coleman and boyer 2012

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Inner Ear Evolution in Primates

Through the Cenozoic: Implications forthe Evolution of HearingMARK N. COLEMAN1* ANDDOUG M. BOYER2

1Department of Anatomy, Midwestern University, Glendale, Arizona 853082Department of Anthropology and Archaeology, Brooklyn College, Brooklyn,

New York 11210

ABSTRACTMammals are unique in being the only group of amniotes that can

hear sounds in the upper frequency range (>

12 kHz), yet details aboutthe evolutionary development of hearing patterns remain poorly under-stood. In this study, we used high resolution X-ray computed tomographyto investigate several functionally relevant auditory structures of theinner ear in a sample of 21 fossil primate species (60 Ma to recent times)and 25 species of living euarchontans (primates, tree shrews, and flyinglemurs). The structures examined include the length of the cochlea, devel-opment of bony spiral lamina and area of the oval window (or stapedialfootplate when present). Using these measurements we predicted aspectsof low-frequency and high-frequency sensitivity and show that hearingpatterns in primates likely evolved in several stages through the firsthalf of the Cenozoic. These results provide temporal boundaries for thedevelopment of hearing patterns in extant lineages and strongly suggestthat the ancestral euarchontan hearing pattern was characterized bygood high-frequency hearing but relatively poor low-frequency sensitivity.They also show that haplorhines are unique among primates (extant orextinct) in having relatively longer cochleae and increased low-frequencysensitivity. We combined these results with additional, older paleontologi-cal evidence to put these findings in a broader evolutionary context. AnatRec, 295:615631, 2012. VC 2012 Wiley Periodicals, Inc.

Key words: primate hearing; hearing evolution; low-frequencyhearing; high-frequency hearing; cochlea; ovalwindow; stapedial footplate; secondary bonylamina

INTRODUCTION

One of the most unique features of auditory percep-tion in mammals is the ability to hear sounds above 12kHz (Fay, 1988). Snakes and turtles are relatively insen-sitive to airborne sounds and can rarely hear soundsabove 2 kHz (Fig. 1). Lizards and crocodilians showslightly better sensitivity but are still limited to frequen-cies below 48 kHz. Most birds can hear sounds up toaround 10 kHz although some predatory birds such asbarn owls can hear sounds as high as 12 kHz (Konishi,1973). In contrast, most mammals have an upper fre-quency limit of hearing that ranges from 30 to 60 kHzand some bats and aquatic mammals are able to detectacoustic signals above 100 kHz (Fig. 1). Humans (upper

limit 18 kHz), elephants (Elephas maximusupperlimit 11 kHz), and naked mole rats (Hetercephalus

glaberupper limit 12 kHz) present a few exceptions

Grant sponsor: National Science Foundation, Evolving EarthFoundation, American Society of Mammalogists, MidwesternUniversity, Stony Brook University; Grant numbers: NSF BCS-0408035, NSF BCS-0622544, NSF BCS-0100825.

*Correspondence to: Mark N. Coleman, Department ofAnatomy, Midwestern University, 19555 N. 59th Ave., Glendale,AZ 85308, USA. E-mail: [email protected]

Received 20 September 2011; Accepted 2 December 2011.

DOI 10.1002/ar.22422Published online 27 January 2012 in Wiley Online Library(wileyonlinelibrary.com).

THE ANATOMICAL RECORD 295:615631 (2012)

VVC 2012 WILEY PERIODICALS, INC.


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to the general mammalian pattern of good high-frequency hearing (Heffner and Heffner, 1982, 1993;Jackson et al., 1999).

Although it has been argued that the development ofa three-bone ossicular system and coiling (and elonga-tion) of the cochlea were key adaptations that led togood high-frequency sensitivity (Masterson et al., 1969;Manley, 1972; Fleischer, 1978; Echteler et al., 1994;Frost and Masterton, 1994; Fox and Meng, 1997), deter-mining 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 thatprimitive mammals shifted to a primarily high-frequency condition soon after acquiring the three-boneossicular system (Jurassic) and then gradually (re)devel-oped good low-frequency sensitivity starting in theCretaceous and extending through the early part of theCenozoic (Masterson et al., 1969; Jerison, 1973; Frostand Masterton, 1994).

Comparative studies in living mammals have gener-ally supported this hypothesis by showing thatprimitive mammals like opossums and hedgehogs arecharacterized by good high-frequency hearing and rela-

tively poor low-frequency sensitivity (Ravizza et al.,1969a, b; Frost and Masterton, 1994). These animalsalso have what is generally considered to be ancestralcharacteristics in ear morphology such as the micro-type middle ear bone configuration, which seemsparticularly well adapted for transmitting high-frequency sounds (Fleischer, 1978; Rosowski, 1992). Inrecent years, it has become increasingly possible to usefossils to investigate evolutionary hearing patterns,although there are still a few temporal gaps, which have

prevented a comprehensive evaluation of proposed evolu-tionary sequences.The incipient development of the three-bone ossicu-

lar system during the Late Triassic (roughly 200 Ma),such as witnessed in fossil mammaliaformes like

Morganucodon, may have resulted in a slight shift to-ward higher frequencies although these gains wereprobably modest since these animals had relativelylarge ossicles and short, uncoiled cochleae (Kermackand Mussett, 1983; Rosowski and Graybeal, 1991;Rosowski, 1992). Comparative studies have shown thathigh-frequency limits are correlated with ossicularmass (Hemila et al., 1995; Coleman and Colbert, 2010),

Fig. 1. Hearing sensitivity for various groups of terrestrial verte-brates. Nonmammalian vertebrates show reduced hearing sensitivity,

particularly at frequencies above 10 kHz compared with most mam-

mals that have heightened overall sensitivity and can hear sounds in

the high-frequency range (>12 kHz). Number in parentheses repre-

sents number of species used to derive group averages. Mean audio-

grams 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 Master-

ton, 1994). Ungulate audiogram based on average values for Bos Tau-

rus, 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 audio-

gram 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 Artibeusjamaicensis (Heffner et al., 2003), Carollia perspicillata (Koay et al.,

2003), Eptesicus fuscus (Koay et al., 1997), Megaderma lyra (Neu-

weiler, 1984), Myotis lucifugas (Dalland, 1965), Noctilio leporinus

(Wenstrup, 1984), Phyllostomus hastatus (Koay et al., 2002), Rhinolo-phus ferrumequinum (Long and Schnitzler, 1975), Rousettus aegyptia-

cus (Koay et al., 1998). Low-frequency rodent audiogram based on

species with a low-frequency cutoff below 500 Hz and a high-

frequency 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). Primateaudiogram data and techniques used to extract and interpolate data

from the literature described in Coleman (2009).

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so the relatively large ossicles in Morganucodon likelyplaced inertial limitations on how quickly the ear bonescould vibrate, limiting high-frequency transmissionthrough the middle ear.

The hearing range in early mammals such as multitu-berculates (late Jurassic late Eocene) was probably not

that much different from that of living monotremes. Mul-tituberculates such as Lambdopsalis share numeroussimilarities to monotremes in middle ear structure suchas the orientation of the ectotympanic bone, the positionof the malleus relative to the incus and the simple mor-phology of the incus (Meng and Wyss, 1995). Mechanicalanalyses of ear function in echidnas (Tachyglossusaculeatus) suggest that their middle ear bones arerelatively inefficient at transmitting sounds, particularat higher frequencies (Aitkin and Johnston, 1972). Inaddition, multituberculates were similar to extant monot-remes in having a relatively short cochlea that curveslaterally but does not complete one full turn (Fox andMeng, 1997). Auditory brainstem response estimates ofhearing in echidnas (Tachyglossus aculeatus) suggestthat these prototherians, and possibly multituberulatesas well, had a relatively limited hearing range from 1.6to 13.9 kHz (Mills and Shepherd, 2001).

During the middle to late Jurassic, the ancestors ofcrown therians (marsupials and placentals) began develop-ing inner ear structures that likely signal the onset ofheightened high-frequency hearing. The cladotherianmammals Henkelotherium guimarotae andDryolestes leir-iensis from late Jurassic deposits in Portugal (156150 Ma)had relatively short cochleae (2.73.3 mm) that completedabout 3/4 of one full turn (270) (Ruf et al., 2009; Luoet al., 2011), similar to multituberculates and monotremes.However, unlike multituberculates and monotremes, Hene-

klotherium and Dryolestes demonstrate evidence fordevelopment of primary and secondary bony laminae alongthe basal end of the cochlear canal (Ruf et al., 2009; Luo

et al., 2011). Possessing both primary and secondary bonylaminae generally reduces the width of the basilar mem-brane and also allows this membrane to be more tense(stiff) along the basal end, both of which help promote thereception of high-frequencies (Fleischer, 1976). Althoughsome animals can hear relatively high frequencies withoutthe presence of a secondary lamina, it is considered a basicanatomical requirement for the specialized high-frequencyhearing of bats and cetaceans (Bruns, 1980; Ketten, 1992;

Vater et al., 2004).Although the bony laminae in Heneklotherium and Dry-

olestes suggest they may have had nascent adaptations forrelatively good high-frequency hearing, additional auditorycharacteristics indicate that the overall range and sensitiv-ity of hearing was probably limited in comparison with

extant therians. For one, the presence of a Meckeliangroove in Heneklotherium and Dryolestes suggest thatthese taxa had a transitional mammalian middle earthat was not as efficient as the definitive mammalianmiddle ear at transmitting airborne sounds (Meng et al.,2011). In addition, their relatively short cochleae likelyplaced limitations on the range of perceptible frequenciesbecause there may not have been adequate space on thebasilar membrane to have auditory sensory neurons (haircells) devoted to both high- and low-frequency sensitivity.

Complete coiling of the cochlear canal may have beenone strategy for increasing basilar membrane length ina compact space. The hearing in the first mammals that

had short but coiled cochleae was presumably like mar-supials such as opossums (Fig. 1), which have coiled butrelatively short basilar membranes [e.g., 6.4 mm, Mono-delphis domestica(Muller et al., 1993)]. The limitedlow-frequency hearing in living opossums is not strictlyrelated to small body size since even the medium-sized

Didelphis virginiana (4 kg) can hear sounds only downto about 1 kHz [overall range 168 kHz(Ravizzaet al., 1969a)]. Furthermore, primitive extant placentalmammals such as hedgehogs (Hemiechinus auritus) alsohave limited low-frequency sensitivity (500 Hz to>60 kHz) and a presumably relatively short cochlea asimplied by the fact that their cochleae have only 1 1/2spiral turns (Lewis et al., 1985).

The oldest known mammal that demonstrates at leastone full coil of the cochlea comes from early Cretaceousdeposits (125100 Ma) in Mongolia and has been attrib-uted to Prokennalestes trofimovi (Wible et al., 2001).

Younger mammalian specimens from late Cretaceousdeposits in Canada (8477 Ma) had cochlear canals withapproximately 1 1/4 turns (Meng and Fox, 1995a) andeven younger specimens from the Bug Creek Anthillslocality in Montana (65 Ma) demonstrate cochleae with1 1/2 turns (Meng and Fox, 1995b). The estimated hearingfor the placental specimens from the Bug Creek Anthillslocality ranged from 1.23 to 87.7 kHz and that of a marsu-pial from the same site had a range from 1.58 to 73.8 kHz(Meng and Fox, 1995b). This evidence suggests that ther-ian mammals living around the time of the K-T boundarywere characterized by heightened high-frequency hearingbut relatively poor low-frequency sensitivity.

During the Cenozoic, therians apparently continuedthese trends in auditory evolution and developed essen-tially modern morphologies (and presumably hearingpatterns) by the Miocene. Fleischer (1976) compared theear structures in extinct and living cetaceans and con-cluded that the specialized hearing of odontocetes

related to echolocation evolved during the Oligocene andwas essentially similar to modern patterns by the Mio-cene. More recently, Coleman et al. (2010) examined themiddle and inner ears of Miocene aged fossil New Worldmonkeys and predicted that these 20 my old primateshad low- (and possibly high-) frequency sensitivity simi-lar to living monkeys from South America. However,there is still a paucity of studies that have focused onreconstructing hearing patterns from the early Cenozoic,a period that figures prominently in arguments like theMasterson hypothesis (Masterson et al., 1969).

The primate fossil record offers an opportunity to beginto address this problem due to the abundance of specimensthat span the Cenozoic era. In this study, we examined rel-evant auditory structures in 21 species of extinct primates

and closely related taxa that range in geologic age from 60Ma until near-modern times. We then compared thesespecimens with a sample of extant euarchontans (Fig. 2)and used predictive equations to estimate the low- andhigh-frequency sensitivity of the fossils.

MATERIALS AND METHODS

Fossil Sample

The fossil specimens examined in this study are givenin Table 1. The actual fossils themselves were not ana-lyzed. Instead, high resolution X-ray computedtomography (HRXCT) was used to construct digital

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models of auditory structures (see below) that are oftenpreserved in fossils and that have been found to be func-tionally relevant. The fossil specimens were scanned atvarious institutions and the voxel dimensions for eachspecimen are given in Table 1. The geologically oldestassemblage of fossils belong to the group referred to asplesiadapiformes, which are now thought to be stem pri-mates with a sister-group relationship to Euprimates

(Bloch et al., 2007). Our sample consisted of six speciesof small to medium-sized plesiadapiforms from North

America and Europe that range in age from 60 t o 54 Ma.The next group consisted of three medium-sized fossilprimates from North America and Europe called ada-poids that range in age from 50 to 35 Ma. We alsoexamined two similarly aged (4535 Ma) small tomedium-sized species of omomyoids from North Amer-ica and Europe. Our sample included one 45 Ma primatespecimen from China that has been suggested to repre-sent a basal anthropoid (MacPhee et al., 1995). Inaddition, we sampled four species of medium-sizedunambiguous 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 depos-its in Madagascar (late Pleistocene-Holocene).

Extant Comparative Sample

The main comparative sample analyzed in this study(Table 2) consisted of a phylogenetically diverse group of25 species (72 specimens total) of living euarchontans.This sample included seven species of platyrrhines (NewWorld monkeys), three species of catarrhines (Old Worldmonkeys) and four species of Tarsiers, which are collec-tively referred to as haplorhines ( anthropoids tarsiers). In addition, we sampled five species of lorisoidsand two species of lemuroids that belong to the primatesuborder termed strepsirhines. We also examined four

species of nonprimate euarchontans: two species of scan-dentians (treeshrews) and two species of dermopterans(flying lemurs).

As with the fossil specimens, HRXCT was used to cre-ate digital models of relevant auditory structures. Mostextant specimens were scanned at the University of

Texas High-Resolution X-ray CT facility (Table 2). Thesescans had voxel dimensions measuring 62.5 lm 62.5 lm 68.0 lm and the final images were 16 bitTIFF files. However, a subset of the extant specimenswas scanned at higher resolutions. These included onespecimen of Tarsius syrichta and two specimens of

Tarsius tarsier(15.0 lm 15.0 lm 15.0 lm), one spec-imen ofCynocephalus volans (15.0 lm 15.0 lm 15.0lm), and four specimens of Ptilocercus lowii (24.0 lm 24.0 lm 26.0 lm). Besides the extant specimens thatwere analyzed using computed tomography, additionaldata on oval window area (or stapedial footplate area)for 71 primate species were taken from publishedreports (Coleman et al., 2010) augmented with previ-ously unpublished data for several species (Appendix 1).

Measuring Auditory Structures

Cochlear length (CL) in fossil and living specimenswas estimated by creating digital endocasts of the innerear using HRXCT and measuring the outer circumfer-ence of the cochlear canal. Image stacks were importedinto ImageJ 1.35f (NIH) where threshold values weredetermined using the half-maximum height protocoldescribed in Coleman and Colbert (2007). The imagestacks were then loaded into 3D Slicer 2.6 open sourcesoftware, where all measurements were taken on threedimensional digital models. The measurements weretaken by placing markers (fiducials) at the smallest pos-sible intervals along the outer circumference of thedigital cochlear endocast, starting at the distal edge ofthe round window and continuing until the approximatelocation of the helicotrema. The distance between adja-cent fiducial points was then measured and all distancessummed to derive the total length estimate.

The number of cochlear spirals (CS) was counted byplacing a transparent radial grid (divided into one

eighths) over two dimensional images of the cochlearendocasts in apical view. The measurement was startedfrom the distal edge of the round window similar to previ-ous studies (West, 1985). The digital cochlear endocastswere also used to evaluate the potential presence of sec-ondary bony laminae that support the outer edge of thebasilar membrane (all specimens observed appeared tohave primary bony laminae). It should be noted thatbecause secondary bony laminae are relatively thin andfragile structures, it may be possible to not detect theirpresence (in specimens that possess them) if the voxeldimensions are too large or if the specimen is damaged.However, we detected secondary bony laminae in somespecimens 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 distinguishits presence when adequately developed. The final struc-ture measured using HRXCT was oval window area(OWA). This structure was estimated by measuring themajor and minor axes (length and width) of the oval win-dow (or stapedial footplate if the stapes was preserved).These measurements were then used to calculate the areausing the formula for an ellipse.

Predicting Hearing Sensitivity

The predictive equations used to estimate certain pa-rameters of hearing sensitivity in the fossil specimens

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.

Technically, the correct designation for the infraorder consistingof New World monkeys Old World monkeys Apes may be Sim-iiformes (Groves, 2005), but in this article we use the traditionaldesignation of Anthropoidea to avoid confusion with the recent lit-erature involving this group.



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were based on previous research on the functional mor-phology of the auditory system in living euarchontanswith known hearing abilities (Coleman, 2007; Colemanand Colbert, 2010). This research found a significant

relationship (r2 0.922, P < 0.001) between CL andsound pressure level at 250 Hz (SPL@250 Hz) asdescribed by the formula:

y 2:433x 83:43

where x CL in millimeters and y SPL@250 Hz indecibels (relative to 20 lPa). This research also detecteda 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

wherex OWA in millimeters2 and y SPL@32 kHz indecibels. In this study we used SPL@250 Hz as a mea-sure of low-frequency sensitivity and SPL@32 kHz as ameasure of high-frequency sensitivity and predictedthese variables in fossil taxa using the formulae pre-sented above.

In addition to predicting low- and high-frequency sen-sitivity in individual fossils, CL and OWA werereconstructed for ancestral nodes and these values werethen used to predict low- and high-frequency sensitivityat the basal stems leading to haplorhines, strepsirrhines,and all primates. Ancestral state reconstructions were

performed with Mesquite (1.12) modular system for evo-lutionary analysis (Maddison and Maddison, 2006), basedon a squared-change parsimony model. Using a relativelywell-resolved phylogeny and character values for terminal

taxa (species), evolutionary programs such as Mesquiteuse algorithms to reconstruct values at internal nodes ofa phylogenetic tree (i.e., essentially weighted mean val-ues). Incorporating temporal information (branch lengthdata) and fossil taxa can greatly increase the confidencein ancestral reconstructions, particularly toward the baseof a phylogenetic tree (Finarelli and Flynn, 2006).

Phylogenetic Relationships andDivergence Dates

The data used to construct the phylogenetic relation-ships and divergence dates for living euarchontans wasbased primarily on Perelman et al. (2011) that usedboth molecular evidence and fossil calibration points.

In addition, the split within scandentia (Tupaia fromPtilocercus) was based on Bininda-Emonds et al. (2007).The position of fossil New World monkeys (Dolichocebus,Tremacebus, Homunculus) as stem platyrrhines is basedon analyses presented in Kay et al. (2008) and the desig-nation ofAegyptopithecus as a stem catarrhine is fromFleagle (1999). The divergence times and relationshipsof the subfossil lemurs is based on Godfrey and Jungers(2003) and Orlando et al. (2008). The designation of omo-myoids as stem haplorhines and adapoids as stemstrepsirrhines is based on traditional as well as recentphylogenetic analyses (Szalay and Delson, 1979; Martin,1990; Ross et al., 1998; Fleagle, 1999; Seiffert et al.,

TABLE 2. CL estimates for extant taxa examined in this study

Genus Group CL N S.D. CS SBL BM

Alouatta seniculus Platyrrhine 27.9 1 2 1/2 n/a 6087Aotus trivirgatus Platyrrhine 22.4 3 1.50 2 3/4 3 n/a 775Callithrix jachhus Platyrrhine 20.3 3 0.31 2 1/2 2 7/8 n/a 372Cebus apella Platyrrhine 31.6 1 3 n/a 3085

Cercopithecus mitis Catarrhine 30.9 3 0.20 3 3 1/8 n/a 6030Cynocephalus volans Dermoptera 19.5 5 2.49 2 1/4 2 5/8 1/2? 1350

Erythrocebus patas Catarrhine 32.4 3 1.72 2 7/8 3 1/8 n/a 9450Eulemur fulvus Lemuroid 21.2 2 0.21 2 1/2 1/41/2 2038Galago senegalensis Lorisoid 17.6 3 0.09 2 1/2 2 3/4 1/2 213Galeopterus variegatus Dermoptera 20.3 2 0.85 2 5/8 2 7/8 n/a? 1100

Lemur catta Lemuroid 20.5 4 0.91 2 3/8 2 1/2 1/4? 2210Loris tardigradus Lorisoid 18.8 1 2 3/8 1/4? 267Macaca fascicularis Catarrhine 28.8 5 1.38 2 7/8 3 1/8 n/a 4475Nycticebus bengalensis Lorisoid 23.2 2 0.08 2 3/8 2 1/2 1/4? 1060Nycticebus javanicus Lorisoid 18.6 3 1.14 2 2 3/8 1/4? 626*Perodicticus potto Lorisoid 21.0 3 0.93 2 1/4 2 1/2 1/4? 833Ptilocercus lowii Scandentia 15.9 4 0.76 2 7/8 3 1/8 1 51Saimiri boliviensis Platyrrhine 25.4 3 1.14 2 7/8 3 n/a 811Saimiri scuireus Platyrrhine 26.7 3 0.85 2 7/8 3 n/a 721Saguinus geoffroyi Platyrrhine 24.2 2 0.26 2 7/8 3 n/a 492Tarsius bancanus Tarsier 24.0 1 3 1/2 2 123

Tarsius pelengensis Tarsier 20.1 4 0.39 3 1/2 3 5/8 2 125**Tarsius syrichta Tarsier 24.1 3 0.95 3 5/8 3 7/8 2 126Tarsius tarsier Tarsier 23.3 2 0.21 3 3/4 3 7/8 2 117Tupaia glis Scandentia 15.0 6 1.20 2 3/4 3 1 180

CL units are in millimeters, N represents number of specimens examined and S.D. represents one standard deviation. CS andSBL 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 onmean values for T. bancanus and T. syrichta which have similarly sized skulls as T. pelengensis (unpublished data).



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2009). The intragroup relationships and position of ple-siadapiforms as sister taxa to Euprimates is based onBloch et al. (2007). The taxonomic affinity of the Shang-huang petrosal has been argued to resemble either abasal anthropoid (MacPhee et al., 1995) or possibly anomomyoid (Ross and Covert, 2000). Both phylogenticinterpretations are investigated here.

RESULTS

The first results to discuss relate to the associationbetween CL and body mass in living and recent (i.e.,

subfossil lemurs) taxa. Considering all of the taxonomicgroups together (Fig. 3Alight gray line), there is a sig-nificant positive relationship between CL and body mass(r2 0.388, P < 0.001). However, the amount of varia-tion explained (coefficient of determination r2) is muchhigher when extant haplorhines (r2 0.692, P < 0.001)are considered separately from the other extant euarch-ontans (r2 0.742, P < 0.001). This is interpreted toindicate that the relative length of the cochlea is dividedinto two distinct groups (Fig. 3Adark black lines):Extant haplorhines have the relatively longest cochleaewhile nonhaplorhine taxa generally have relativelyshorter cochleae. There is also a significant positive rela-tionship between body mass and OWA in extant andrecent taxa (r2 0.825, P < 0.001). However, in this

comparison haplorhines do not appear to be distinctfrom the other euarchontan taxa and are scattered alongboth sides of the best fit regression line (Fig. 3B).

Although the phylogenetic relationship of tarsiersremains debatable (Perelman et al., 2011), this studyreveals that they share certain similarities in cochlearstructure with living anthropoids. For example, tarsiershave remarkably long cochleae for their body size (20.124.1 mm) and three of the four species investigated fallabove the haplorhine regression line (Fig. 3A). They alsodemonstrate a high number of spiral turns (3 1/23 7/8),which is most similar to the catarrhines among the taxain our study (catarrhines 2 7/83 1/8; platyrrhines 2

1/23; strepsirrhines 22 3/4; dermopterans 2 1/427/8; scandentians 2 3/4 3 1/8). In fact, tarsiers havemore spiral turns than almost any other mammal thathas been examined with the exception of a few animalslike guinea pigs that display an average of 4 1/4 turns(West, 1985). Tarsiers also exhibit a well developed sec-ondary bony lamina that extends along the radial wallof the cochlear canal for approximately two full spiralturns (Fig. 4). In contrast, secondary bony laminae werenot 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 rel-atively shorter cochleae compared with tarsiers andanthropoids (Fig. 3A). Also unlike anthropoids, some ofthe strepsirrhines appear to display some indication of asecondary bony lamina. The lamina is most highlyexpressed in Galago senegalensis which shows a depres-sion on the outer surface of the cochlear endocastswhich extends for approximately 1/2 turn (Fig. 4). A sec-ondary spiral (bony) lamina was also identified ingalagos in a previous study by Fleischer (1973). Eulemur

fulvus also shows indications of a secondary bony lam-ina, although not as distinct as in galagos and it appearsto stretch for only 1/4 1/2 turns. Lemur, Nycticebus,

Perodicticus, and Loris could also have short secondarylaminae (1/4 turn) but the current evidence from the

cochlear endocasts does not allow for a conclusive deter-mination. Higher resolution CT scans are needed tobetter evaluate the extent of development of this struc-ture in these and other strepsirrhine taxa.

The recently extinct subfossil lemurs show a similarpattern in CL to their smaller bodied living relatives,although there is more scatter around the nonhaplorhineline. Despite their large body mass, most subfossil lemurcochleae are no longer than New World monkeys like

Aotusand Saimiri that are well over an order of magni-tude smaller in body mass (Table 2). Archaeolemur sp.presents the main exception to this pattern [often calledthe monkey-lemur because of its post-cranial and

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

haplorhine line (r2 0.692, P


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dental similarities to Old World monkeys (Fleagle,1999)], and had an estimated relative CL more similarto living haplorhines (Fig. 3A). Subfossil lemurs display1 7/82 5/8 spiral turns of the cochlea and none of thespecimens examined here demonstrated indications of asecondary bony lamina. Considering OWA, most subfos-sil lemurs show relatively small values based on bodymass estimates for these species (Fig. 3B). In fact, Mega-ladapis sp. and Palaeopropithecus sp. had areas that

were approximately half the size of chimpanzees (Pantroglodytes), which are roughly equivalent in overallmass. As with CL, Archaeolemur is unusual comparedwith the other subfossil lemurs and shows a mean valuefor OWA that falls just above the regression line (Fig.3A).

Common treeshrews (Tupaia glis) have the absolutely(15.0 mm) and relatively shortest cochleae of any extantspecies examined (Fig. 3A). Pen-tailed treeshrews (Ptilo-cercus lowii) actually have slightly longer cochleae andare somewhat more coiled than common tree-shrews de-spite being over three times smaller in body mass. Thesetwo species of treeshrews also have among the smallest

values for OWA (Fig. 3B). Tupaia glis displays indica-tions of a secondary bony lamina that is reminiscent ofgalagos although it appears to proceed for nearly onefull turn. The secondary lamina is quite evident on thecochlear endocasts for Ptilocercus lowii and clearlyextends for at least one full turn (Fig. 4). Both genera ofdermopterans (Cynocephalus and Galeopterus) have CLvalues 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, butis not plainly visible on the endocasts of Galeopterusvariegatus. A previous analysis found that Cynocephalusvariegatus ( Galeopterus variegatus) had a weaklydeveloped ridge along the radial wall of the cochlearcanal but that it was structurally different from the sec-ondary lamina of animals like tupaia and galagos andmore similar to the condition (spiral ligament) inhumans (Fleischer, 1973).

Plesiadapiformes, the geologically oldest taxa, had rel-atively short cochleae compared with livingeuarchontans and display values that consistently placebelow the nonhaplorhine line (Fig. 3A). Plesiadapis

Fig. 4. CT cochlear endocast models for representative living

euarchontans (anthropoid, tarsier, strepsirrhine and treeshrew) and

fossil primates (plesiadapiform, adapoid, omomyoid, and the Shang-

huang petrosal). All models scaled to approximately the same size.

Note the high number of spiral turns and development of the second-

ary bony lamina (black arrows) in Tarsius. Also, note the lack of any

evidence of a secondary lamina in squirrel monkeys (Saimiri).



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cookei had the longest cochlea of any plesiadapiformexamined but still was relatively shorter than anyextant species except common treeshrews. Carpolestessimpsoni, 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 closeto the best fit regression line although Carpolestes wasrelatively smaller than most other taxa (Fig. 3B). Carpo-lestes also had a clearly developed secondary bonylamina that extended for at least 1/2 turn (Fig. 4). All ofthe remaining plesiadapiformes also appear to have hada secondary lamina although generally not apparentlyas developed as in Carpolestes (i.e., shallower depressionin the endocasts and extending only 1/41/2 turns).

In contrast to plesiadapiformes, the geologicallyyounger adapoids (5035 Ma) all demonstrate CL valuesthat are very close to the nonhaplorhine regression line,similar to most living strepsirrhines. However, theadapoids we examined were similar to most plesiadapi-formes in seemingly possessing a secondary bony laminathat was about 1/41/2 turns long (e.g., Adapis - Fig. 4).The roughly coeval omomyoids illustrate a mixed pat-tern with one species showing similarities to adapoidswhile the other species resembles plesiadapiformes insome 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 thatextended for nearly one full turn (Fig. 4). The largerbodied and geologically younger Microchoerus (35 Ma),on the other hand, produced a CL value that fell slightlyabove the nonhaplorhine line and had a less developed(although still visible) secondary lamina that wasapproximately 1/4 turn long.

The 45 Ma Shanghuang petrosal, a possible basalanthropoid, had a short cochlea with relative values simi-

lar to most plesiadapiformes (Fig. 3A). In fact, theShanghuang petrosal had the second shortest cochlea ofany taxon in our sample (13.3 mm). The cochlear endocastfor this specimen also clearly revealed a secondary bonylamina that goes at least one full spiral turn (Fig. 4). Incontrast, the 3020 Ma unambiguous fossil anthropoidsshow the longest cochleae of any extinct group examined.Three of these specimens fall just below the haplorhineline, while Tremacebus harringtoni actually falls slightlycloser to the nonhaplorhine line (Fig. 3A). However, a pre-vious analysis of Tremacebus suggested that thisspecimen may be distorted, reducing its apparent length(Coleman et al., 2010). Regardless, none of these speci-mens displayed indications of a secondary bony lamina.

Using the values for CL and OWA, we estimated meas-

ures of low-frequency sensitivity (SPL@250 Hz) and high-frequency sensitivity (SPL@32 kHz) for each of the fossilspecimens using the predictive equations presented above(Table 3). These values are illustrated in Figure 5 alongwith the same audiometric parameters for extant anthro-poids and strepsirrhines as well as two primitive livingplacental mammals, treeshrews and hedgehogs.

Carpolestes simpsoni and the Shanghuang petrosal areboth predicted to have had relatively poor low-frequencysensitivity that was outside the range of living primatesbut intermediate between the values for treeshrews andhedgehogs. Nannodectes, Omomys, and Pronothodecteswere also apparently less sensitive to low-frequency

sounds with predicted values of SPL@250 Hz betweenthe values for treeshrews and the upper limits for livingstrepsirrhines. On the other side of the auditory spec-trum, all of these taxa (in addition to Ignacius) appearto have had good high-frequency sensitivity, based onpredictions from OWA, that was above the range of anyof the living anthropoids that have had their hearingtested. In fact, the predicted values of SPL@32 kHz for

Carpolestes, Shanghuang and Omomys were all below 10dB SPL. In living primates, there is a significant correla-tion between SPL@32 kHz and high-frequency cutoff (r 0.833, P 0.003), and the few euarchontans thathave SPL@32 kHz values below 10 dB SPL also have ahigh-frequency cutoff of 60 kHz or higher (Table 4).

Whats more, all of these taxa apparently had rela-tively well developed secondary lamina that extendedbetween 1/2 and one full spiral turn. The expression ofthis feature also suggests that these taxa were welladapted to hear high-frequencies based on the observa-tion that Galago senegalensis and Tupaia glis showsimilar development of the secondary lamina (1/2 andone full turn, respectively) and have among the bestknown high-frequency sensitivity of any extant euarch-

ontan. The relationship between secondary laminaedevelopment and good high-frequency sensitivity in pri-mates is further supported by the recent finding thatTarsius syrichta has a high-frequency cutoff of75 kHz(Ramsier et al., 2011), which is the highest of any pri-mate tested, and also demonstrates the greatestdevelopment of secondary laminae among the primatesin our sample (~two full turns Fig. 4).

Low-frequency sensitivity in Plesiadapis tricuspidens,P. cookei, Microchoerus, and the three adapoids we inves-tigated appear to have been somewhat better than thefossil taxa described above. The predicted values ofSPL@250 Hz are below those for treeshrews and are

TABLE 3. Predicted hearing sensitivity in fossils

Taxon SPL@250 Hz SPL@32 kHz

Carpolestes simpsoni 62.4 (6 12.6) 6.5 (6 14.0)Ignacius graybullianus 13.0 (6 12.6)Nannodectes intermedius 48.1 (6 10.0) 11.5 (6 12.8)Plesiadapis cookei 37.2 (6 9.0) 22.4 (6 13.4)

Plesiadapis tricuspidens 42.0 (6 4.2) 15.8 (6 3.8)Pronothodectes gaoi 45.8 (6 5.1) 13.8 (6 12.6)Adapissp. 35.5 (6 8.9) 20.7 (6 13.0)Notharctus tenebrosus 33.3 (6 8.8)Smilodectes gracilis 34.8 (6 8.9)

Microchoerussp. 32.4 (6 8.8) 16.4 (6 12.5)Omomys carteri 46.1 (6 9.8) 8.2 (6 13.5)

Archaeolemursp. 7.9 (6 7.6) 40.9 (6 18.1)Babakotia radofi 32.1 (6 2.9) 19.8 (6 12.9)Megaladapissp. 7.3 (6 11.4) 34.2 (6 13.6)Mesopropithecussp. 25.0 (6 9.1)Palaeopropithecussp. 25.9 (6 3.4) 31.6 (6 11.9)Dolichocebus gaimanensis 24.1 (6 9.1) 23.2 (6 13.6)Tremacebus harringtoni 29.9 (6 8.9)

Homunculus patagonicus 23.6 (6 9.1) 17.5 (6 12.6)Aegyptopithecus zeuxis 20.9 (6 9.4) 26.8 (6 14.8)Shanguang petrosal 51.1 (6 10.5) 9.1 (6 13.3)

Low-frequency (SPL@250 Hz) and high-frequency (SPL@32kHz) sensitivity predictions and 95% confidence intervals(6) for all extinct taxa investigated in this study. SPL@250Hz predicted using CL values and SPL@32 kHz predictedusing oval window area based on analyses in Coleman andColbert (2010).



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similar to the middle and lower values displayed by livingstrepsirrhines but also overlap the upper values forextant anthropoids. In other words, the estimated valuesare toward the middle of the distribution of values in liv-ing forms (Fig. 5). Conversely, the predicted SPL@32 kHzfor these taxa suggests reduced high-frequency sensitivitycompared with the first group of fossils described and inthis case overlaps the range of values for living anthro-poids. P. tricuspidens and Microchoerus produced values

that are found in all three comparative groups of livingtaxa, whereas the values for P. cookei and Adapis werehigher than those for treeshrews (indicating less sensitiv-ity) but still within the ranges of extant strepsirrhinesand anthropoids. These predicted values of SPL@32 kHzplus the apparent presence of moderately developed sec-ondary laminae in the fossils (1/41/2 turns) suggests anupper frequency limit (high-frequency cutoff) between4158 kHz based on modern analogues (Table 4).

The four species of fossil anthropoids we examined allproduced predicted values of SPL@250 Hz that are simi-lar to those found in living anthropoids but below therange of strepsirrhines, treeshrews or hedgehogs (Fig.5). In contrast, the estimated high-frequency sensitivityfor this group was less uniform. The predicted value of

SPL@32 kHz for Aegyptopithecus falls exclusively withinthe range for extant anthropoids. In contrast, the valuefor Dolichocebus also overlaps the range of values forstrepsirrhines and the value for Homunculus overlapsthe ranges of all three comparative groups. However,considering the finding that secondary bony laminaewere not detected in any of these fossils (or in livinganthropoids) and the fact that the predicted values wereall encompassed by the range of living anthropoids, sug-gests a high-frequency cutoff between 34 and 45 kHz forthis group of fossils.

It should be noted that the predictive equation used toestimate high-frequency sensitivity (based on OWA) has

a higher margin of error than the equation used to pre-dict low-frequency sensitivity (based on CL). However,these two traits may in fact be interrelated to somedegreee. Although Coleman and Colbert (2010) did notfind a significant relationship between high-frequencysensitivity and CL, studies from other researchers haveidentified such a relationship. Echteler et al. (1994) foundthat the high-frequency cutoff in mammals goes up asbasilar membrane length decreases and Kirk and Gosse-

lin-Ildari (2009) found that smaller cochlear volumes arealso related to increased high-frequency sensitivity.Therefore, the general pattern identified here that theprimates with smaller (shorter) cochleae also had smallerOWAs strengthens the interpretations for changes inhigh-frequency hearing based on oval window area alone.

TABLE 4. Values for SPL@32 kHz and high-frequencycutoff in living euarchontans with known hearing

sensitivity

Taxon SPL@32 kHz Hi-Cut

Aotussp. 14 45Galago senegalensis 7 65

Lemur catta 14 58Macaca fuscata 39 34

Nycticebus coucang 23 44Papio cynocephalus 24 41Perodicticus potto 16 41Phaner furcifer 8 60Saimirisp. 14.3 44Tupaia glis 6.6 60

Sound pressure level at 32 kHz (SPL@32 kHz) in decibelsand high-frequency cutoff (Hi-Cut) in kilohertz. There is asignificant correlation between SPL@32 kHz and high-frequency cutoff in these euarchontan taxa (r 0.833,

P 0.003). Note that taxa with a value of less than 10 dBfor SPL@32 kHz also have a high-frequency cutoff of60 kHz or higher.

Fig. 5. Predicted low-frequency and high-frequency sensitivity for

fossil specimens. Sound pressure level at 250 Hz (SPL@250 Hz) was

used as a proxy for low-frequency sensitivity and sound pressure level

at 32 kHz (SPL@32 kHz) was used as a proxy for high-frequency sen-

sitivity. Predicted values for the fossils are compared with the range of

values for living primates, treeshrews and hedgehogs (gray rectan-

gles). Extant primate and treeshrew audiometric data based on Cole-

man (2009) and augmented with data for Callithrix jacchus (common

marmosets) from Osmanski and Wang (2011). Audiometric data for

hedgehogs from Ravizza et al. (1969b).



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DISCUSSION

To further investigate evolutionary trends in OWA,CL and development of the secondary bony lamina, we

mapped the values for these characters onto a phyloge-netic tree and reconstructed the values for keytransitional points along the tree not represented by fos-sils (Fig. 6). One major challenge when constructing a

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

changes in body mass whereas variation in CL (Fig. 6B) shows grade

shifts whereby older fossil groups demonstrate relatively shorter coch-

leae. Asterisks along stems indicate development of the secondary

bony lamina for that clade unless otherwise noted. 1 (*) absent; 2(**) poorly developed; 3 (***) moderate to highly developed.



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phylogenetic tree of primates that includes the fossils inour sample relates to the phylogenetic position of theShanghuang petrosal. As briefly described in the Materi-als and Methods Section, various authors havesuggested that the Shanghuang petrosal could be eithera basal anthropoid (MacPhee et al., 1995) or a memberof the Omomyiformes (Ross and Covert, 2000). Asrevealed by our study, the cochlear endocast of the

Shanghuang petrosal is superficially similar to the coch-lea 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 3/4vs. 2 3/8), and both appear to have a secondary bony lam-ina that extended for about one turn. In addition, bothspecimens have similar values for OWA (0.37 mm2 vs.0.41 mm2). However, they do appear to differ somewhat

Fig. 6. Continued.



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in the apical height of the cochlear spiral (Fig. 4). Regard-less of phylogenetic affinity, the Shanghuang petrosallikely had hearing capabilities that were very similar tothat of Omomys based on the predictions in sensitivitypresented here. Since the taxonomic identity of theShanghuang petrosal remains uncertain, we will tenta-tively consider it to belong to an Omomyiform althoughwe will also discuss the implications in the case that itactually came from a basal anthropoid.

Evolutionary changes in OWA, and presumably high-frequency sensitivity, seem to be largely related to over-all increases in body size (Fig. 3B, Fig. 6A). Small

mammals (with small heads) need heightened high-frequency sensitivity to take advantage of spectral cuesthat aid in the ability to localize the source of a sound(Heffner and Heffner, 2010). However, as animals getlarger, there is likely reduced selection to maintainheightened high-frequency sensitivity for localization pur-poses. Therefore, if OWA is one of the proximatemechanisms governing high-frequency sensitivity, then itmakes 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 insome groups may also reflect this trend toward largerbody size in mammals. This may explain why the largebodied subfossil lemurs appear to be devoid of secondarylaminae while at least some of the relatively smaller liv-

ing strepsirrhines (e.g., Galago, Eulemur) apparentlypossess such structures. However, the absence or pres-ence of the secondary laminae is not strictly tied to bodysize since small-bodied monkeys like tamarins and mar-mosets apparently lack them while similarly-sizedprimates like galagos and lorises possess them (Fig. 6B).It also does not appear that the development of second-ary laminae is directly related to either CL or thenumber of cochlear spirals since tarsiers show the great-est expression of laminae development, yet have a highnumber 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 developmentof a secondary bony lamina (Fig. 6B) supports the notionthat the presence of this structure is the ancestral condi-tion for the cladotherian clade (Ruf et al., 2009).

When examining changes in CL, some interestingphylogenetic and temporal patterns become evident (Fig.6B). Note that only the geologically youngest fossilsshow CL values that approach those found in livingforms. Although increases in body size through timehave no doubt resulted in overall increases in CL,changes in body size alone cannot explain these pat-terns. For example, Plesiadapis cookei, the

plesiadapiform with the longest cochlea (19.0 mm) andamong the largest in body mass (2,059 g) in our sam-ple, still possessed a cochlea that was shorter than amodern 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 omomyoidOmomys had a relatively shorter cochlea than the geologi-cally younger omomyoid Microchoerus (Fig. 3A).Furthermore, if the Shanghuang petrosal is that of a basalanthropoid (or basal haplorhine for that matter), then thereis a large difference in relative CL between this 45 Maspecimen compared with the 3020 Ma fossil anthropoidswe investigated from Africa and South America.

The reconstructed values at the branch leading to allprimates (1 Fig. 6) for OWA was 0.66 mm2 and that for

CL was 17.9 mm. These values suggest that basal pri-mates had low-frequency sensitivity that wasintermediate between the mean values for extant strep-sirrhines and treeshrews and high-frequency sensitivitysimilar to living strepsirrhines (Fig. 7). Considering theShanghuang petrosal to belong to a stem anthropoidonly moderately influences these reconstructed values(0.63 mm2 and 17.5 mm) and consequently does not sig-nificantly alter this interpretation. The reconstructedvalues at the branch leading to strepsirrhines (2 Fig.6) was 0.77 mm2 for OWA and 19.6 mm for CL. Thesevalues suggest slightly less high-frequency sensitivitybut slightly better low-frequency hearing than found in

Fig. 7. Low-frequency sensitivity (SPL@250 Hz) and high-frequency

sensitivity (SPL@32 kHz) predictions for basal primates (1), basalstrepsirrhines (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 andMasterton, 1994), and echidnas (Mills and Shepherd, 2001).



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living strepsirrhines (Fig. 7). Again, evaluating this pat-tern with Shanghuang as a basal anthropoid had littleeffect on the reconstructed values (0.74 mm2 and 19.3mm). The reconstructed values at the branch leading tohaplorrhines (3 Fig. 6) were 0.69 mm2 and 18.7 mmsuggesting both high- and low-frequency sensitivity that

was very similar to the mean for the extant strepsir-rhines for which hearing sensitivity has been tested(Fig. 7). As before, there are only minor changes ifShanghuang is positioned as a basal anthropoid (0.64mm2 and 18.1 mm).

In contrast to the minimal influence of the Shang-huang petrosal on the reconstructed values at thebranches labeled 1, 2, 3 discussed above, its phylogeneticposition does significantly alter the interpretations asso-ciated with the branch leading to anthropoids (4 Fig. 6). If the Shanghuang petrosal was that of an Omo-myiform, then the reconstructed values at the branchlabeled 4 were 1.12 mm2 and 24.4 mm for OWA and CL,respectively. This suggests that the relatively long coch-leae characteristic of anthropoids and tarsiers is ashared derived trait with an origin that likely stretchesback 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 havebeen 0.70 mm2 and 18.2 mm, similar to the inferred val-ues for basal haplorrhines. This scenario implies thatthe relatively long cochleae of tarsiers developed inde-pendently to that of anthropoids. Regardless of whenanthropoids and tarsiers began to develop their rela-tively long cochleae, it appears that their early ancestors(basal haplorhines) were characterized by reduced low-frequency and increased high-frequency sensitivity com-pared with modern and more recent species. The earliestfossil evidence for hearing sensitivity that is on par withthat of living haplorrhines does not appear until 3020Ma as witnessed in definitive fossil anthropoids like

Aegyptopithecusand Dolichocebus (Fig. 5).The pattern of increased cochlear coiling and elonga-

tion documented in Cretaceous mammals (seeintroduction) is continued in the geologically younger fos-sil primates examined in this study. Comparable with theBug Creek Anthills specimens, Carpolestes simpsoni fromthe late Paleocene had about 1 1/2 spiral turns, similar toliving hedgehogs that also display 1 1/2 turns of the coch-lea. The predicted low-frequency sensitivity for C.simpsoni (also similar to the known low-frequency sensi-tivity of hedgehogs) implies that this animal likely couldnot have perceived sounds much below 250 Hz (based onthe traditional low-frequency cutoff of 60 dB). A recentstudy of cochlear volume in this specimen also suggeststhat C. simpsoni had a hearing range that was shifted to-

ward higher frequencies (Armstrong et al., 2011).The similarly aged Pronothodectes gaoi (middle-latePaleocene) and Nannodectes intermedius (late Paleo-cene) had cochleae that spiraled for 2 1/82 3/8 turnsand ranged in length from 14.515.6 mm. The slightlyyounger Plesiadapis tricuspidens and Plesiadapis cookei(late Paleocene-early Eocene) had essentially the samenumber of spirals (2 1/42 3/8) but slightly longer coch-leae (17.019.0 mm). The three early-late Eoceneadapoids we investigated show a slight increase in coch-lear turns (2 1/42 5/8) and CL (19.720.6) comparedwith Plesiadapis spp. The omomyid, Omomys carterifrom the middle Eocene displays 2 3/4 spirals but a rela-

tively short length of 15.4 mm compared with the lateEocene-early Oligocene Microchoerus sp. that exhibits acochlea with 3 1/8 turns and a length of 21 mm. Finally,the fossil anthropoids in our sample show cochlearcharacteristics that are within the range of extantanthropoids (Table 2). Aegyptopithecus zeuxis (early Oli-

gocene) had 2 7/8 turns (25.7 mm) and fossilplatyrrhines (early Miocene) had 2 3/43 1/8 turns (2224.5 mm) (Coleman et al., 2010).

Broader Implications

Our results provide paleontological evidence that ba-sal primates (late Cretaceous) had good high-frequencysensitivity but relatively poor low-frequency sensitivitycompared with modern members of the order. Then, theybegan to develop good low-frequency sensitivity withslight decreases in high-frequency sensitivity startingduring the late Paleocene-early Eocene. Finally, essen-tially modern patterns had evolved by the Oligocene(30 Ma), although slight modifications to the entireauditory apparatus appear to have continued through theearly part of the Miocene (Coleman et al., 2010).

These findings, in combination with other studies ongeologically older mammals, are in accordance with thehypothesis articulated by Masterson et al. (1969) thatmammals went through a period of reduced low-frequency sensitivity during the evolution of modernhearing patterns, although the timing of events are dif-ferent than originally proposed. This purported sequenceof changes in hearing sensitivity has considerable impli-cations for the evolution of vocal communication,predator-prey interactions and the development of hear-ing specializations in mammals. For example, thetransition to a primarily high-frequency hearing patternwas likely paralleled by a shift to higher vocalization fre-quencies making it improbable that early primates (and

possibly mammals as well) used low-frequency, long-range communication signals like those that are utilizedby many species of primates today. This also raises thepossibility that at least some early primate (and mam-malian) vocalizations were above the upper limit ofhearing of contemporaneous nonmammalian predators(i.e., dinosaurs), resulting in opportunities to exploit newbehavioral and ecological niches and potentially alteringpredator-prey dynamics. Furthermore, the ancestralhearing phase of good high-frequency and poor low-frequency sensitivity (9045 Ma) in primates may betypical of other mammalian orders and would have beena critical first step toward developing the unique hearingpatterns like those of echolocating bats. In fact, low-fre-quency sensitivity in many bats is very similar to that

in opossums (Fig. 1) suggesting that the specializedhearing of bats may not be that far removed from thepattern that characterized mammals during the reducedlow-frequency sensitivity phase.

SUMMARY AND FUTURE DIRECTIONS

Plesiadapiformes, the earliest fossil primates forwhich we have evidence were characterized by havingsmall oval window areas and relatively short cochleathat housed moderate to well-developed secondary bonylaminae. These traits are interpreted to suggest thatthese taxa had good high-frequency but relatively poor



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low-frequency sensitivity, somewhat intermediatebetween extant strepsirrhines and primitive living mam-mals like treeshrews and hedgehogs. Then, with theorigin of haplorrhines and strepsirrhines (Euprimates), pri-mates began to develop relatively longer cochleae andreduced expression of secondary bony laminae indicating

an increase in low-frequency sensitivity and modest reduc-tions in high-frequency sensitivity. This strepsirrhinestage of hearing dates back to at least the Eocene (50Ma) based on fossil taxa like adapoids but could date wellback into the late Cretaceous based on molecular evidence.

Finally, sometime after the origin of Euprimates, hap-lorrhines continued the pattern of cochlear elongationand reduction (or loss) of secondary bony laminae(except in tarsiers). The African and South Americanfossil evidence suggest that this process was completedby the early Miocene, but the origin of this stage ofprimate hearing remains unresolved. Early fossil haplor-rhines like Omomys and the Shanghuang petrosalsuggest that haplorrhines and strepsirrhines (andpossibly anthropoids and tarsiers as well) may have devel-oped cochlear elongation independently, relative to the

basal primate condition. Among living haplorrhines, onlytarsiers have developed relatively long cochleae whilestill retaining well developed secondary bony laminaeadaptations that apparently confer both heightened high-and low- frequency sensitivity to this unique genus.

Paleontological evidence and comparative studies onauditory function promise to continue refining ourunderstanding of hearing evolution. Investigating moreprimate specimens from the Eocene and Oligocene willshed more light on the evolution of the hearing patternsin primates and help put these findings in a larger theo-retical framework. In particular, analyzing the auditoryregion of (definitive) basal anthropoids could help usunderstand the development of the unique traits of thisgroup of primates (to which humans belong). It willalso be interesting to begin examining other orders ofmammals (e.g., rodents, carnivores) from the earlyCenozoic to see if similar patterns of auditory evolutionhave occurred. Ultimately, this type of informationcontributes to a more complete understanding of theenvironmental processes that have resulted in thebehavioral and ecological diversity seen among primates,mammals, and other vertebrate groups.

ACKNOWLEDGEMENT

We thank the following individuals and institutions foraccess 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) Ada-

pis, P. tricuspidens; R. F. Kay (Duke U.) Dolichocebus,Homunculus, Tremacebus; E.R. Seiffert (Stony Brook U.) Aegyptopithecus; E.L. Simons (Duke U.) Aegyptopi-thecus, Archaeolemur, Babakotia, Megaladapis, Mesopro-

pithecus, Palaeopropithecus; A. Walker (PennsylvaniaState U.) Notharctus and Smilodectes (used with per-mission of the Division of Paleontology, AMNH), Adapis,

P. tricuspidens; K.C. Beard (Carnegie) Shanghuang pe-trosal. 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. Gor-dan, T. Ryan, A. Walker, E. Westwig. We would also like toacknowledge B. Demes, J. Georgi, A. Grossman, C. Heesy,W. Jungers, J. Rosowski, and C. Ross for helpful discus-sions and comments about the analysis and early versionsof the manuscript. Lastly, we thank two anonymous

reviewers for useful comments on the manuscript.

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APPENDIX: OVAL WINDOW AREASTAPE-DIAL FOOTPLATE AREA FOR EXTANT

EUARCHONTANS

OWA-SFA estimates based on Coleman et al. (2010)unless indicated by asterisks. Taxa noted with one aster-isk (*) indicate individual species values that were previ-ously published as the mean for the genus, those withtwo asterisks (**) indicate updated values based on addi-tional specimens, and those with three asterisks (***)indicate previously unpublished values.

Species OWA-SFA N S.D.

Alouatta caraya* 1.47 8 0.13Alouatta pigra* 1.51 3 0.05Alouatta seniculus* 1.54 11 0.17Aotus azarae* 0.75 18 0.07Aotus lemurinus* 0.7 1Aotus nancymae* 0.82 6 0.09Aotus trivirgatus* 0.71 4 0.05Aotus vociferans* 0.69 1

Species OWA-SFA N S.D.

Arctocebus calabarensis** 0.7 3 0.15Ateles paniscus* 1.63 11 0.20Avahi laniger** 0.69 3 0.06Brachyteles arachnoides 1.43 1Cacajao calvus* 1.06 2 0.04

Cacajao melanocephalus* 1.07 1Callicebus donacophilus* 0.87 4 0.15Callicebus hoffmansi* 0.82 1Callicebus personatis* 0.89 1Callicebus torquatus* 1 2 0.05Callimico goeldii 0.59 3 0.09Callithrix jacchus 0.55 5 0.04Cebuella pygmaea 0.42 2 0.05Cebus albifrons* 1.02 10 0.13Cebus apella* 1.07 14 0.14Cebus capucinus* 1.07 4 0.14Cercopithecus mitis* 1.25 3 0.03Cercopithecus neglectus* 1.36 3 0.21Chiropotes albinasus*** 0.96 1Chiropotes satanus 0.96 5 0.12Chlorocebus aethiops 1.17 2 0.01Chlorocebus pygerythrus*** 1.08 1

Colobus guereza*** 1.04 1Cynocephalus volans*** 1.03 4 0.20

Daubentonia madagascariensis 1.32 2 0.17Erythrocebus patas 1.37 3 0.12Eulemur fulvus* 0.67 1Eulemur rufus* 0.67 1Galago senegalensis 0.55 9 0.05Galeopterus variegatus*** 0.84 2 0.01

Hylobates muelleri*** 1.2 1Indri indri 1.05 2 0.18Lagothrix lagotricha 1.59 3 0.21Lemur catta 0.77 13 0.10Leontopithecus rosalia 0.64 6 0.07Lepilemur mustelinus 0.72 5 0.15Lophocebus albigena 1.38 1Loris tardigratus 0.59 2 0.05Macaca fascicularis 1.11 7 0.13

Macaca mulatta*** 1.14 1Miopithecus talapoin*** 0.83 1Nycticebus bengalensis* 0.64 2 0.01Nycticebus javanicus* 0.53 3 0.03Pan troglodytes*** 3.01 2 0.00Perodicticus potto 0.74 12 0.05Phaner furcifer 0.54 1Pithecia monochus* 1.04 3 0.16Pithecia pithecia* 0.97 5 0.08Propithecus diadema* 1.07 1Propithecus verreauxi* 0.89 1Ptilocercus lowii*** 0.33 4 0.03Saguinus fuscicollis* 0.4 1Saguinus mystax* 0.44 1Saguinus oedipus* 0.56 1Saimiri boliviensis* 0.6 15 0.06Saimiri scuireus* 0.64 4 0.03

Tarsius bancanus*** 0.46 2 0.00Tarsius pelengensis*** 0.26 4 0.04Tarsius spectrum*** 0.47 2 0.05Tarsius syrichta*** 0.6 2 0.04Trachypithecus cristatus*** 1.13 2 0.13Tupaia glis 0.26 6 0.07Varecia variegata 1.04 1


coleman and boyer 2012

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