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ABSTRACT
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, 295:615631, 2012. V
INTRODUCTION
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 48 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.
V
616
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-
617
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 168 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 (125100 Ma) in Mongolia and has been attributed to Prokennalestes trofimovi (Wible et al., 2001).
Younger mammalian specimens from late Cretaceous
deposits in Canada (8477 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.
618
Houde skull
USNM 482353
USNM 309902
43098
DB047
1371
17415
17416
17417
17418
UM 87990
PLV14
AMNH131764
AMNH131762
Montpellier PRR
UCM57459
DPC10903
DPC10905
DPC92M236
FN91M269
Anjokibe Cave
DPC13776
Randriamanatina
DPC13751
DPC17306
MACN 14128
type specimen
KAN-CL-041
CGM 85785
CM 69728
Specimen
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Plesiadapiform
Adapoid
Adapoid
Adapoid
Omomyoid
Omomyoid
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Subfossil Lemur
Platyrrhine
Platyrrhine
Platyrrhine
Catarrhine
?
24.03
23.57
23.68
24.40
22.00
24.60
25.70
13.30
14.50
15.60
15.30
17.30
16.10
17.20
17.50
17.00
18.99
19.71
20.61
19.99
20.98
15.35
30.26
31.84
19.98
22.23
31.30
8.64
CL
2
2
3
2
2
2
2
2
2
2
2
2
2
2
2
2
3
2
2
2
1
1
2
1
2
3/8
1/8
3/8
3/8
1/4
1/4
3/8
3/8
3/8
1/4
5/8
1/2
1/8
3/4
1/4
5/8
7/8
7/8
1/4
7/8
1/8
2
2
1/8
3/4
3
7/8
3/8
1 1/2
CS
0.80
1.24
0.41
1.18
1.73
1.07
1.57
1.58
0.75
0.37
2.19
1.59
0.91
0.88
1.03
0.95
0.62
0.63
0.73
0.29
0.59
0.52
0.63
1/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/41/2
1/4
1
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
n/a
1
OWA
SBL
BM
100
303
288
652
652
2183
2183
2183
2183
2183
2059
1500*
2152
1009
1168*
220
19500*
19500*
15000
15000
60000*
60000*
11000*
49500*
49500*
1541
1500**
1860
3000
100
.042
.006
.040
.044
.040
.050
.050
.050
.050
.050
.053
.036
.040
.040
.037
.015
.040
.035
.040
.040
.035
.043
.035
.041
.003
.042
.042
.045
.056
.008
.046
.006
.049
.049
.049
.058
.058
.058
.058
.058
.060
.041
.046
.046
.042
.018
.069
.042
.069
.053
.042
.050
.053
.047
.052
.047
.047
.048
.064
.009
Voxel Dimensions
BM Ref.
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).
Carpolestes simpsoni
Ignacius graybullianus
Nannodectes intermedius
Pronothodectes gaoi
Pronothodectes gaoi
Plesiadapis tricuspidens
Plesiadapis tricuspidens
Plesiadapis tricuspidens
Plesiadapis tricuspidens
Plesiadapis tricuspidens
Plesiadapis cookei
Adapis sp.
Notharctus tenebrosus
Smilodectes gracilis
Microchoerus sp.
Omomys carteri
Archaeolemur sp.
Archaeolemur sp.
Babakotia radofilai
Babakotia radofilai
Megaladapis sp.
Megaladapis sp.
Mesopropithecus sp.
Palaeopropithecus sp.
Palaeopropithecus sp.
Dolichocebus gaimanensis
Tremacebus harringtoni
Homunculus patagonicus
Aegyptopithecus zeuxis
Shanghuang petrosal
Taxon
619
620
Group
CL
Platyrrhine
Platyrrhine
Platyrrhine
Platyrrhine
Catarrhine
Dermoptera
Catarrhine
Lemuroid
Lorisoid
Dermoptera
Lemuroid
Lorisoid
Catarrhine
Lorisoid
Lorisoid
Lorisoid
Scandentia
Platyrrhine
Platyrrhine
Platyrrhine
Tarsier
Tarsier
Tarsier
Tarsier
Scandentia
27.9
22.4
20.3
31.6
30.9
19.5
32.4
21.2
17.6
20.3
20.5
18.8
28.8
23.2
18.6
21.0
15.9
25.4
26.7
24.2
24.0
20.1
24.1
23.3
15.0
1
3
3
1
3
5
3
2
3
2
4
1
5
2
3
3
4
3
3
2
1
4
3
2
6
S.D.
1.50
0.31
0.20
2.49
1.72
0.21
0.09
0.85
0.91
CS
2
2
2
2
2
2
1.38
0.08
1.14
0.93
0.76
1.14
0.85
0.26
2
2
0.39
0.95
0.21
1.20
3
3
3
2
2
2 1/2
2 3/4 3
1/2 2 7/8
3
3 3 1/8
1/4 2 5/8
7/8 3 1/8
2 1/2
1/2 2 3/4
5/8 2 7/8
3/8 2 1/2
2 3/8
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
3 1/2
1/2 3 5/8
5/8 3 7/8
3/4 3 7/8
2 3/4 3
SBL
BM
n/a
n/a
n/a
n/a
n/a
1/2?
n/a
1/41/2
1/2
n/a?
1/4?
1/4?
n/a
1/4?
1/4?
1/4?
1
n/a
n/a
n/a
2
2
2
2
1
6087
775
372
3085
6030
1350
9450
2038
213
1100
2210
267
4475
1060
626*
833
51
811
721
492
123
125**
126
117
180
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 0.922, P < 0.001) between CL and
sound pressure level at 250 Hz (SPL@250 Hz) as
described by the formula:
y 2:433x 83:43
where x CL in millimeters and y SPL@250 Hz in
decibels (relative to 20 lPa). This research also detected
a significant, albeit weaker association (r2 0.579, P
0.011) between OWA and sound pressure level at 32 kHz
(SPL@32 kHz) described by the formula:
y 21:467x 0:297
where x OWA in millimeters2 and y SPL@32 kHz in
decibels. In this study we used SPL@250 Hz as a measure of low-frequency sensitivity and SPL@32 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).
621
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.
RESULTS
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. 3Alight gray line), there is a significant positive relationship between CL and body mass
(r2 0.388, P < 0.001). However, the amount of variation explained (coefficient of determination r2) is much
higher when extant haplorhines (r2 0.692, P < 0.001)
are considered separately from the other extant euarchontans (r2 0.742, P < 0.001). This is interpreted to
indicate that the relative length of the cochlea is divided
into two distinct groups (Fig. 3Adark 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 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 1/23 7/8),
which is most similar to the catarrhines among the taxa
in our study (catarrhines 2 7/83 1/8; platyrrhines 2
622
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).
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 ( 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
short
cochleae
compared
with
living
euarchontans and display values that consistently place
below the nonhaplorhine line (Fig. 3A). Plesiadapis
623
SPL@250 Hz
SPL@32 kHz
Carpolestes simpsoni
Ignacius graybullianus
Nannodectes intermedius
Plesiadapis cookei
Plesiadapis tricuspidens
Pronothodectes gaoi
Adapis sp.
Notharctus tenebrosus
Smilodectes gracilis
Microchoerus sp.
Omomys carteri
Archaeolemur sp.
Babakotia radofi
Megaladapis sp.
Mesopropithecus sp.
Palaeopropithecus sp.
Dolichocebus gaimanensis
Tremacebus harringtoni
Homunculus patagonicus
Aegyptopithecus zeuxis
Shanguang petrosal
62.4 (6 12.6)
6.5
13.0
11.5
22.4
15.8
13.8
20.7
(6
(6
(6
(6
(6
(6
(6
14.0)
12.6)
12.8)
13.4)
3.8)
12.6)
13.0)
16.4
8.2
40.9
19.8
34.2
(6
(6
(6
(6
(6
12.5)
13.5)
18.1)
12.9)
13.6)
48.1
37.2
42.0
45.8
35.5
33.3
34.8
32.4
46.1
7.9
32.1
7.3
25.0
25.9
24.1
29.9
23.6
20.9
51.1
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
(6
10.0)
9.0)
4.2)
5.1)
8.9)
8.8)
8.9)
8.8)
9.8)
7.6)
2.9)
11.4)
9.1)
3.4)
9.1)
8.9)
9.1)
9.4)
10.5)
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)
624
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).
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 SPL@32 kHz and high-frequency
cutoff in living euarchontans with known hearing
sensitivity
Taxon
Aotus sp.
Galago senegalensis
Lemur catta
Macaca fuscata
Nycticebus coucang
Papio cynocephalus
Perodicticus potto
Phaner furcifer
Saimiri sp.
Tupaia glis
SPL@32 kHz
Hi-Cut
14
7
14
39
23
24
16
8
14.3
6.6
45
65
58
34
44
41
41
60
44
60
DISCUSSION
To further investigate evolutionary trends in OWA,
CL and development of the secondary bony lamina, we
625
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
626
Fig. 6. Continued.
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
627
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
628
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 3020
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 1/82 3/8 turns
and ranged in length from 14.515.6 mm. The slightly
younger Plesiadapis tricuspidens and Plesiadapis cookei
(late Paleocene-early Eocene) had essentially the same
number of spirals (2 1/42 3/8) but slightly longer cochleae (17.019.0 mm). The three early-late Eocene
adapoids we investigated show a slight increase in cochlear turns (2 1/42 5/8) and CL (19.720.6) compared
with Plesiadapis spp. The omomyid, Omomys carteri
from the middle Eocene displays 2 3/4 spirals but a rela-
Broader Implications
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 (9045 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.
low-frequency
sensitivity,
somewhat
intermediate
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.
ACKNOWLEDGEMENT
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 dHistoire 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
629
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.
LITERATURE CITED
Aitkin LM, Johnston BM. 1972. Middle-ear function in a monotreme-echidna (Tachyglossus aculeatus). J Exp Zool 180:245250.
Armstrong SD, Bloch JI, Houde P, Silcox MT. 2011. Cochlear labyrinth volume in euarchontoglirans: implications for the evolution
of hearing in primates. Anat Rec 294:263266.
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 446:507512.
Bloch JI, Gingerich P. 1998. Carpolestes simpsoni, a new species
(Mammalia, Proprimates) from the late Paleocene of the Clarks
Fork Basin, Wyoming. Contributions from the Museum of Paleontology: The University of Michigan. Vol. 30: p 131162.
Bloch JI, Silcox MT, Boyer DM, Sargis EJ. 2007. New Paleocene
skeletons and the relationship of plesiadapiforms to crown-clade
primates. PNAS USA 104:11591164.
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 161:2950.
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 30:5591.
Coleman MN, Colbert MW. 2007. Technical note: CT thresholding
protocols for taking measurements on three-dimensional models.
Am J Phys Anth 133:723725.
Coleman MN, Colbert MW. 2010. Correlations between auditory
structures and hearing sensitivity in non-human primates.
J Morph 271:511532.
Coleman MN, Kay RF, Colbert MW. 2010. Auditory morphology and
hearing sensitivity in fossil New World monkeys. Anat Rec 293:
17111721.
Dalland J. 1965. Hearing sensitivity in bats. Science 150:11851186.
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. 308359.
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. 134171.
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 55:301313.
Fleagle JG. 1999. Primate adaptation and evolution. San Diego:
Academic Press.
Fleischer G. 1973. Studien am Skelett des Geh
ororgans der
S
augetiere, einschliesslich des Menschen Mitt 21:131239.
Fleischer G. 1976. Hearing in extinct cetaceans as determined by
cochlear structure. J Paleontol 50:133152.
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 187:265269.
630
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 121:249291.
Frost SB, Masterton RB. 1994. Hearing in primitive mammals:
Monodelphis domestica and Marmosa elegans. Hear Res 76:6772.
Gilbert CC. 2005. Dietary ecospace and the diversity of euprimates during the early and middle eocene. Am J Phys Anthro. 126:237249.
Godfrey LR, Jungers WL. 2003. Subfossil lemurs. In: Goodman SM,
Benstead JP, editors. The natural history of Madagascar. Chicago:
University of Chicago Press. p 12471252.
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 111184.
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:
15841599.
Heffner HE, Heffner RS. 1985a. Hearing in two cricetid rodents:
Wood rat (Neotoma floridana and grasshopper mouse (Onychomys
leucogaster). J Comp Psychol 99:275288.
Heffner HE, Heffner RS, Contos C, Ott T. 1994a. Audiogram of the
hooded Norway rat. Hear Res 73:244247.
Heffner RS, Heffner HH, Masterton B. 1971. Behavioral measurements of absolute and frequency difference thresholds in guinea
pig. J Acoust Soc Am 49:18881895.
Heffner RS, Heffner HE. 1982. Hearing in the elephant (Elephas
maximus) - Absolute sensitivity, frequency discrimination, and
sound localization. J Comp Physiol Psychol 96:926944.
Heffner RS, Heffner HE. 1983. Hearing in large mammals - horse
(Equus caballus) and cattle (Bos taurus). Behav Neurosci 97:299309.
Heffner RS, Heffner HE. 1985b. Hearing range in the domestic cat.
Hear Res 19:8588.
Heffner RS, Heffner HE. 1985c. Hearing in mammals: the least
weasel. J Mamm 66:745755.
Heffner RS, Heffner HE. 1990a. Hearing in domestic pigs (Sus
scrofa) and goats (Capra hircus). Hear. Res. 48:231240.
Heffner RS, Heffner HE. 1990b. Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear Res 46:239252.
Heffner RS, Heffner HE. 1991. Behavioral hearing range of the
chinchilla. Hear Res 52:1316.
Heffner RS, Heffner HE. 1992. Hearing and sound localization in
blind mole rats, Spalax ehrenbergi. Hear Res 62:206216.
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 331:418433.
Heffner RS, Heffner HE. 2010. Explaining high frequency hearing.
Anat Rec 293:20802082.
Heffner RS, Heffner HE, Contos C, Kearns D. 1994b. Hearing in
prairie dogs: transition between surface and subterranian
rodents. Hear Res 73:185189.
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 157:138152.
Heffner RS, Koay G, Heffner HE. 2003. Hearing in American leafnosed bats. III: Artibeus jamaicensis. Hear Res 184:113122.
Hemil
a S, Nummela S, Reuter T. 1995. What middle ear parameters tell about impedance matching and high frequency hearing.
Hear Res 85:3144.
Jackson LL, Heffner HE, Heffner RS. 1997. Audiogram of the fox
squirrel (Sciurus niger). J Comp Psychol 111:100104.
Jackson LL, Heffner RS, Heffner HE. 1999. Free-field audiogram of the
Japanese macaque (Macaca fuscata). J Acoust Soc Am 106:30173023.
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 54:323382.
Kelly JB, Kavanagh GL, Dalton JCH. 1986. Haring in the ferret
(Mustela putorius) - thresholds for pure tone detection. Hear Res
24:269275.
631
OWA-SFA
S.D.
1.47
1.51
1.54
0.75
0.7
0.82
0.71
0.69
8
3
11
18
1
6
4
1
0.13
0.05
0.17
0.07
0.09
0.05
Species
Arctocebus calabarensis**
Ateles paniscus*
Avahi laniger**
Brachyteles arachnoides
Cacajao calvus*
Cacajao melanocephalus*
Callicebus donacophilus*
Callicebus hoffmansi*
Callicebus personatis*
Callicebus torquatus*
Callimico goeldii
Callithrix jacchus
Cebuella pygmaea
Cebus albifrons*
Cebus apella*
Cebus capucinus*
Cercopithecus mitis*
Cercopithecus neglectus*
Chiropotes albinasus***
Chiropotes satanus
Chlorocebus aethiops
Chlorocebus pygerythrus***
Colobus guereza***
Cynocephalus volans***
Daubentonia madagascariensis
Erythrocebus patas
Eulemur fulvus*
Eulemur rufus*
Galago senegalensis
Galeopterus variegatus***
Hylobates muelleri***
Indri indri
Lagothrix lagotricha
Lemur catta
Leontopithecus rosalia
Lepilemur mustelinus
Lophocebus albigena
Loris tardigratus
Macaca fascicularis
Macaca mulatta***
Miopithecus talapoin***
Nycticebus bengalensis*
Nycticebus javanicus*
Pan troglodytes***
Perodicticus potto
Phaner furcifer
Pithecia monochus*
Pithecia pithecia*
Propithecus diadema*
Propithecus verreauxi*
Ptilocercus lowii***
Saguinus fuscicollis*
Saguinus mystax*
Saguinus oedipus*
Saimiri boliviensis*
Saimiri scuireus*
Tarsius bancanus***
Tarsius pelengensis***
Tarsius spectrum***
Tarsius syrichta***
Trachypithecus cristatus***
Tupaia glis
Varecia variegata
OWA-SFA
S.D.
0.7
1.63
0.69
1.43
1.06
1.07
0.87
0.82
0.89
1
0.59
0.55
0.42
1.02
1.07
1.07
1.25
1.36
0.96
0.96
1.17
1.08
1.04
1.03
1.32
1.37
0.67
0.67
0.55
0.84
1.2
1.05
1.59
0.77
0.64
0.72
1.38
0.59
1.11
1.14
0.83
0.64
0.53
3.01
0.74
0.54
1.04
0.97
1.07
0.89
0.33
0.4
0.44
0.56
0.6
0.64
0.46
0.26
0.47
0.6
1.13
0.26
1.04
3
11
3
1
2
1
4
1
1
2
3
5
2
10
14
4
3
3
1
5
2
1
1
4
2
3
1
1
9
2
1
2
3
13
6
5
1
2
7
1
1
2
3
2
12
1
3
5
1
1
4
1
1
1
15
4
2
4
2
2
2
6
1
0.15
0.20
0.06
0.04
0.15
0.05
0.09
0.04
0.05
0.13
0.14
0.14
0.03
0.21
0.12
0.01
0.20
0.17
0.12
0.05
0.01
0.18
0.21
0.10
0.07
0.15
0.05
0.13
0.01
0.03
0.00
0.05
0.16
0.08
0.03
0.06
0.03
0.00
0.04
0.05
0.04
0.13
0.07