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Stony Brook University SSStttooonnnyyy BBBrrrooooookkk UUUnnniiivvveeerrrsssiiitttyyy The official electronic file of this thesis or dissertation is maintained by the University Libraries on behalf of The Graduate School at Stony Brook University. ©©© AAAllllll RRRiiiggghhhtttsss RRReeessseeerrrvvveeeddd bbbyyy AAAuuuttthhhooorrr... The Functional Morphology and Evolution of the Primate Auditory System A Dissertation Presented by: Mark Newman Coleman to The Graduate School in Partial fulfillment of the Requirements for the Degree of Doctor of Philosophy in Anthropology Stony Brook University May 2007 Stony Brook University The Graduate School Mark Newman Coleman We, the dissertation committee for the above candidate for the Doctorate of Philosophy degree, hereby recommend acceptance of this dissertation. Dr. Callum F. Ross Associate Professor (Co-primary Advisor) Department of Organismal Biology and Anatomy, University of Chicago Dr. Brigitte Demes Professor (Defense Chairperson and Advisor) Department of Anatomy, Stony Brook University Dr. William Jungers Chairman and Professor (Co-primary Advisor) Department of Anatomy, Stony Brook University Dr. John J. Rosowski Professor (Outside Committee Member) Harvard Medical School This dissertation is accepted by the Graduate School Lawrence Martin Dean of the Graduate School ii Abstract of the Dissertation The Functional Morphology and Evolution of the Primate Auditory System By Mark Newman Coleman Doctor of Philosophy in Anthropology Stony Brook University 2007 Primates express numerous modifications on the fundamental mammalian ear morphology, and these differences have proven useful for phylogenetic classification at various taxonomic levels. However, the functional consequences related to diversity in primate auditory structure remain speculative and unproven. Although a considerable amount of research on the functional morphology of the ear has been done in other vertebrate groups, primates remain poorly studied. This dissertation sought to help fill this void by exploring the form-to-function relationships of the primate auditory system. To address this problem, numerous structures from the outer, middle, and inner ears were measured in a broad sample of primates with known hearing capabilities. The structures investigated included the size and shape of the pinna, the areas of the tympanic membrane and stapedial footplate, the masses and lever arm lengths of the ossicles, the volumes of the middle ear cavities, and the length of the cochlea. In total, over 1400 iii specimens representing more than 50 genera were assayed. The methods used to obtain these data included traditional morphometric measurement techniques, high-resolution computed-tomography (CT), digital photography, latex casting, and dissections of cadaveric specimens. By identifying specific form-to-function relationships it was possible to test current theories on auditory function, evaluate inter-specific differences in hearing performance, and predict the hearing sensitivity in extinct primate taxa. The results from these investigations demonstrate that a variety of auditory structures show significant correlations with particular aspects of hearing sensitivity. The majority of these relationships agrees with expectations from acoustic theory but some fundamental theories were not supported. For example, the idea that longer ossicular lever arms result in increased hearing sensitivity was rejected. By applying the functional relationships that are theoretically sound, hearing sensitivity was estimated in four fossil species representing pivotal nodes in primate evolution. These estimations suggest that primates have been steadily reinvading the “low-frequency niche” by progressive modification of various auditory structures. They also show that these adaptations were not present in our closest extinct relatives. The data provided by this dissertation present many opportunities for future research and will help shed light on the adaptive significance of differences in hearing performance. iv Table of Contents List of Figures vi List of Tables x Acknowledgments 1. Introduction 1 2. Previous Research on Auditory Morphology 8 Diversity in Auditory Anatomy in Primates and Other Mammals 8 Auditory Theory and Functional Morphology of the Ear 26 3. Previous Research on Auditory Sensitivity 53 Animal Psychophysics and Audiograms 55 Studies Producing Audiograms 60 Problems with Comparing Audiograms 184 Final Audiogram Datasets 205 4. Research Design 224 Theories Tested 225 Measurements Taken and Validation Experiments 226 Final Morphometric Variables 244 5. Defining the Appropriate Size Variable for Allometric Studies 248 Materials and Methods 250 Results 259 Discussion 270 Summary 276 6. Defining the Operational Analytical Unit: Ontogeny, Phylogeny, and Sexual Dimorphism in the Primate Auditory System 279 Materials and Methods 279 Results: Anthropoids 282 Results: Strepsirrhines 307 Discussion 312 7. Form-to-Function Relationships of the Ear 320 Morphometric-Audiometric Comparisons Using TIPS 325 Subgroup Comparisons 372 Morphometric-Audiometric Comparisons Using PICS 384 Discussion 406 Closing Remarks 417 8. Predicting Hearing Sensitivity in Fossils 421 The Fossils 421 Analysis and Results 425 Discussion 436 Concluding Remarks 444 References 446 Appendices 475 v List of Figures 1.1 Coronal section through human ear 1 1.2 Evolution of auditory features in primates and tree shrews 3 1.3 Adaptive triangle 4 2.1 Prominent features of the human outer ear 9 2.2 Primate outer ears 10 2.3 Basic structures of the malleus and incus 18 2.4 Internal view of a cochlea 23 2.5 Transformation of sound from free-field to eardrum 27 2.6 Middle ear pressure transfer ratio 37 2.7 Regression of ossicular mass against high-frequency limit 45 3.1 Perithreshold function for determining threshold value 58 3.2 Threshold extraction method 59 3.3 Audiogram from Elder (1934) 62 3.4 Audiograms from Wendt (1934) 64 3.5 Audiogram from Harris (1943) 68 3.6 Audiograms from Seiden (1957) 71 3.7 Audiogram from Clack and Herman (1963) 74 3.8 Audiograms from Semenoff and Young (1964) 76 3.9 Audiograms A from Fujita and Elliot (1965) 79 3.10 Audiograms B from Fujita and Elliot (1965) 81 3.11 Audiograms C from Fujita and Elliot (1965) 82 3.12 Audiograms D from Fujita and Elliot (1965) 84 3.13 Audiograms from Behar et al. (1965) 86 3.14 High-frequency limits from Farrer and Prim (1965) 88 3.15 Audiograms from Stebbins (1966) 92 3.16 Audiograms from Clack (1966) 94 3.17 Audiograms from Dalton (1968) 100 3.18 Audiograms from Dalton et al. (1969) 103 3.19 Audiograms from Bragg and Dreyer (1969) 105 3.20 Audiograms from Heffner et al. (1969) 108 3.21 Audiograms from Heffner and Masterson (1970) 111 3.22 Audiograms from Gourevitch (1970) 114 3.23 Audiograms from Mitchell et al. (1970) 117 3.24 Audiograms from Mitchell (1970) and Mitchell et al. (1971) 121 3.25 Audiograms from Gillette et al. (1971) 125 3.26 Audiograms from Green (1971, 1975) 129 3.27 Audiograms from Pugh et al. (1973) 132 3.28 Audiograms from Stebbins (1973) 135 3.29 Audiograms from Beecher (1974a, 1974b) 138 3.30 Audiograms A from Pfingst et al. (1975) 144 3.31 Audiograms B from Pfingst et al. (1975) 147 3.32 Audiograms from Pfingst et al. (1978) 149 3.33 Audiograms from Lonsbury-Martin and Martin 151 3.34 Audiograms from Heinz et al. (1982) 152 vi 3.35 Audiograms from Bennett et al. (1983) 156 3.36 Audiograms from Brown and Waser (1984) 158 3.37 Audiograms from Brown (1986) 161 3.38 Audiograms from Smith et al. (1987) 164 3.39 Audiograms from Owren et al. (1988) 168 3.40 Audiograms from Kojima (1990) 173 3.41 Audiograms from Smith and Olszyk (1997) 176 3.42 Audiograms from Jackson et al. (1999) 179 3.43 Audiograms from Lasky et al. (1999) 182 3.44 Human audiogram transducer comparison 193 3.45 Saimiri spp. transducer and conditioning procedure comparison 194 3.46 Macaca fascicularis transducer and conditioning procedure comparison 195 3.47 Macaca fuscata transducer and conditioning procedure comparison 196 3.48 Macaca mulatta transducer and conditioning procedure comparison 197 3.49 Eulemur fulvus audiograms 207 3.50 All Macaca mulatta audiograms 208 3.51 Macaca nemestrina audiograms (headphones) 210 3.52 Pan troglodytes audiograms 211 3.53 Saimiri spp.audiograms (speaker) 212 3.54 Audiogram measurement image 215 3.55 Relative audibility functions 218 3.56 Saimiri spp. and Macaca fascicularis audiograms 221 3.57 Cebus capucinus and Macaca mulatta audiograms 222 4.1 Measurements taken on outer ears 228 4.2 Tympanic ring measurement technique 229 4.3 Ossicular lever arm measurements 232 4.4 Microbalance used to weigh ossicular mass 233 4.5 CT slice showing HMH and visual threshold boundaries 240 4.6 CT image of cochlea showing measurements points 244 5.1 Geoskull 255 5.2 Scatterplot of skull size against # of non-significant results 260 5.3 Scatterplot of CV values against # of measurements taken 262 5.4 Scatterplot of r2 values against # of measurements taken 263 5.5 Boxplots of mandibular robusticity in platyrrhines 272 5.6 Scatterplot of CV values against measurement values 273 6.1 Boxplots of ontogenetic comparisons for Aotus azarae 282 6.2 Boxplots of ontogenetic comparisons for Aotus nancymae 283 6.3 Boxplots of ontogenetic comparisons for Aotus vociferans 284 6.4 Boxplots of ontogenetic comparisons for Saimiri boliviensis 287 6.5 Boxplots of ontogenetic comparisons for Saimiri sciureus 288 6.6 Boxplots of ontogenetic comparisons for Alouatta seniculus 290 6.7 Boxplots of ontogenetic comparisons for Alouatta
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