Annals of Anatomy 223 (2019) 19–31 Contents lists available at ScienceDirect Annals of Anatomy jou rnal homepage: www.elsevier.com/locate/aanat Invited Review Comparative morphology of the primate tongue a,b,∗ c d c Shin-ichi Iwasaki , Ken Yoshimura , Junji Shindo , Ikuo Kageyama a Department of Medical Technology and Clinical Engineering, Faculty of Health and Medical Sciences, Hokuriku University, Kanazawa, Japan b Professor emeritus, The Nippon Dental University, Tokyo and Niigata, Japan c Department of Anatomy, The Nippon Dental University School of Life Dentistry at Niigata, Niigata, Japan d Laboratory of Wildlife Science, School of Veterinary Medicine, Kitasato University, Towada, Japan a r t i c l e i n f o a b s t r a c t Article history: To clarify the role of the primate tongue as a means to better understand the evolution of oral function Received 16 November 2018 among primates – an example of adaptation within the restricted phylogenetic group - we review the Accepted 15 January 2019 morphological knowledge of the tongues of extant primates in relation to phylogenetic classification. Prosimians tongues are more effective than those of Haplorhini for taking up food with the tongue alone, Keywords: because they are capable of fine movement when outside the oral cavity. However, the role of the tongue Primate in food uptake has diminished when juxtaposed with progress in hand manipulation of food and tools Tongue in Haplorhini, especially with the manipulation of tools by Homininae. This change in the tongue from Lingual papillae prosimians to Homininae can be regarded as degeneration in food uptake by the tongue, although the Comparative anatomy functional role of the tongue within the oral cavity has not diminished. The distribution pattern and form Functional evolution of lingual papillae, except foliate papillae, are very similar among all reported primates species. Although foliate papillae are generally well developed in Haplorhini, most prosimian species have no foliate papil- lae, or a different type of papillae that substitute for foliate papillae. There are three vallate papillae in prosimian species and the New-World macaques, Platyrrhini. These papillae exhibit an inverted V-shape and are more numerous in Old World macaques, Catarrhini. These differences seem to be the result of phylogenetic origin. © 2019 Elsevier GmbH. All rights reserved. Contents 1. Introduction . 20 2. Primate evolution and phylogenetics . 20 3. Comparative morphology of the tongue and lingual papillae in extant primates . 20 3.1. Strepsirrhini (Semiorder) . 21 3.1.1. Lemuriformes (Infraorder) . 21 3.1.2. Lorisiformes (Infraorder) . 22 3.2. Haplorhini (Semiorder) . 23 3.2.1. Tarsiiformes (Infraorder) . 23 3.2.2. Platyrrhini (Infraorder) . 23 3.2.3. Catarrhini (Infraorder). .24 4. Comparative morphology of the tongue and lingual papillae among species . 26 5. The tongue musculature in extant primates . 26 6. Functional role of the tongue in primate evolution . 29 7. Conclusions . 30 Acknowledgements. .30 References . 30 ∗ Corresponding author at: Department of Medical Technology and Clinical Engineering, Faculty of Health and Medical Sciences, Hokuriku University, 1-1 Taiyo- gaoka, Kanazawa 920-1180, Ishikawa, Japan E-mail address: [email protected] (S.-i. Iwasaki). https://doi.org/10.1016/j.aanat.2019.01.008 0940-9602/© 2019 Elsevier GmbH. All rights reserved. 20 S.-i. Iwasaki, K. Yoshimura, J. Shindo, et al. / Annals of Anatomy 223 (2019) 19–31 1. Introduction The tongue has important roles in food uptake, mastication and swallowing in most tetrapods. A movable tongue of voluntary muscle has developed through adaptation in terrestrial vertebrate evolution and has persisted in almost all extant tetrapods, irrespec- tive of their living environment (Iwasaki, 2002). Recently, Iwasaki et al. (2019) reported significant variations in the role of the tongue in tetrapods. On the one hand, the tongue can be extremely impor- tant in food uptake, as in frogs of the Amphibia, chameleons of the Reptilia and humming birds of the Aves. On the other hand, the role of the tongue is significantly diminished in a few species of frogs, turtle species and some bird species. Naturally, in the latter case, the tongue cannot play an important role in food uptake, mastication or swallowing. The degenerative tendency of the tongue illustrated Fig. 1. Classification of extant primate genera from order to infraorder, as compared by these examples is a form of evolutionary specialization. How- with the results of molecular phylogenetic analysis. The red underlining shows five ever, the mechanism by which this form of degeneration originated groups (infraorder) of the systematic classification. The blue asterisks show the five during the process of evolution has not been described. groups identified by molecular phylogenetic analysis. Unlike that of all other vertebrates, the human tongue has an extremely unusual role as the essential organ of spoken language. split - the first divergence after the appearance of the primates - This function also exemplifies evolutionary specialization of the namely, the estimation before the Cretaceous-Paleogene extinc- vertebrate tongue. An important challenge is to clarify the evolu- tion (Springer et al., 2012; Pozzi et al., 2014), and that after the tionary process underlying this function. However, we first need to Cretaceous-Paleogene extinction (Martin 1993; Chatterjee et al., clarify morphological knowledge of the tongues of extant primates 2009; O’Leary et al., 2013). Strepsirrhini is thought to be the in relation to phylogenetic classification. Before describing the evo- ancestor of all extant prosimians (Whitten and Brockman, 2001). lution of the anthropoid tongue prior to the appearance of humans, Molecular and fossil evidence (Goodman et al., 1998) suggested that the role of the primate tongue should be considered in order to Strepsirrhini divided into Lemuriformes and Loriformes, which is better understand how oral function evolved among primates, an thought to be the ancestor of lemurs, lorises and allies, whereas example of adaptation within a restricted phylogenetic group. In Haplorhines divided into Tarsiiformes, the putative ancestor of tar- particular, among primates the tongue of the human, Homo sapi- siers, which are classified as prosimians, and Anthropoides, after ens, has achieved significant specialization in language acquisition. the Cretaceous-Paleogene extinction. Furthermore, Anthropoides Taken together, these analyses may improve our understanding of divided into Platyrrhini, which is thought to be the ancestor of New the evolutionary role of the human tongue. World monkeys, and Catarrhini, the putative ancestor of Old World In this report, we review the relevant literature in order to clarify monkeys. The divergence of the Catarrhini groups Hominoidea and the morphological differences and similarities of primate tongues, Cercopithecidea is estimated to have occurred 23 to 29 Mya (Raaum including the human tongue. We hope that our findings will lead et al., 2005; Chatterjee et al., 2009; Steiper and Young, 2009). In to new hypotheses on the functional role of the primate tongue, addition, the divergence of genus Homo and genus Pan is estimated including that of humans which combine insights from different to have occurred 6 Mya (Raaum et al., 2005). fields, thus yielding a more comprehensive understanding of pri- In a review of primate phylogenetics, Perelman et al. (2011) mate evolution. estimated the extant number of primate species at 261 to 377, and 67 to 69 primate genera originated from a common ances- tor (Goodman et al., 1998; Grove, 2001; Wilson and Reeder, 2005). 2. Primate evolution and phylogenetics Data is accumulating on the numbers of primate species and gen- era. Although there are several different classifications of extant The amniotic Synapsids include the original mammalian ances- primates (Goodman et al., 1998; Groves, 2001; Miller et al., 2005; tor and are thought to have diverged from a Sauropsid reptile Masters et al., 2007; Disotell, 2008; Perelman et al., 2011; Fleagle, during the late Carboniferous, about 320 to 315 million years ago 2013; Pozzi et al., 2014), there are five primate infraorders, namely (Mya), i.e., just a few tens of millions of years after the appearance Lemuriformes, Lorisiformes, Tarsiiformes, Platyrrhini and Catar- of the first amniotes in the mid-Carboniferous, around 340 Mya rhini, according to a recent classification, as shown in Fig. 1 (Carroll, 1992; Steward, 1997; Laurin and Gauthier, 2011). At the (Disotell, 2008; Fleagle, 2013). On the basis of the most recent end of the Mesozoic, the Cretaceous-Paleogene extinction around molecular phylogenetic analysis, Pozzi et al. (2014) reported that 65.5 Mya decisively changed the interrelationship between reptiles extant primates can be divided into five groups; Lorisiformes, and mammals (Alvarez et al., 1980; Schulte et al., 2010). During Lemuriformes, Haplorhini, Anthropoidea and Catarrhini. How- this event, all non-avian dinosaurs, ammonites, Mosasaurus, Ple- ever, in a classification of extant primate genera, Haplorhini is a siosaurus, and many groups of mammals suddenly disappeared semiorder that includes the suborders Tarsiiformes and Anthro- (MacLeod et al., 1997). The consensus is that mammals began to poidea, and the suborder Anthropoidea includes the infraorders rapidly diversify during the Paleogene period after the Cretaceous- Platyrrhini and Catarrhini (Disotell, 2008; Fleagle, 2013). This dis-