The Cochlea of the Aroeira 3 Middle Pleistocene Cranium-A Comparative

Journal of Human Evolution 148 (2020) 102887 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Short Communications The cochlea of the Aroeira 3 Middle Pleistocene craniumda comparative study * Mercedes Conde-Valverde a, , Ignacio Martínez a, Rolf Quam a, b, c, d, Juan-Luis Arsuaga a, c, e, Joan Daura f, g, Montserrat Sanz f, g,Joao~ Zilhao~ g, h, i a Catedra de Bioacústica Evolutiva y Paleoantropología (HM Hospitales e Universidad de Alcala), Area de Antropología Física, Departamento de Ciencias de la Vida, Universidad de Alcala, 28871 Alcala de Henares, Madrid, Spain b Department of Anthropology, Binghamton University (SUNY) Binghamton, NY, 13902-6000, USA c Centro Mixto (UCM-ISCIII) de Evolucion y Comportamiento Humanos, Av. Monforte de Lemos 5, 28029, Madrid, Spain d Division of Anthropology, American Museum of Natural History, Central Park West-79th St., New York, NY, 10024, USA e Departamento de Geodinamica, Estratigrafía y Paleontología, Facultad de Ciencias Geologicas, Universidad Complutense de Madrid, 28040, Madrid, Spain f Grup de Recerca del Quaternari (GRQ)-SERP, Departament d'Historia i Arqueologia, C/ Montalegre 6-8, 08001 Barcelona, Spain g UNIARQ-Centro de Arqueologia da Universidade de Lisboa, Faculdade de Letras, Universidade de Lisboa, Alameda da Universidades, 1600-214, Lisbon, Portugal h Department d’Historia i Arqueologia, Universitat de Barcelona, 08007, Barcelona, Spain i Institucio Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluís Companys 23, 08010, Barcelona, Spain article info Article history: characteristic of the Neandertals; (2) a number of fossils dated to Received 9 April 2020 the middle portion of the Middle Pleistocene, including the Accepted 10 September 2020 Atapuerca-Sima de los Huesos (SH) fossils, Swanscombe, Stein- Available online xxx heim, and Reilingen, which show many primitive features, along with some derived Neandertal characteristics; and (3) a group of Keywords: fossils that includes those from the sites of Mauer, Arago, and Inner ear Cochlear evolution Ceprano, which are also dated to the middle portion of the Middle Homo Pleistocene, but show few, if any, clear Neandertal features. Daura Middle Pleistocene et al. (2017) included the Aroeira 3 cranium in the second group. Gruta da Aroeira In particular, the morphology of the glabellar region and the large, triangular postglenoid process were argued to be similar to those of the SH hominins, Steinheim, and Petralona. The preservation of the complete right temporal bone in Aroeira 3 has also allowed for the bony labyrinth to be virtually reconstructed and studied (Conde- Valverde et al., 2018). The bony labyrinth can be divided into three distinct regions: 1. Introduction the semicircular canals, the cochlea, and the vestibule, which joins these two regions together. The semicircular canals perceive head The partial adult cranium Aroeira 3 was discovered in 2014 in movement in three spatial directions, and the cochlea houses the the Gruta da Aroeira, in the Portuguese municipality of Torres organ of Corti, which is responsible for the perception of different Novas and has been dated by means of UeTh disequilibrium to sounds. Jeffery and Spoor (2004) studied changes in the bony lab- between 389 and 436 ka (Daura et al., 2017), making it one of the yrinth during prenatal development and found that adult size is best dated European Middle Pleistocene crania known so far. Cur- achieved during weeks 17e19 of gestation. At the same time, these rent models of Middle Pleistocene human evolution in Europe posit authors suggested the possibility of changes occurring throughout the existence of three distinct hominin groups (Arsuaga et al., 2014; ontogeny. This suggestion has been confirmed by Lyu et al. (2016), Daura et al., 2017): (1) the specimens from some late Middle who found differences in the orientation of the semicircular canals, Pleistocene sites such as Ehringsdorf, La Chaise, or Biache-Saint- and by McRackan et al. (2012), who reported changes in the Vaast, which show most of the derived features often considered orientation of the cochlea with respect to the outer and middle ear, throughout growth and development. Several studies have also discussed the question of sexual dimorphism in the cochlea. A * Corresponding author. meta-analysis by Miller (2007) examined 11 studies, including 109 E-mail address: [email protected] (M. Conde-Valverde). https://doi.org/10.1016/j.jhevol.2020.102887 0047-2484/© 2020 Elsevier Ltd. All rights reserved. M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887 males and 57 females, and found only a single study (Sato et al., The earlier study of the inner ear in Aroeira 3 shows this indi- 1991) which reported significant differences between the sexes in vidual had a largely primitive bony labyrinth, similar to earlier cochlear length. This anomalous result was attributed to the small members of the genus Homo, and lacking the derived Neandertal sample size (6 males and 7 females) used in the Sato et al. (1991) condition in the semicircular canal proportions present in SH study, and Miller (2007) concluded that the cochlea does not (Conde-Valverde et al., 2018). Interestingly, Aroeira 3 shares with show sex differences. More recently, Osipov et al. (2013) analyzed SH a low value of the index of the basal turn of the cochlea, which linear measurements of the bony labyrinth defined by Spoor (1993) was interpreted as evidence for the existence of an Iberian paleo- in 49 males and 45 females. While they found some degree of deme from Marine Isotope Stages 12e11 (Conde-Valverde et al., sexual dimorphism in the semicircular canal dimensions, none of 2018). Although that study only included two variables of the co- the cochlear dimensions examined showed significant differences chlea, the results revealed the significant potential of the cochlea in between males and females. In a more recent study, using the same studies of Middle Pleistocene populations. Thus, a more detailed variables in a sample of 48 females and 50 males representing three analysis of the cochlear dimensions is warranted. We have relied on different populations, Uhl et al. (2020) again found sexual dimor- the 3D reconstruction published in Conde-Valverde et al. (2018), phism in the canals in all three populations (German, Zulu, and and we have measured 12 new cochlear variables compared with Oneota), but the cochlea was sexually dimorphic only in the Oneota that previous study. We have also carried out a new analysis sample. Most recently, however, Braga et al. (2019) demonstrated designed to compare the general proportions of the cochlea in sex-based differences in the torsion of the cochlea in a sample of 50 Aroeira 3 with the SH hominins, Neandertals, recent humans, and females and 44 males. Taken together, these studies indicate the chimpanzees. Our objective is to obtain new information and a importance of considering potential effects of ontogeny and sexual better understanding of the place of this specimen within the dimorphism in studies of taxonomy and phylogeny in hominin context of Middle Pleistocene human evolution in Europe. Given fossils. the close geographic proximity and similar chronology with the SH Within the bony labyrinth, studies of the semicircular canals have fossils, as well as the previously reported similarities in cochlear provided important data and insights into the taxonomy and phy- morphology, we hypothesize Aroeira 3 to show similar cochlear logeny of fossil hominins (Spoor, 1993; Hublin et al., 1996; Spoor dimensions and proportions to the SH fossils and lack the derived et al., 2003; Bouchneb and Crevecoeur, 2009; Gunz et al., 2013; features present in the cochlea of Neandertals and modern humans. Hill et al., 2014; Quam et al., 2016; Li et al., 2017). In general, these studies have shown that the size and proportions of the semicircular 2. Materials and methods canals in living humans are similar to those in Early Pleistocene Homo fossil specimens, suggesting the bony labyrinth morphology We have used the 3D reconstructions published by Conde- in modern humans is largely primitive. At the same time, the Valverde et al. (2018) for Aroeira 3 and those published by semicircular canals in Neandertals show a derived morphology, with Conde-Valverde et al. (2019) for the comparative samples. Tech- absolutely and relatively small anterior and posterior canals and a nical data for the mCT scanning and virtual reconstructions can be larger lateral canal (Hublin et al., 1996; Spoor et al., 2003). The Ne- found in those studies (Conde-Valverde et al., 2019: Table S1). The andertals also show a relatively low placement of the posterior canal, cochlea in Aroeira 3 has been compared with a sample of relative to the plane of the lateral canal (Hublin et al., 1996; Spoor P. troglodytes where we have estimated the sex, one of recent et al., 2003). Interestingly, the absolute and relative sizes of the humans of unknown sex, and two fossil samples. The P. troglodytes semicircular canals in the SH hominins show the derived Neandertal sample includes 10 adult individuals (4 females, 4 males, and 2 of pattern (Quam et al., 2016). Despite being centered on the semi- unknown sex) from the Estacion Biologica de Donana~ (Sevilla, circular canals morphology, these studies also included two vari- Spain). Sex was estimated based on well-known sexual differences ables (cochlear height and width) which allowed to calculate the in the canine size and projection (Dean and Beynon, 1991). The shape index of the cochlear basal turn (COh/w; Spoor, 1993). A low recent humans sample includes 10 adults of unknown sex, 9 of value of this index was considered a population-specificfeatureof them from the mass grave in the Cementerio San Jose (Burgos, the SH hominins (Quam et al., 2016). Spain) and one from the cemetery of Sepulveda (Segovia, Spain).

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