Evolution of grasping among anthropoids

The prevailing hypothesis about grasping in primates stipulates an evolution from power towards precision grips in hominids. The evolution of grasping is far more complex, as shown by analysis of new morphometric and behavioural data. The latter concern the modes of food grasping in 11 species (one platyrrhine, nine catarrhines and humans). We show that precision grip and thumb‐lateral behaviours are linked to carpus and thumb length, whereas power grasping is linked to second and third digit length. No phylogenetic signal was found in the behavioural characters when using squared‐change parsimony and phylogenetic eigenvector regression, but such a signal was found in morphometric characters. Our findings shed new light on previously proposed models of the evolution of grasping. Inference models suggest that Australopithecus, Oreopithecus and Proconsul used a precision grip.

[1]  M. Girondot,et al.  The evolution of long bone microstructure and lifestyle in lissamphibians , 2004, Paleobiology.

[2]  S. Pellis,et al.  Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species , 1998, Behavioural Brain Research.

[3]  Bernard Wood,et al.  Older than the Oldowan? Rethinking the emergence of hominin tool use , 2003 .

[4]  Nathan M. Young,et al.  Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  S. Perry The Complete Capuchin , 2005, International Journal of Primatology.

[6]  J. Schmitz,et al.  Primate jumping genes elucidate strepsirrhine phylogeny. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[7]  K. Beard,et al.  A survey of fossil primate hands , 1993 .

[8]  K. Nishikawa,et al.  Evolution of forelimb movement patterns for prey manipulation in anurans. , 1997, The Journal of experimental zoology.

[9]  Ian Q. Whishaw,et al.  Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems , 1996, Behavioural Brain Research.

[10]  K. Bard,et al.  Precision grips in young chimpanzees , 1996, American journal of primatology.

[11]  Dorothy M Fragaszy,et al.  Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). , 1995, Journal of comparative psychology.

[12]  C. Lovejoy,et al.  Hominid tarsal, metatarsal, and phalangeal bones recovered from the Hadar Formation: 1974-1977 collections , 1982 .

[13]  A. Janke,et al.  Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. , 2004, Hereditas.

[14]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

[15]  D. Graur,et al.  Playing chicken (Gallus gallus): methodological inconsistencies of molecular divergence date estimates due to secondary calibration points. , 2002, Gene.

[16]  Derek E Wildman,et al.  Moving primate genomics beyond the chimpanzee genome. , 2005, Trends in genetics : TIG.

[17]  P. Nystrom,et al.  The Life of Primates , 2008 .

[18]  C. Bergé,et al.  Use and Manufacture of Tools to Extract Food by Captive Gorilla gorilla gorilla: Experimental Approach , 2005, Folia Primatologica.

[19]  E. de Margerie,et al.  Phylogenetic signal in bone microstructure of sauropsids. , 2005, Systematic biology.

[20]  P. R. Davis,et al.  The fore-limb skeleton and associated remains of Proconsul Africanus , 1959 .

[21]  CALIBRATION AGE AND QUARTET DIVERGENCE DATE ESTIMATION , 2004, Evolution; international journal of organic evolution.

[22]  V. Bracha,et al.  The reaching reaction in the rat: A part of the digging pattern? , 1990, Behavioural Brain Research.

[23]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[24]  Sue Taylor Parker,et al.  Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in cebus monkeys and great apes , 1977 .

[25]  C. Brochu PATTERNS OF CALIBRATION AGE SENSITIVITY WITH QUARTET DATING METHODS , 2004, Journal of Paleontology.

[26]  E. Visalberghi,et al.  The Complete Capuchin: The Biology of the Genus Cebus , 2004 .

[27]  Ziheng Yang,et al.  Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context , 2004, Molecular ecology.

[28]  D. Brooks,et al.  Miocene hominoid biogeography: pulses of dispersal and differentiation , 2007 .

[29]  R. L. Susman Hand function and tool behavior in early hominids. , 1998, Journal of human evolution.

[30]  D. Wildman,et al.  Accelerated evolution of the electron transport chain in anthropoid primates. , 2004, Trends in genetics : TIG.

[31]  Dorothy Fragaszy,et al.  Manual Function in Cebus apella. Digital Mobility, Preshaping, and Endurance in Repetitive Grasping , 2000, International Journal of Primatology.

[32]  R. L. Susman,et al.  New hominid fossils from the Swartkrans formation (1979-1986 excavations): postcranial specimens. , 1989, American journal of physical anthropology.

[33]  M. Godinot,et al.  Morphologie quantitative deprimates éocènes comparés aux primates actuels: Exemples de recherches en cours , 1997 .

[34]  Alan Walker,et al.  Comparative and functional anatomy of Proconsul phalanges from the Kaswanga Primate Site, Rusinga Island, Kenya , 1994 .

[35]  Valentina Truppa,et al.  Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item. , 2004, American journal of physical anthropology.

[36]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

[37]  M. Christel Grasping techniques and hand preferences in Hominoidea , 1993 .

[38]  S. Viegas,et al.  Evolution of the power ("squeeze") grip and its morphological correlates in hominids. , 1992, American journal of physical anthropology.

[39]  C Boesch,et al.  Tool use and tool making in wild chimpanzees. , 1990, Folia primatologica; international journal of primatology.

[40]  P. Legendre,et al.  QUANTIFYING PHYLOGENETICALLY STRUCTURED ENVIRONMENTAL VARIATION , 2003, Evolution; international journal of organic evolution.

[41]  I. Whishaw,et al.  On the origin of skilled forelimb movements , 2000, Trends in Neurosciences.

[42]  S. Moyà-Solà,et al.  Evidence of hominid-like precision grip capability in the hand of the Miocene ape Oreopithecus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. T. Stern,et al.  The locomotor anatomy of Australopithecus afarensis. , 1983, American journal of physical anthropology.

[44]  J. Diniz‐Filho,et al.  AN EIGENVECTOR METHOD FOR ESTIMATING PHYLOGENETIC INERTIA , 1998, Evolution; international journal of organic evolution.

[45]  L. Witmer 2 The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils , 2007 .

[46]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[47]  M. Laurin The evolution of body size, Cope's rule and the origin of amniotes. , 2004, Systematic biology.

[48]  T. Poole The Handbook of Ethological Methods, Philip N. Lehner. Garland STMP Press, New York (1979), Price $24.50 , 1980 .

[49]  R. L. Susman,et al.  Oreopithecus bambolii: an unlikely case of hominid-like grip capability in a Miocene ape. , 2004, Journal of human evolution.

[50]  J. R. Napier,et al.  STUDIES OF THE HANDS OF LIVING PRIMATES , 2009 .

[51]  Y. Coppens,et al.  La préhension chez les Primates : précision, outils et perspectives évolutives , 2006 .

[52]  A. Walker,et al.  New Postcranial Fossils of Proconsul africanus and Proconsul nyanzae , 1983 .

[53]  M. Laurin,et al.  Fossils, molecules, divergence times, and the origin of lissamphibians. , 2007, Systematic biology.

[54]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[55]  C. Ward,et al.  Function, Phylogeny, and Fossils , 1997, Advances in Primatology.

[56]  E. Douzery,et al.  Primate phylogeny, evolutionary rate variations, and divergence times: a contribution from the nuclear gene IRBP. , 2004, American journal of physical anthropology.

[57]  D. Fragaszy,et al.  Behavioral development and maternal care in tufted capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) from birth through seven months. , 1991, Developmental psychobiology.

[58]  James G. Ogg,et al.  A Geologic Time Scale 2004: CONCEPTS AND METHODS , 2004 .

[59]  R. L. Susman,et al.  Who Made the Oldowan Tools? Fossil Evidence for Tool Behavior in Plio-Pleistocene Hominids , 1991, Journal of Anthropological Research.

[60]  V. Bels,et al.  Substrate optimization in nut cracking by capuchin monkeys (Cebus apella) , 2006, American Journal of Primatology.

[61]  H. Mchenry,et al.  The capitate of Australopithecus afarensis and A. africanus. , 1983, American journal of physical anthropology.

[62]  R. Corruccini,et al.  New Interpretations of Ape and Human Ancestry , 1983, Advances in Primatology.

[63]  R. L. Susman Comparative and functional morphology of hominoid fingers. , 1979, American journal of physical anthropology.

[64]  Marianne I. Christel,et al.  How Precisely Do Bonobos (Pan paniscus) Grasp Small Objects? , 1998, International Journal of Primatology.

[65]  B. Williams,et al.  Phylogenetic analysis of anthropoid relationships. , 1998, Journal of human evolution.

[66]  R. L. Susman,et al.  Fossil evidence for early hominid tool use. , 1994, Science.

[67]  D. Graur,et al.  Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. , 2004, Trends in genetics : TIG.

[68]  W. B. Harland,et al.  A Geologic time scale , 1982 .