Journal of Human Evolution 63 (2012) 64e78 Contents lists available at SciVerse ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Evolution and homologies of primate and modern human hand and forearm muscles, with notes on thumb movements and tool use Rui Diogo a,*, Brian G. Richmond b,c, Bernard Wood b,c a Department of Anatomy, Howard University College of Medicine, 520 W St. NW, Washington, DC 20059, USA b Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, George Washington University, DC 20052, USA c Human Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA article info abstract Article history: In this paper, we explore how the results of a primate-wide higher-level phylogenetic analysis of muscle Received 21 January 2012 characters can improve our understanding of the evolution and homologies of the forearm and hand Accepted 5 April 2012 muscles of modern humans. Contrary to what is often suggested in the literature, none of the forearm Available online 27 May 2012 and hand muscle structures usually present in modern humans are autapomorphic. All are found in one or more extant non-human primate taxa. What is unique is the particular combination of muscles. Keywords: However, more muscles go to the thumb in modern humans than in almost all other primates, rein- Phylogenetic analysis forcing the hypothesis that focal thumb movements probably played an important role in human Morphology Extensor pollicis brevis evolution. What makes the modern human thumb myology special within the primate clade is not so fl Flexor pollicis longus much its intrinsic musculature but two extrinsic muscles, extensor pollicis brevis and exor pollicis Adductor pollicis accessorius longus, that are otherwise only found in hylobatids. It is likely that these two forearm muscles play different functional roles in hylobatids and modern humans. In the former, the thumb is separated from elongated digits by a deep cleft and there is no pulp-to-pulp opposition, whereas modern humans exhibit powerful thumb flexion and greater manipulative abilities, such as those involved in the manufacture and use of tools. The functional and evolutionary significance of a third peculiar structure, the intrinsic hand structure that is often called the ‘interosseous volaris primus of Henle’ (and which we suggest is referred to as the musculus adductor pollicis accessorius) is still obscure. The presence of distinct contrahentes digitorum and intermetacarpales in adult chimpanzees is likely the result of pro- longed or delayed development of the hand musculature of these apes. In relation to these structures, extant chimpanzees are more neotenic than modern humans. Ó 2012 Elsevier Ltd. All rights reserved. Introduction (1932) and Straus (1941a, b), usually investigated a wide range of non-primate species but only a few primate taxa (e.g., Brooks, 1886; An understanding of comparative myology is crucial for devel- Parsons, 1898; McMurrich, 1903a, b; Forster, 1917; Howell, 1936a, b; oping hypotheses about the functional morphology of the modern Haines, 1939, 1946, 1950; Straus, 1942a, b). This pattern contrasts human forearm and hand, and particularly their involvement in the with most of the reports published since the 1950s that have manufacture and use of tools (e.g., Day and Napier, 1961, 1963; mainly focused on primates, or even more narrowly, on hominoids Napier, 1962; Tuttle, 1969; Lewis, 1989; Marzke, 1992, 1997; or on modern humans (Hominina: see Fig. 1), and when they did Susman, 1994, 1998; Marzke et al., 1998; Susman et al., 1999; provide a non-primate comparative context it was a relatively Tocheri et al., 2008). The relatively few publications that have narrow one (e.g., Abramowitz, 1955; Day and Napier, 1963; included myological information in discussions of the evolution of Dylevsky, 1967; Tuttle, 1969; Dunlap et al., 1985; Aziz and Dunlap, the primate and modern human forearm and hand can be divided 1986; Susman, 1994, 1998; Marzke et al., 1998; Susman et al., into two groups. Publications prior to the 1950s were mainly the 1999). A notable exception is Lewis' (1989) book that includes work of comparative vertebrate, tetrapod or mammalian anato- detailed information based on his own dissections of a wide range mists who, with the exception of authors such as Howell and Straus of non-primate tetrapods. These studies have generated hypotheses regarding the evolu- tion of primate forearm and hand anatomy, among them that modern humans are derived relative to other extant primates in * Corresponding author. fl fl E-mail addresses: [email protected], [email protected] (R. Diogo). possessing a true exor pollicis longus, a deep head of exor pollicis 0047-2484/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2012.04.001 R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78 65 LEMURIFORMES nomenclature of the forearm and hand muscles of primate and Lemur (Lemuridae) STREPSIRRHINI non-primate tetrapod taxa has been the subject of some confusion Propithecus (Indriidae) and controversy (see Diogo, 2007, 2009; Diogo and Abdala, 2007, Loris (Lorisidae) 2010; Diogo et al., 2009; Diogo and Wood, 2011, 2012). For example, Nycticebus (Lorisidae) statements that some non-hominoid primates have a separate 1,2 LORISIFORMES flexor pollicis longus (e.g., Marzke, 1997; Shrewsbury et al., 2003) Tarsius (Tarsiiformes; Tarsiidae) refer to older publications that often used the name ‘flexor pollicis ’ fl PRIMATES Pithecia (Pitheciidae) longus for the tendon of the exor digitorum profundus that fl Aotus (Aotidae) inserts onto digit 1 and not for a separate exor pollicis longus that has a distinct belly and tendon (see below). 3,4,5 Callithrix (Callitrichinae) Saimiri (Saimiriinae) In recent papers (Diogo and Abdala, 2007; Diogo et al., 2009; CEBIDAE Abdala and Diogo, 2010; Diogo and Wood, 2011) and monographs HAPLORRHINI CEBIDAE+AOTIDAE (Diogo, 2007; Diogo and Abdala, 2010; Diogo and Wood, 2012), PLATYRRHINI Diogo and colleagues have reported the results of their long-term Colobus (Colobinae) dissection-based study of the comparative anatomy, homologies Cercopithecus (Cercopithecini) and evolution of the pectoral and forelimb muscles of all major 6 Macaca (Macanina) groups of non-primate vertebrates and representatives of all of the Papio (Papionina) major primate higher taxa. Diogo and Wood (2011, 2012) combined ANTHROPOIDEA PAPIONINI data from these dissections with carefully validated information 7,8,9 CERCOPITHECINAE from the literature to undertake the first comprehensive parsimony CERCOPITHECIDAE and Bayesian cladistic analyses of the order Primates based on CATARRHINI Hylobates (Hylobatidae) 10,11, myological data (Fig. 1) and for a range of outgroups (tree-shrews, 12,13 14,15, Pongo (Ponginae) 16,17 18,19, dermopterans and rodents). A goal of the project was to establish HOMINOIDEA Gorilla (Gorillini) 20 the homologies of the pectoral and forelimb muscles of vertebrates HOMINIDAE Pan (Panina) and to provide the comparative context for more detailed evolu- HOMININAE Homo (Hominina) 21,22,23, tionary and taxon-based analyses. HOMININI 24,25 The present paper uses data from these dissections to test Figure 1. Single most parsimonious primate tree (L 301, CI 58, RI 73) obtained from the hypotheses about the evolution of the hand musculature of modern cladistic analysis of 166 characters of the head, neck, pectoral and forelimb muscula- humans. Because we have dissected members of all of the major ture (Diogo and Wood, 2011, 2012), showing the unambiguous transitions (homo- primate groups and the major non-primate vertebrate taxa, we can plasic: regular font; non-homoplasic: bold) of the forearm and hand musculature that better understand the descriptions of authors that use different occurred in the branches leading to modern humans: 1) Opponens pollicis is a distinct muscle (this muscle became secondarily undifferentiated in Callithrix); 2) Opponens nomenclatures for these muscles. This has allowed us to clarify digiti minimi is a distinct muscle (also found in a few other mammals, e.g., Rattus); 3) much of the nomenclatural confusion involved in the descriptions Flexor carpi radialis inserts onto the metacarpals II and III (also found in a few other of the forearm and hand muscles of primates (see above). We also mammals, e.g., Tupaia); 4) There are more than two contrahentes digitorum (reverted use these data to critically examine the proposition that modern in some haplorrhines, e.g., modern humans); 5) Adductor pollicis has slightly differ- fl entiated transverse and oblique heads; 6) Supinator has ulnar and humeral heads humans are derived in having a exor pollicis longus, deep head of (independently acquired in Lorisiformes); 7) Adductor pollicis further differentiated flexor pollicis brevis, a ‘volar interosseous’ or ‘interosseous volaris into distinct transverse and oblique heads; 8) Opponens pollicis reaches the distal primus’ of Henle, and an extensor pollicis brevis. portion of metacarpal I (feature independently acquired in Lorisiformes); 9) Opponens digiti minimi is slightly differentiated into superficial and deep bundles; 10) Flexor Materials and methods digitorum superficialis originates from the radius; 11) Flexor digitorum superficialis originates from the ulna; 12) Epitrochleoanconeus is not a distinct muscle (this muscle became undifferentiated in Lorisiformes and in hominoids, and then became