-nosed bats. 1: Phyllostomus hastatus. Hear Res 171:96–102.
Koay G, Heffner HE, Heffner RS. 1997. Audiogram of the big brown
bat (Eptesicus fuscus). Hear Res 105:202–210.
Koay G, Heffner RS, Bitter KS, Heffner HE. 2003. Hearing in American leaf-nosed bats. II: Carollia perspicillata. Hear Res 178:27–34.
Koay G, Heffner RS, Heffner HE. 1998. Hearing in a megachiropteran
fruit bat (Rousettus aegyptiacus). J Comp Psychol 112:371–382.
Konishi M. 1973. How owl tracks its prey. Am Scient 61:414–424.
Lewis ER, Leverenz EL, Bialek WS. 1985. The vertebrate inner ear.
Boca Raton, FL: CRC Press.
Long GR, Schnitzler HU. 1975. Behavioral audiograms from the
bat, Rhinolophus ferrumequinum. J Comp Physiol 100:211––219.
Luo Z, Ruf I, Schultz JA, Martin T. 2011. Fossil evidence on evolution
of inner ear cochlea in Jurassic mammals. Proc R. Soc B 278:28–34.
MacPhee RDE, Beard KC, Qi T. 1995. Significance of primate petrosal from middle eocene fissure-fillings at Shanghuang, Jiangsu
Province, People’s Republic of China. J Hum Evol 29:501–514.
Maddison WP, Maddison DR. 2006. Mesquite: A modular system for
evolutionary analysis. Version 1.12. Available at: http://mesquiteproject.org. Accessed on March 20, 2008.
Manley GA. 1972. Review of some current concepts of functional evolution of the ear in terrestrial vertebrates. Evolution 26:608–621.
Martin RD. 1990. Primate origins and evolution: A phylogenetic
reconstruction. Princeton, NJ: Princeton University Press.
Masterson RB, Heffner H, Ravizza R. 1969. The evolution of human
hearing. J Acoust Soc Am 45:966–985.
Meng J, Fox RC. 1995a. Osseous inner-ear structures and hearing
in early marsupials and placentals. Zool J Linn Soc 115:47–71.
Meng J, Fox RC. 1995b. Therian petrosals from the Oldman and
milk river formations (Late Cretaceous), Alberta, Canada. J Vert
Meng J, Wyss AR. 1995. Monotreme affinities and low-frequency
hearing suggested by multituberculate ear. Nature 377:141–144.
Meng J, Wang Y, Li C. 2011. Transitional mammalian middle ear
from a new Cretaceous Jehol eutriconodont. Nature 472:181–185.
Mills DM, Shepherd K. 2001. Distortion product otoacoustic emission and auditory brainstem responses in the echidna (Tachyglossus aculeatus). JARO 2:130–146.
Muller M, Wess FP, Bruns V. 1993. Cochlear place-frequency map
in the marsupial Monodelphis domestica. Hear Res 67:198–202.
Myers P. 2000. "Dermoptera" (On-line). Animal diversity web.
Nekaris KAI, Blackham GV, Nijman V. 2008. Conservation implications of low encounter rates of five noctural primate species (Nycticebus spp.) in Asia. Biodivers Conserv 17:733–747.
Neuweiler G. 1984. Foraging, echolocation and audition in bats.
Orlando L, Calvignac S, Schnebelen C, Douady CJ, Godfrey LR,
anni C. 2008. DNA from extinct gaint lemurs links archaeolemurids to extant indriids. BMC Evol Biol 8:121.
Osmanski MS, Wang X. (2011). Measurement of absolute auditory
thresholds in the commom marmoset (Callithrix jacchus). Hear
Perelman P, Johnson WE, Roos C, Seu
anez HN, Horvath JE, Moreira MAM, Kessing B, Pontius J, Roelke M, Rumpler Y, Schneider
MPC, Silva A, O’Brien S, Pecon-Slattery J. 2011. A molecular
phylogeny of living primates. PLoS Genetics 7(3):1–17.
Ramsier MA, Cunningham AJ, Moritz GL, Williams CV, Ong PS,
Dominy NJ. 2011. Auditory sensitivity of the Philippine tarsier,
Tarsius syrichta. Am. J. Phys. Anth. 144(S52):247–248.
Ravizza RJ, Heffner HE, Masterton B. 1969a. Hearing in primitive
mammals. 1. Opossum (Didelphis virginianus). J Aud Res 9:1–7.
Ravizza RJ, Heffner HE, Masterton B. 1969b. Hearing in primitive
mammals. 2. Hedgehog (Hemiechinus auritus). J Aud Res 9:8–11.
INNER EAR EVOLUTION IN PRIMATES
Ravizza RJ, Masterton B. 1972. Contribution of the neocortex to
sound localization in opossum (Didelphis virginiana). J Neurophysiol 35:344–356.
Rosowski JJ. 1992. Hearing in transitional mammals: Predictions
from the middle ear anatomy and hearing capabilities of extant
mammals. In: Webster DB, Fay RR, Popper AN, editors. The evolutionary biology of hearing. New York: Springer-Verlag. p 615–632.
Rosowski JJ, Graybeal A. 1991. What did Morganucodon hear. Zool
J Linn Soc 101:131–168.
Ross CF, Covert HH. 2000. The petrosal of Omomys carteri and the
evolution of the primate basicranium. J Hum Evol 39:225–251.
Ross CF, Williams BA, Kay RF. 1998. Phylogenetic analysis of
anthropoid relationships. J Hum Evol 35:221–306.
Ruf I, Luo Z, Wible JR, Martin T. 2009. Petrosal anatomy and inner
ear structures of the Late Jurassic Henkelotherium (Mammalia,
Cladotheria, Dryolestidae): insight into the early evolution of the
ear region in cladotherian mammals. J Anat 214:679–693.
Ryan A. 1976. Hearing sensitivity of the Mongolian gerbil, Meriones
unguiculatis. J Acoust Soc Am 59:1222–1226.
Seiffert ER, Perry JMG, Simons EL, Boyer DM. 2009. Convergent
evolution of anthropoid-like adaptations in Eocene adapiform primates. Nature 461:1118–1121.
Smith RJ, Jungers WL. 1997. Body mass in comparative primatology. J Hum Evol 32:523–559.
Szalay FS, Delson E. 1979. The evolutionary history of the primates. New York: Academic Press.
Vater M, Meng J, Fox RC. 2004. Hearing organ evolution and specialization: early and later mammals. In: Manley GA, Popper AN,
Fay RR, editors. Evolution of the vertebrate auditory system.
New York: Springer. p 256–288.
Webster DB, Webster M. 1972. Kangaroo rat auditory thresholds
before and after middle ear reduction. Brain Behav Evol 5:41–53.
Wenstrup JJ. 1984. Auditory sensitivity in the fish catching bat,
Noctilio leporinus. J Comp Physiol 155:91–101.
West CD. 1985. The relationship of the spiral turns of the cochlea
and the length of the basilar membrane to the range of audible
frequencies in ground dwelling mammals. J Acoust Soc Am 77:
Wible J, Rougier G, Novacek M, McKenna M. 2001. Earliest eutherian ear region: a petrosal referred to Prokennalestes from the
early cretaceous of Mongolia. Am Mus Nov 3322:1–44.
Wollack CH. 1965. Auditory thresholds in the raccoon (Procyon
lotor). J Aud Res 5:139–144.
APPENDIX: OVAL WINDOW AREA—STAPEDIAL FOOTPLATE AREA FOR EXTANT
OWA-SFA estimates based on Coleman et al. (2010)
unless indicated by asterisks. Taxa noted with one asterisk (*) indicate individual species values that were previously published as the mean for the genus, those with
two asterisks (**) indicate updated values based on additional specimens, and those with three asterisks (***)
indicate previously unpublished values.