Unexpected Convergent Evolution of Nasal Domes Between Pleistocene Bovids and Cretaceous Hadrosaur Dinosaurs

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Unexpected Convergent Evolution of Nasal Domes between Pleistocene Bovids and Cretaceous Hadrosaur Dinosaurs

Highlights Authors d Pleistocene Rusingoryx atopocranion are first known Haley D. O’Brien, J. Tyler Faith, Kirsten mammals with hollow nasal crests E. Jenkins, ..., Gilbert Price, Yue-xing Feng, Christian A. Tryon d Rusingoryx ontogeny and evolution are broadly similar to lambeosaurine hadrosaurs Correspondence [email protected] (H.D.O.), d The best-supported nasal crest function is phonic [email protected] (J.T.F.) modification d Combination of convergent ontogeny, evolution, and function In Brief may explain crest rarity O’Brien et al. analyze first known mammalian osseous nasal crests from a new Rusingoryx assemblage. Analogous to those of lambeosaurine hadrosaurs, these crests may facilitate vocalization. This morphology is an outstanding example of convergent evolution between dinosaurs and bovids, driven by ontogenetic, evolutionary, and environmental pressures.

Unexpected Convergent Evolution of Nasal Domes between Pleistocene Bovids and Cretaceous Hadrosaur Dinosaurs

Haley D. O’Brien,1,* J. Tyler Faith,2,* Kirsten E. Jenkins,3 Daniel J. Peppe,4 Thomas W. Plummer,5 Zenobia L. Jacobs,6 Bo Li,6 Renaud Joannes-Boyau,7 Gilbert Price,8 Yue-xing Feng,8 and Christian A. Tryon9 1Department of Biological Sciences, Graduate Program in Ecology and Evolutionary Biology, Ohio University, Athens, OH 45701, USA 2Department of Archaeology, University of Queensland, Brisbane, St Lucia, QLD 4072, Australia 3Department of Anthropology, University of Minnesota, 395 Humphrey Center, 301 19th Avenue S, Minneapolis, MN 55455, USA 4Department of Geology, Baylor University, One Bear Place #97354, Waco, TX 76798, USA 5Department of Anthropology, Queens College, City University of New York, 314 Powdermaker Hall, 65-30 Kissena Boulevard, Flushing, NY 11367, USA 6Center for Archaeological Science, University of Wollongong, Room 268, Building 41, Northﬁelds Avenue, Wollongong, NSW 2522, Australia 7Department of GeoScience, Southern Cross University, PO Box 157, Lismore, NSW 2480, Australia 8School of Earth Sciences, University of Queensland, Brisbane, St Lucia, QLD 4072, Australia 9Department of Anthropology, Harvard University, Peabody Museum, 11 Divinity Avenue, Cambridge, MA 02138, USA *Correspondence: [email protected] (H.D.O.), [email protected] (J.T.F.) http://dx.doi.org/10.1016/j.cub.2015.12.050

SUMMARY the Wasiriya Beds at the Wakondo locality of Rusinga Island, Kenya (Figure 1;[1]). The holotype consists of basicranial, oc- The fossil record provides tangible, historical evidence cipital, and frontal regions, as well as a right horncore [1]; how- for the mode and operation of evolution across deep ever, the facial region is not preserved. Due to 3 cm of upwardly time. Striking patterns of convergence are some of angled nasal bones, it was initially postulated that Rusingoryx the strongest examples of these operations, whereby, may have had a proboscis or an enlarged, domed nasal region over time, similar environmental and/or behavioral [1]. Due in part to the incompleteness of the type specimen, this pressures precipitate similarity in form and function reconstruction was dismissed and the taxonomic validity of Ru- singoryx was questioned [2] until a more recent reexamination between disparately related taxa. Here we present fos- and expanded sample of horn cores and dental material [3]. sil evidence for an unexpected convergence between Here we present six new Rusingoryx cranial specimens exca- gregarious plant-eating mammals and dinosaurs. vated en masse from a channel deposit within the type locality Recent excavations of Late Pleistocene deposits on [4]. These new specimens reveal the presence of an extreme, Rusinga Island, Kenya, have uncovered a catastrophic osseous nasal dome and associated anatomical features assemblage of the wildebeest-like bovid Rusingoryx unparalleled among extant vertebrates. Because there are atopocranion. Previously known from fragmentary numerous specimens across a spectrum of ages, from old to material, these new specimens reveal large, hollow, young, this dataset facilitates ontogenetic, evolutionary, and osseous nasal crests: a craniofacial novelty for mam- functional analyses of this bizarre Late Pleistocene bovid mals that is remarkably comparable to the nasal crests morphology. Our analyses focus on KNM-RU-52572, a com- of lambeosaurine hadrosaur dinosaurs. Using adult plete adult skull that includes all craniofacial bones, maxillary dentition, and the right horncore. For within-species compari- and juvenile material from this assemblage, as well son, we refer to skulls of an 12- to 16-month-old juvenile as computed tomographic imaging, we investigate (KNM-RU-59434) from the Wakondo assemblage and a puta- this convergence from morphological, developmental, tive female referable to the genus Rusingoryx (KNM-HA- functional, and paleoenvironmental perspectives. Our 54933) with a diminutive nasal crest collected from the nearby detailed analyses reveal broad parallels between Pleistocene ( 285,000–40,000 years ago) Luanda West locality R. atopocranion and basal Lambeosaurinae, suggest- on the Homa Peninsula. Interspecific comparisons were also ing that osseous nasal crests may require a highly made across extinct and extant Alcelaphinae, with intracranial specific combination of ontogeny, evolution, and envi- morphology also studied for Megalotragus isaaci (paratype: ronmental pressures in order to develop. KNM-ER-2000). KNM-RU-52572 is post-depositionally compressed in the sagittal plane. The caudal portion of the cranium matches RESULTS AND DISCUSSION the holotype, and the dentition follows recent descriptions of fragmentary material [3]. In mature individuals, the frontal, Abbreviated Description nasal, and premaxillary elements form a prominent, osseous Rusingoryx atopocranion was first described from a partial skull nasal dome. Palatal morphology, best exemplified in compar- (National Museum of Kenya [KNM]-RU-10553A) collected from ative material from the Homa Peninsula (KNM-HA-54933;

Current Biology 26, 503–508, February 22, 2016 ª2016 Elsevier Ltd All rights reserved 503 Figure 1. Rusingoryx atopocranion (A–D) KNM-HA-54933, putative Rusingoryx female from Homa Peninsula. (A) Skull, right lateral view. (B) Digital rendering, with reconstruction of the supralaryngeal vocal tract (SVT) in yellow. (C and D) Coronal and sagittal CT sections demonstrating enlarged maxillary sinuses and the course of the nasal tract. (E–H) KNM-RU-52571, adult R. atopocranion from Wakondo. (E) Skull, right lateral view. (F) The SVT ascends parallel to the outer contour of the skull, departing from the hard palate near the caudal border of the premaxilla. After reaching its apex, the SVT descends toward the internal nares in an ‘‘S’’-shaped curve. (G and H) Coronal and sagittal CT sections. (I–L) KNM-RU-59434, juvenile R. atopocranion excavated from Wakondo. (I) Skull and mandible in right lateral view. (J–L) Digital reconstruction, coronal, and sagittal CT sections (respectively) of the SVT demonstrate ontogenetic differences between adult (KNM-RU-52571) and juvenile R. atopocranion. The nasal portion of the SVT is deeper in the juvenile, and the caudal portion is relatively more voluminous. Scale bars, 4 cm. Abbreviations: aPSep, anterior palatine sinus septum; ms, maxillary sinus; MSep, maxillary sinus septum; NFL, nasal ﬂoor; NSep, nasal septum; pPSep, posterior palatine sinus septum (anterior wall of airway); ps, palatine sinus. See also Figures S1 and S2.

Figures 1A–1D and S1), is likewise exaggerated. The hard pal- ascending parallel to the outer surface of the nasal dome and ate projects deeply caudal to the lateral palatal indentations serving as a roof to the extraordinarily voluminous maxillopala- and bears deep grooves corresponding to attachment sites tine paranasal sinuses. These sinuses comprise the largest pro- for palatal and supralaryngeal musculature (Figure S1). The portion of cranial volume and extend to the midline, where they horizontal palatine bone is completely closed and does not are separated by a median septum (Figures 1C and 1G). Based allow for the passage of the internal nares. Instead, the airway on careful examination of computed tomography (CT) scans, the passes over inflated maxillopalatine paranasal sinuses, result- paranasal sinuses and the airway are not connected by ostia ing in a nasal passage that enters the pharynx from the dorsal larger than 2 mm, rendering them dead airspace (Movie S1). aspect (Figure 1; Movie S1). For a detailed description of The nasal tract is straight through the rostral portion of the cra- R. atopocranion cranial morphology, see Supplemental Exper- nium but deviates ventrally in the frontal region, forming an imental Procedures. ‘‘S’’-shaped curve. This morphology has not been observed pre- Internal morphology reveals further peculiarities. The floor of viously in mammalian taxa. The closest analog is, instead, the the nasal tract significantly departs from the hard palate, nasal tract of basal lambeosaurine hadrosaur dinosaurs [4–10].

504 Current Biology 26, 503–508, February 22, 2016 ª2016 Elsevier Ltd All rights reserved Figure 2. Ontogenetic Similarities between Nasal-Domed Alcelaphine Bovids and Lam- beosaurine Hadrosaur Dinosaurs (A and B) Juvenile R. atopocranion, KNM-RU- 59434 (A). The approximate age of the specimen is 12–16 months. The developing dome is comprised predominantly of nasal bones, and its caudal border is anterior to the orbit. This is in contrast to adult R. atopocranion (B), where the dome is largely comprised of the frontal and nasal bones dorsally, and expanded lacrimal and maxillary bones later- ally. The caudal border of the dome has migrated caudally, situated above the posterior border of the orbit. The frontal becomes angulated. (C and D) A grossly similar pattern is seen in the ontogeny of Hypacrosaurus altispinus. The caudal border of the incipient juvenile crest (C) (Canadian Museum of Nature CMN-2247) migrates from anterior to posterior relative to the orbit. In the adult (D) (CMN-8501), the crest is largely supported by caudolateral portions of the premaxilla, and posterior migration is contingent on ﬂexion of the prefrontal and frontal bones. The airway, highlighted in yellow, is presented for comparison with Figure 1; redrawn from [6]. Scale bars, 4 cm. Abbreviations: Fr, frontal; Jg, jugal; Lac, lacrimal; Mx, maxillary; Na, nasal; Occ, occipital; PMx, premaxilla; PrF, prefrontal; Q, quadrate; Sq, squamosal.

In addition to gross morphology, the following investigations of Evolution ontogeny, evolution, and function of the Rusingoryx nasal To evaluate the evolutionary trajectory of nasal dome acquisi- dome also reveal broad-scale similarities between Alcelaphinae tion, we incorporated new Rusingoryx and referred Homa Penin- and Lambeosaurinae. sula specimens into a phylogenetic analysis of extinct and extant alcelaphines (Figure S2; Supplemental Experimental Proce- Juvenile Morphology dures). Subsequent character-mapping nasal morphology illu- In addition to mature individuals, the assemblage contains the minates the stepwise morphological acquisition of the nasal complete skull of a juvenile (KNM-RU-59434), ontogenetic age dome. The most primitive nasal-domed alcelaphine in our phy- approximately 12–16 months (Supplemental Experimental Pro- logeny, Megalotragus isaaci, possesses a diminutive nasal cedures). This skull bears an incipient crest with a slight degree dome with internal nares that enter the cranium anteriorly (Fig- of angulation rostral to the frontonasal suture. The nasal bones ure 3). Next in succession, M. kattwinkeli demonstrates that crest are slightly elevated, and the premaxilla contacts the maxilla elevation is preceded by a dorsal migration of the nasal pas- and nasals on its caudal border. This suggests that the crest sages (Figures 2 and 3). Subsequent elaboration of crest shifts caudally throughout maturation, such that in adults it initi- morphology is predominately accomplished by inﬂation of lateral ates posterior to the caudal margin of the orbit (Figure 2). The facial bones and sinuses. As with ontogeny, these morphological maxilla heightens throughout development, ultimately forming changes mirror the evolutionary transition from primitive to the lateral wall of the crest. Internally, the angle between the ﬂoor derived lambeosaurine hadrosaurs, wherein dorsal translation of the nasal cavity and hard palate becomes more obtuse, and of the internal nares occurs prior to the heightening and elonga- the portion of the chamber enclosing maxilloturbinates in the ju- tion of the rostral and lateral facial bones ([8]; Figure 3). venile is relatively larger than that of adults. In these respects, the suite of apparent ontogenetic changes in Rusingoryx show Function remarkable similarities to lambeosaurine hadrosaur crest devel- Because the nasal dome and tortuous nasal tract are novel opment ([7]; Figure 2). In both groups, the crest enlarges by (1) structures within Mammalia, direct functional comparisons with increased angulation of the analogous prefrontal and frontal living taxa cannot be made. Plausible functional interpretations bones (hadrosaur and bovid, respectively; herein abbreviated were therefore based on morphological inferences and mathe- as the (pre)frontal elements) (2), simultaneous elongation and matical models. As Rusingoryx is an open-grassland species caudal migration of the rostral facial bones, and (3) distension [11], we prioritized thermoregulation [12], visual display [12], of lateral facial elements [7]. and vocalization [9, 10] as functions particularly relevant to

Current Biology 26, 503–508, February 22, 2016 ª2016 Elsevier Ltd All rights reserved 505 Figure 3. Comparative Evolution of Nasal Crests between Lambeosaurinae and Alcelaphinae Lambeosaurinae are in black text and Alcelaphinae in purple text. Trait acquisition of the nasal dome in both groups follows grossly similar patterns. In the earliest members of both groups, the nasal passages enter the cranium horizontally, and the (pre)frontal elements reflect the primitive condition. Frontal elements then begin to telescope as the nasal passages migrate to enter the pharynx dorsally. This sequence initiates crest formation. Lateral facial elements, including the premaxilla of hadrosaurs and the maxilla of alcelaphines, are then recruited to form the lateral walls of the nasal vestibule. Crest elaboration is at its most derived when the caudal margin of the crest rotates, forming an acute angle with the skull roof. Internally, the nasal airway must contort to follow the roof of the nasal passage. Black elements represent structures that are not preserved. Parasaurolophini presented for consistency with source; redrawn from [8]. See also Figure S3. increased fitness in climatologically arid and behaviorally gregar- with thermoregulation, but there is little conclusive evidence ious contexts. These functions have also been hypothesized for that the elaborate nasal dome enhanced these capacities the nasal domes of lambeosaurine hadrosaurs [9, 10, 12], beyond those of other bovids. enabling another means of comparison between these groups. We next evaluated the potential for visual display, which We first looked for evidence that the Rusingoryx nasal dome among bovids is often realized in the form of male-male honest houses exceptional variants of osseous structures related to or combative signaling ornaments, like horns. Given the propen- thermoregulation. In mammals, cranial thermoregulation is sity for head-striking behavior among artiodactyls [16, 17], the achieved via evaporative cooling across the mucosae of the dome could be used for combative display. Nasal dome maxilloturbinates [13]. Elaboration of the maxilloturbinates is morphology, however, is less congruent with such a hypothesis: positively correlated with an increased demand to conserve res- the narrow depth of the skull bones and voluminous, non- piratory water [13, 14], such that filling its enlarged nasal cham- buttressed cranial cavities (Figure 1; Movie S1) yield a skull ber with a higher surface area of maxilloturbinates could be unlikely to have withstood substantial battery. Along with the beneficial for the thermal and hydrological budgets of Rusin- peculiar, posterior positioning of the horns (Figures 1 and S1), goryx. However, because the elevated nasal cavity floor restricts it is unreasonable to implicate the nasal dome as having an effec- the volume of the dome available for turbinates (Figure 1; Movie tive role in aggressive male-male combat. S1), the intracranial morphology of Rusingoryx is not consistent Competition among males, as well as intra- and interspecific with a hypothesis of enhanced turbinate function. In addition to signaling, can also be accomplished vocally, and there are turbinates, circulating air through the large maxillary sinuses numerous morphological details that substantiate the hypothesis may also dissipate heat; however, there is little evidence for that the nasal dome may play a role in long-distance vocalization the requisite airflow between the sinuses and nasal passages and/or sonic display. Externally, the hard palate possesses that would facilitate evaporative cooling [15]. Like all mammals, deep, bilateral grooves for attachment of the muscles that the maxilloturbinates of R. atopocranion would have assisted shorten the pharynx and elevate the soft palate and larynx

506 Current Biology 26, 503–508, February 22, 2016 ª2016 Elsevier Ltd All rights reserved Table 1. Reconstructed Resonant Frequencies Taxon Specimen SVT Length n = 1 n = 2 n = 3 Note Range Rusingoryx atopocranion KNM-RU-52572 0.74026 m 248.872 Hz 497.744 Hz 746.616 Hz B3–F4 cf. Rusingoryx female KNM-HA-54933 0.42371 m 390.597 Hz 781.194 Hz 1,171.791 Hz G4–D5 Megalotragus isaaci KNM-ER-2000 0.64147 m 258.001 Hz 516.002 Hz 774.003 Hz C3–G5 Values are based on the length of the osseous supralaryngeal vocal tract (SVT) and were calculated using equations described in Supplemental Exper- imental Procedures.

(Figure S1; Movie S1). In addition, the basicranium houses robust because very low-frequency vocalizations may be outside of muscular tubercles for insertion of the rostral pharyngeal con- the potential hearing range of many East African carnivores. It strictors (Figures S1 and S2; Movie S1). This muscle configura- has been hypothesized that similar habitat pressures may have tion is suggestive of an exceptional ability to lift the larynx toward influenced vocal potential in lambeosaurine hadrosaurs [9], the nasal tract. Such laryngeal elevation is also observed in with low-frequency vocalizations allowing these gregarious ani- bovids that vocalize through fleshy nasal vestibules [18–21]. mals to communicate intraspecifically in open and closed Furthermore, the large maxillary and palatal sinuses may have habitats. amplified vocal output by acting as resonating chambers [20, 22]. Prior to this discovery, completely ossified nasal crests have Digital renderings of the osseous supralaryngeal vocal tract only been observed in Archosauria. The large nasal dome of Ru- (SVT; Figure 1) enabled quantitative assessment of the potential singoryx presents a new, mammalian context for studying these for phonic modification using simple bioacoustic models [9, 10, elaborate structures and sheds light on the gross morphological 20, 23]. In mammals, the pharynx and nasal passages, together and developmental changes that predicate elevation of the nasal with the SVT, modify the sound waves produced in the larynx by skeleton. In two distantly related vertebrate groups, lambeosaur- vibrating preferentially at certain resonant frequencies that are ine hadrosaurs and alcelaphine bovids, crest formation follows inversely proportional to vocal tract length [18–25]. Acoustic homoplastic increases in maxillary height and dorsal migration models for harmonic wave production [9, 10, 24] suggest that of the internal nares during both ontogeny and evolution. In the Rusingoryx nasal dome could be capable of propagating both groups, the crest is interpreted to produce vocalizations low-pitched sounds, between 248 and 746 Hz (Table 1; Supple- across the analogous life history contexts of herd forming and mental Experimental Procedures). Because the soft-tissue vocal herbivory. Although similar behaviors are prevalent throughout tract length cannot be reconstructed, these estimated fre- modern vertebrates, they are accomplished largely through quencies are conservatively high. An addition of only 20 cm to soft tissue structures. Just as telescoping of the nasal bones the vocal tract length would result in vocalizations below and reducing the anterior facial skeleton is common to verte- 200 Hz, closer to the range of infrasound. Comparatively, the brates that have developed fleshy trunks, the comparable se- vocal ranges of many other mammals initiate around quences of evolutionary and ontogenetic changes observed for 1,100 Hz [23], suggesting that Rusingoryx vocalizations are hollow dome formation (in conjunction with similar selective low and potentially below the range detectable by predators. pressures) suggests that there are potentially few sequences Perhaps most surprising is the almost complete overlap between of stepwise transformations that result in the formation of large, Rusingoryx resonant frequency reconstructions and those hollow, osseous nasal crests. Expanding comparative studies to calculated for lambeosaurine hadrosaurs [9, 10]. additional taxa may begin to explain the rarity of such skull Environmentally, vocalization is a practical function for the morphology in other vertebrates. crest of Rusingoryx. In animals that form large or diffuse aggrega- tions, efficient communication over long distances, particularly SUPPLEMENTAL INFORMATION through infrasonic vocalizations, may aid in predator avoidance and intraspecific signaling [26]. Within contemporary Alcelaphi- Supplemental Information includes three figures, one table, Supplemental nae, wildebeests (Connochaetes spp.) and hartebeest (Alcela- Data, Supplemental Experimental Procedures, and one movie and can be phus buselaphus) are found in large herds across semi-arid, found with this article online at http://dx.doi.org/10.1016/j.cub.2015.12.050. short-grass savannas of Sub-Saharan Africa. Social behavior is integral in alcelaphines to the extent that elaborate horns, loud AUTHOR CONTRIBUTIONS vocalizations, and conspicuous coloration in adults suggest Conceptualization, H.D.O. and J.T.F.; Methodology, H.D.O.; Validation, K.E.J., that selection may favor species-specific social signals over D.J.P., C.A.T., T.W.P., and G.P.; Formal Analysis, H.D.O., J.T.F., and K.E.J.; predator selection against conspicuousness [27]. Nasal vocali- Writing – Original Draft, H.D.O.; Writing – Reviewing and Editing, J.T.F., zations of Rusingoryx may similarly fall under this evolutionary K.E.J., D.J.P., C.A.T., T.W.P., G.P., and Z.L.J.; Visualization, H.D.O.; Supervi- pretext. Paleoenvironmental evidence from the Wasiriya Beds sion, C.A.T.; Project Administration, J.T.F., D.J.P., and C.A.T.; Funding Acqui- [3, 11, 28, 29] indicates widespread semi-arid grasslands, and sition, J.T.F., C.A.T., D.J.P., T.W.P.; Fieldwork, Y.-x.F., K.E.J., J.T.F., D.J.P., C.A.T., Z.L.J., R.J.-B., and G.P. a markedly high degree of hypsodonty in Rusingoryx molars im- plies a preference for such habitats [3]. Dry environments are ACKNOWLEDGMENTS ideal for low-frequency vocalizations, as these sound waves can travel over 10 km in such environments [26]. Potential selec- This research was conducted under Republic of Kenya research permits tive pressures may also involve mitigation of the trade-offs NCST/5/002/R/576 and NCST/RCD/12B/012/07. Funding was provided by between intraspecific communication and predator avoidance the National Geographic Society (CRE), R. Potts and the Human Origins

Current Biology 26, 503–508, February 22, 2016 ª2016 Elsevier Ltd All rights reserved 507 Program at the Smithsonian Institution, National Science Foundation (BCS- 11. Tryon, C.A., Faith, J.T., Peppe, D.J., Keegan, W.F., Keegan, K.N., Jenkins, 1327047, BCS-1013199, BCS-1013108), Australian Research Council K.H., Nightingale, S., Patterson, D., Van Plantinga, A., Driese, S., et al. (DP1092843, DP140100919, DP120101752, DE120101533), L.S.B. Leakey (2014). Sites on the landscape: paleoenvironmental context of late Foundation, Paleontological Society, American Society of Mammalogists, Pleistocene archaeological sites from the Lake Victoria Basin, equatorial Geological Society of America, Society for Integrative and Comparative East Africa. Quat. Int. 331, 20–30. Biology, American Museum of Natural History (AMNH), Baylor University, Har- 12. Hopson, J.A. (1975). The evolution of cranial display structures in hadro- vard University, New York University, Ohio University, City University of New saurian dinosaurs. Paleobiology 1, 21–43. York, the American School for Prehistoric Research, and University of Wollon- 13. Negus, V. (1958). Comparative Anatomy and Physiology of the Nose and gong. Excavation assistance: M.E. Macharwas, B. Ngeneo, J. Olelo, S. Od- Paranasal Sinuses (Williams & Wilkins). hiambo, L. Mbogori, M. Laird, D.O. Miriga, J.O. Oyugi, R. Onkondoyo, I. Onyango, S. Odoyo, W.O. Oyoro, and J. Siembo. Specimen preparation: 14. Schmidt-Nielsen, K., Schroter, R.C., and Shkolnik, A. (1981). Desaturation E.S. Longoria. CT data collection: the radiology department at the Upper Hill of exhaled air in camels. Proc. R. Soc. Lond. B Biol. Sci. 211, 305–319. Medical Centre, Nairobi. Museum collection access: F.K. Manthi, E. Mbua, 15. Badlangana, N.L., Adams, J.W., and Manger, P.R. (2011). A comparative P. Kiura, M. Munguu, I.O. Farah (National Museum of Kenya); P. Brewer (Nat- assessment of the size of the frontal air sinus in the giraffe (Giraffa camel- ural History Museum of London); R.D.E. MacPhee, E. Westwig, and J. Galkin opardalis). Anat. Rec. (Hoboken) 294, 931–940. (AMNH); and C. Argot (Muse´ um National d’Histoire Naturelle). Sincere thanks 16. Skinner, J.D., and Chimimba, C.T. (2005). The Mammals of the Southern are given to the editor and two anonymous reviewers, as well as L.M. Witmer, African Subregion (Cambridge University Press). P. O’Connor, N.J. Stevens, D. Lieberman, E. Gorscak, A. Prieto-Marquez, C. 17. Kingdon, J., and Hoffman, M. (2013). Pigs, Hippopotamuses, Chevrotain, VanBuren, S. Reilly, G. O’Brien, and P. Gignac for input and editing assistance. Giraffes, Deer and Bovids. Mammals of Africa, Volume VI (Bloomsbury Publishing). Received: September 1, 2015 18. Frey, R., Volodin, I., and Volodina, E. (2007). A nose that roars: anatomical Revised: November 18, 2015 specializations and behavioural features of rutting male saiga. J. Anat. Accepted: December 14, 2015 211, 717–736. Published: February 4, 2016; corrected online February 22, 2016 19. Kingswood, S.C., and Kumamoto, A.T. (1996). Madoqua guentheri. REFERENCES Mamm. Species 539, 1–10. 20. Fitch, W.T. (2000). The phonetic potential of nonhuman vocal tracts: 1. Pickford, M., and Thomas, H. (1984). An aberrant new bovid (Mammalia) in comparative cineradiographic observations of vocalizing animals. subrecent deposits from Rusinga Island, Kenya. P. K. Ned. Akad. Phonetica 57, 205–218. Wetensc. B87, 441–452. 21. Efremova, K.O., Volodin, I.A., Volodina, E.V., Frey, R., Lapshina, E.N., and 2. Harris, J.M. (1991). Koobi Fora Research Project, Volume 3 (Oxford Soldatova, N.V. (2011). Developmental changes of nasal and oral calls in University Press). the goitred gazelle Gazella subgutturosa, a nonhuman mammal with a 3. Faith, J.T., Choiniere, J.N., Tryon, C.A., Peppe, D.J., and Fox, D.L. (2011). sexually dimorphic and descended larynx. Naturwissenschaften 98, Taxonomic status and paleoecology of Rusingoryx atopocranion 919–931. (Mammalia, Artiodactyla), an extinct Pleistocene bovid from Rusinga 22. Alexander, G.D., Houston, D.C., and Campbell, M. (1994). A possible Island, Kenya. Quat. Res. 75, 697–707. acoustic function for the casque structure in hornbills (Aves: 4. Jenkins, K., Faith, J.T., Tryon, C.A., Peppe, D.J., Nightingale, S., Ogondo, Bucerotidae). J. Zool. (Lond.) 233, 57–67. J., Johnson, C.R., and Driese, S. (2012). New excavations of a Late 23. Fitch, W.T. (1997). Vocal tract length and formant frequency dispersion Pleistocene bonebed and associated MSA artifacts from Rusinga Island, correlate with body size in rhesus macaques. J. Acoust. Soc. Am. 102, Kenya. PaleoAnthropology 2012, A17. 1213–1222. 5. Evans, D.C. (2006). Nasal cavity homologies and cranial crest function in 24. Titze, I.R. (1994). Principles of Voice Production (Prentice Hall). lambeosaurine dinosaurs. Paleobiology 32, 109–125. 25. Rendall, D., Kollias, S., Ney, C., and Lloyd, P. (2005). Pitch (F0) and formant 6. Evans, D.C., Ridgely, R., and Witmer, L.M. (2009). Endocranial anatomy of proﬁles of human vowels and vowel-like baboon grunts: the role of vocal- lambeosaurine hadrosaurids (Dinosauria: Ornithischia): a sensorineural izer body size and voice-acoustic allometry. J. Acoust. Soc. Am. 117, perspective on cranial crest function. Anat. Rec. (Hoboken) 292, 1315– 944–955. 1337. 26. Garstang, M., Larom, D., Raspet, R., and Lindeque, M. (1995). 7. Evans, D.C. (2010). Cranial anatomy and systematics of Hypacrosaurus al- Atmospheric controls on elephant communication. J. Exp. Biol. 198, tispinus, and a comparative analysis of skull growth in lambeosaurine ha- 939–951. drosaurids (Dinosauria: Ornithischia). Zool. J. Linn. Soc. 159, 398–434. 27. Estes, R.D. (1991). Behavior Guide to African Mammals (University of 8. Prieto-Ma´ rquez, A., and Wagner, J.R. (2013). The ‘Unicorn’ dinosaur that California Press). wasn’t: a new reconstruction of the crest of Tsintaosaurus and the early 28. Tryon, C.A., Tyler Faith, J., Peppe, D.J., Fox, D.L., McNulty, K.P., Jenkins, evolution of the lambeosaurine crest and rostrum. PLoS ONE 8, e82268. K., Dunsworth, H., and Harcourt-Smith, W. (2010). The Pleistocene 9. Weishampel, D.B. (1981). Acoustic analyses of potential vocalization in archaeology and environments of the Wasiriya Beds, Rusinga Island, lambeosaurine dinosaurs (Reptilia: Ornithischia). Paleobiology 7, Kenya. J. Hum. Evol. 59, 657–671. 252–261. 29. Tryon, C.A., Peppe, D.J., Faith, J.T., Van Plantinga, A., Nightengale, S., 10. Weishampel, D.B. (1997). Dinosaur cacophony: inferring function in extinct and Ogondo, J. (2012). Late Pleistocene artefacts and fauna from organisms. Bioscience 47, 150–159. Rusinga and Mfangano islands, Lake Victoria, Kenya. Azania 47, 14–38.