Abstract
Anthropoid vision contributes not only to reaching and grasping but also to the orienting of a food item during the withdraw movement to precisely place it in the mouth for eating. The evolutionary history of this visual control of feeding is not known. It likely evolved from the nonvisual control of the hand that is used with good effect for eating in many non-primate animal species. Strepsirrhines are a relatively large monophyletic group, diverging near the base of the primate cladogram, and described as using vision to reach for food. It is not known whether they use vision to orient food items during the withdraw movement. Video recordings of 7,464 withdraw movements from 22 species of captive strepsirrhines eating their normal food provisions were used to assess whether and how vision contributes to the withdraw movement. The constituent acts of withdraw movements, head orientation, body posture, ground-withdraw and inhand-withdraw, were assessed using frame-by-frame video inspection. Strepsirrhines were versatile in using their hands to get food to the mouth. They displayed variation between and within families that were weakly related to phylogenetic relationships and mainly related to feeding niches. There was no evidence that any species used vision to assist with the withdraw movement. Instead strepsirrhines used mouth reaching to take food from the hand and/or perioral contact to positioning food for biting. Our findings support two hypotheses: that visual mediation of food orienting for placement in the mouth during the withdraw movement is an anthropoid innovation, and that the evolution of the visual control of feeding was not a singular event.
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References
Adams, D. C. (2014). A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Systematic Biology, 63, 685–697. https://doi.org/10.1093/sysbio/syu030.
Adams, D. C., Collyer, M. L., & Kaliontzopoulou, A. (2018). Geomorph: Software for geometric morphometric analyses. R package version 3.0.6. https://cran.r-project.org/package=geomorph.
Arbib, M. (1981). Perceptual structures and distributed motor control. Supplement 2. Handbook of Physiology, The Nervous System, Motor control. https://doi.org/10.1002/cphy.cp010233
Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Evolutionary Anthropology: Issues News and Reviews, 19, 114–118. https://doi.org/10.1002/evan.20251.
Bishop, A. (1964). Use of the hand in lower primates. In: Biology of Primates, Buettner-Janush J. pp 135–225
Cartmill, M. (1972). Arboreal adaptations and the origin of the order Primates. In: The functional and evolutionary biology of primates, Tuttle R. (pp 97–122)
Cartmill, M. (1974). Rethinking primate origins. Science, 184, 436–443.
Cartmill, M. (1992). New views on primate origins. Evolutionary anthropology: Issues news and reviews, 1, 105–111. https://doi.org/10.1002/evan.1360010308.
Cartmill, M. (2012). Primate origins, human origins, and the end of higher taxa. Evolutionary Anthropology, 21, 208–220. https://doi.org/10.1002/evan.21324.
Christel, M. (1993). Grasping techniques and hand preferences in Hominoidea. Hands of Primates (pp. 91–108). Wien: Springer-Verlag.
Christel, M., & Fragaszy, D. (2000). Manual function in Cebus apella. Digital mobility, Preshaping, and endurance in repetitive grasping. International Journal of Primatology, 21, 697–719. https://doi.org/10.1023/A:1005521522418.
de Bruin, N., Sacrey, L. A. R., Brown, L. A., et al. (2008). Visual guidance for hand advance but not hand withdrawal in a reach-to-eat task in adult humans: Reaching is a composite movement. Journal of Motor Behavior, 40, 337–346. https://doi.org/10.3200/JMBR.40.4.337-346.
Edwards, M. G., Wing, A. M., Stevens, J., & Humphreys, G. W. (2005). Knowing your nose better than your thumb: Measures of over-grasp reveal that face-parts are special for grasping. Experimental Brain Research, 161, 72–80. https://doi.org/10.1007/s00221-004-2047-2.
Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15.
Fuller, W. A. (2011). Sampling Statistics. John Wiley & Sons.
Goldman-Rakic, P. S. (1992). Working Memory and the mind. Scientific American, 267, 110–117. https://doi.org/10.1038/scientificamerican0992-110.
Grant, S., & Conway, M. L. (2019). Some binocular advantages for planning reach, but not grasp, components of prehension. Experimental Brain Research, 237, 1239–1255. https://doi.org/10.1007/s00221-019-05503-4.
Hirsche, L. A., Cenni, C., Leca, J. B., & Whishaw, I. Q. (2022). Two types of Withdraw-to-eat Movement related to food size in Long-Tailed Macaques (Macaca fascicularis): Insights into the evolution of the Visual Control of Hand Shaping in Anthropoid Primates. Animal Behavior and Cognition, 9(2), 176–195. https://doi.org/10.26451/abc.09.02.02.2022.
Ivanco, T. L., Pellis, S. M., & Whishaw, I. Q. (1996). Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): Relations to anatomical differences in motor systems. Behavioural Brain Research, 79, 163–181. https://doi.org/10.1016/0166-4328(96)00011-3.
Iwaniuk, A. N., & Whishaw, I. Q. (2000). On the origin of skilled forelimb movements. Trends in Neurosciences, 23, 372–376. https://doi.org/10.1016/S0166-2236(00)01618-0.
Iwaniuk, A. N., Nelson, J. E., Ivanco, T. L., et al. (1998). Reaching, grasping and manipulation of food objects by two tree kangaroo species, Dendrolagus lumholtzi and Dendrolagus matschiei. Australian Journal of Zoology, 46, 235. https://doi.org/10.1071/ZO98004.
Jacobs, R. L. (2015). The evolution of color vision in red-bellied lemurs (Eulemur rubriventer). Stony Brook University: Stony Brook, NY: The Graduate School.
Jeannerod, M. (1981). Intersegmental coordination during reaching at natural visual objects. Attention and performance, IX, 153–169.
Jeannerod, M., Paulignan, Y., & Weiss, P. (1998). Grasping an object: one movement, several components. Sensory guidance of movement 5–20. https://doi.org/10.1002/9780470515563.ch2
Jeannerod, M., Arbib, M. A., Rizzolatti, G., & Sakata, H. (1995). Grasping objects: The cortical mechanisms of visuomotor transformation. Trends in Neurosciences, 18, 314–320. https://doi.org/10.1016/0166-2236(95)93921-J.
Karl, J. M., & Whishaw, I. Q. (2013). Different Evolutionary Origins for the Reach and the grasp: An explanation for dual Visuomotor channels in Primate Parietofrontal Cortex. Frontiers in Neurology. https://doi.org/10.3389/fneur.2013.00208.
Karl, J. M., Sacrey, L. A. R., Doan, J. B., & Whishaw, I. Q. (2012). Oral hapsis guides accurate hand preshaping for grasping food targets in the mouth. Experimental Brain Research, 221, 223–240. https://doi.org/10.1007/s00221-012-3164-y.
Karl, J. M., Wilson, A. M., Bertoli, M. E., & Shubear, N. S. (2018). Touch the table before the target: Contact with an underlying surface may assist the development of precise visually controlled reach and grasp movements in human infants. Experimental Brain Research, 236, 2185–2207. https://doi.org/10.1007/s00221-018-5293-4.
Kirk, E. C. (2004). Comparative morphology of the eye in primates. Anatomical Record, 281A, 1095–1103. https://doi.org/10.1002/ar.a.20115.
Leopold, D. A., Mitchell, J. F., & Freiwald, W. A. (2020). Chap. 25 - Evolved Mechanisms of High-Level Visual Perception in Primates. In: Kaas JH (ed) Evolutionary Neuroscience (Second Edition, pp 589–625). Academic Press, London.
Lhota, S., Jůnek, T., & Bartoš, L. (2009). Patterns and laterality of hand use in free-ranging aye-ayes (Daubentonia madagascariensis) and a comparison with captive studies. Journal of Ethology, 27, 419–428. https://doi.org/10.1007/s10164-008-0136-6.
Macfarlane, N. B. W., & Graziano, M. S. A. (2009). Diversity of grip in Macaca mulatta. Experimental Brain Research, 197, 255–268. https://doi.org/10.1007/s00221-009-1909-z.
Marzke, M. W., Marchant, L. F., McGrew, W. C., & Reece, S. P. (2015). Grips and hand movements of chimpanzees during feeding in Mahale Mountains National Park, Tanzania. American Journal of Physical Anthropology, 156, 317–326. https://doi.org/10.1002/ajpa.22651.
Nekaris, K. A. I. (2005). Foraging behaviour of the slender loris (Loris lydekkerianus lydekkerianus): Implications for theories of primate origins. Journal of Human Evolution, 49, 289–300. https://doi.org/10.1016/j.jhevol.2005.04.004.
Nevo, O., & Heymann, E. W. (2015). Led by the nose: Olfaction in primate feeding ecology. Evolutionary Anthropology, 24, 137–148. https://doi.org/10.1002/evan.21458.
Paradis, E., & Schliep, K. (2019). Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35, 526–528. https://doi.org/10.1093/bioinformatics/bty633.
Peckre, L. R., Fabre, A. C., Wall, C. E., et al. (2016). Holding-on: Co-evolution between infant carrying and grasping behaviour in strepsirrhines. Scientific Reports, 6, https://doi.org/10.1038/srep37729.
Peckre, L. R., Fabre, A. C., Hambuckers, J., et al. (2019). Food properties influence grasping strategies in strepsirrhines. Biological Journal of the Linnean Society. https://doi.org/10.1093/biolinnean/bly215.
Peckre, L. R., Lowie, A., Brewer, D., et al. (2019). Food mobility and the evolution of grasping behavior: A case study in strepsirrhine primates. Journal of Experimental Biology. https://doi.org/10.1242/jeb.207688.
Perrenoud, M., Herrel, A., Borel, A., & Pouydebat, E. (2020). Strategies of food detection in a captive cathemeral lemur, Eulemur rubriventer. Belgium Journal of Zoology, 145, https://doi.org/10.26496/bjz.2015.59.
Pouydebat, E., Laurin, M., Gorce, P., & Bels, V. (2008). Evolution of grasping among anthropoids. Journal of Evolutionary Biology, 21, 1732–1743. https://doi.org/10.1111/j.1420-9101.2008.01582.x.
Preuss, T. M., & Goldman-Rakic, P. S. (1991). Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. Journal of Comparative Neurology, 310, 429–474. https://doi.org/10.1002/cne.903100402.
R Core Team. (2021). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Reghem, E., Tia, B., Bels, V., & Pouydebat, E. (2011). Food Prehension and Manipulation in Microcebus murinus (Prosimii, Cheirogaleidae). Folia Primatologica, 82, 177–188. https://doi.org/10.1159/000334077.
Sacrey, L. A. R., Travis, S. G., & Whishaw, I. Q. (2011). Drug treatment and familiar music aids an attention shift from vision to somatosensation in Parkinson’s disease on the reach-to-eat task. Behavioural Brain Research, 217, 391–398. https://doi.org/10.1016/j.bbr.2010.11.010.
Sartori, L., Camperio-Ciani, A., Bulgheroni, M., & Castiello, U. (2015). Intersegmental coordination in the kinematics of Prehension movements of Macaques. Plos One, 10, e0132937. https://doi.org/10.1371/journal.pone.0132937.
Scott, J. E. (2019). Macroevolutionary effects on primate trophic evolution and their implications for reconstructing primate origins. Journal of Human Evolution, 133, 1–12. https://doi.org/10.1016/j.jhevol.2019.05.001.
Sussman, R. W. (1991). Primate origins and the evolution of angiosperms. American Journal of Primatology, 23, 209–223. https://doi.org/10.1002/ajp.1350230402.
Sussman, R. W., & Raven, P. H. (1978). Pollination by lemurs and marsupials: An archaic coevolutionary system. Science, 200, 731–736. https://doi.org/10.1126/science.200.4343.731.
Sussman, R. W., Rasmussen, D. T., & Raven, P. H. (2013). Rethinking primate origins again. American Journal of Primatology, 75, 95–106. https://doi.org/10.1002/ajp.22096.
Sustaita, D., Pouydebat, E., Manzano, A., et al. (2013). Getting a grip on tetrapod grasping: Form, function, and evolution: Grasping in tetrapods. Biological Reviews, 88, 380–405. https://doi.org/10.1111/brv.12010.
Veilleux, C. C., & Christopher, K. E. (2009). Visual acuity in the cathemeral strepsirrhine Eulemur macaco flavifrons. American Journal of Primatology, 71, 343–352. https://doi.org/10.1002/ajp.20665.
Whishaw, I. Q., & Coles, B. L. K. (1996). Varieties of paw and digit movement during spontaneous food handling in rats: Postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behavioural Brain Research, 77, 135–148. https://doi.org/10.1016/0166-4328(95)00209-X.
Whishaw, I. Q., & Karl, J. M. (2014). The contribution of the reach and the grasp to shaping brain and behaviour. Canadian Journal of Experimental Psychology/Revue canadienne de psychologie expérimentale, 68, 223–235. https://doi.org/10.1037/cep0000042.
Whishaw, I. Q., & Karl, J. M. (2019). The evolution of the hand as a tool in feeding behavior: The multiple motor channel theory of hand use. In V. Bels, & I. Q. Whishaw (Eds.), Feeding in vertebrates (pp. 159–186). Cham: Springer International Publishing.
Whishaw, I. Q., Faraji, J., Agha, M., B., et al. (2018). A mouse’s spontaneous eating repertoire aids performance on laboratory skilled reaching tasks: A motoric example of instinctual drift with an ethological description of the withdraw movements in freely-moving and head-fixed mice. Behavioural Brain Research, 337, 80–90. https://doi.org/10.1016/j.bbr.2017.09.044.
Whishaw, I. Q., Sarna, J. R., & Pellis, S. M. (1998). Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behavioural Brain Research, 96, 79–91. https://doi.org/10.1016/S0166-4328(97)00200-3.
Whishaw, I. Q., Ghasroddashti, A., Mirza Agha, B., & Mohajerani, M. H. (2020). The temporal choreography of the yo-yo movement of getting spaghetti into the mouth by the head-fixed mouse. Behavioural Brain Research, 381, 112241. https://doi.org/10.1016/j.bbr.2019.112241.
Acknowledgements
We thank the staff of the Duke Lemur Center, the Antwerp Zoo and the Vincennes Zoo for their assistance during data collection. A.-C.F. thanks the Fondation Fyssen and the Marie-Skłodowska Curie fellowship (EU project 655694 – GETAGRIP) for funding. C.E.W. thanks the National Science Foundation for funding (BCS-1062239). E. Pouydebat thanks the “ATM Collections Vivantes, MNHN, Paris, France” for funding. This is Duke Lemur Center Publication Number 1546.
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I.Q.W. conceptualized the study, L.R.P. and A.-C. F. collected the data. I.Q.W. and L.R.P. analyzed the data and drafted the manuscript. A.-C.F., E.P. and C.E.W. provided funding for data collection. All authors participated in reviewing and editing the MS and gave final approval for publication.
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Peckre, L.R., Fabre, AC., Wall, C.E. et al. Evolutionary History of food Withdraw Movements in Primates: Food Withdraw is Mediated by Nonvisual Strategies in 22 Species of Strepsirrhines. Evol Biol 50, 206–223 (2023). https://doi.org/10.1007/s11692-023-09598-0
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DOI: https://doi.org/10.1007/s11692-023-09598-0