Early Pleistocene faunivorous hominins were not kleptoparasitic, and this impacted the evolution of human anatomy and socio-ecology.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 08 2021
09 08 2021
Historique:
received:
25
03
2021
accepted:
05
07
2021
entrez:
10
8
2021
pubmed:
11
8
2021
medline:
12
11
2021
Statut:
epublish
Résumé
Humans are unique in their diet, physiology and socio-reproductive behavior compared to other primates. They are also unique in the ubiquitous adaptation to all biomes and habitats. From an evolutionary perspective, these trends seem to have started about two million years ago, coinciding with the emergence of encephalization, the reduction of the dental apparatus, the adoption of a fully terrestrial lifestyle, resulting in the emergence of the modern anatomical bauplan, the focalization of certain activities in the landscape, the use of stone tools, and the exit from Africa. It is in this period that clear taphonomic evidence of a switch in diet with respect to Pliocene hominins occurred, with the adoption of carnivory. Until now, the degree of carnivorism in early humans remained controversial. A persistent hypothesis is that hominins acquired meat irregularly (potentially as fallback food) and opportunistically through klepto-foraging. Here, we test this hypothesis and show, in contrast, that the butchery practices of early Pleistocene hominins (unveiled through systematic study of the patterning and intensity of cut marks on their prey) could not have resulted from having frequent secondary access to carcasses. We provide evidence of hominin primary access to animal resources and emphasize the role that meat played in their diets, their ecology and their anatomical evolution, ultimately resulting in the ecologically unrestricted terrestrial adaptation of our species. This has major implications to the evolution of human physiology and potentially for the evolution of the human brain.
Identifiants
pubmed: 34373471
doi: 10.1038/s41598-021-94783-4
pii: 10.1038/s41598-021-94783-4
pmc: PMC8352906
doi:
Types de publication
Historical Article
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
16135Informations de copyright
© 2021. The Author(s).
Références
Domínguez-Rodrigo, M., Barba, R. & Egeland, C. P. Deconstructing Olduvai: a taphonomic study of the Bed I sites (Springer Science & Business Media, 2007).
doi: 10.1007/978-1-4020-6152-3
Domínguez-Rodrigo, M. & Pickering, T. R. The meat of the matter: An evolutionary perspective on human carnivory. Azania 2, 1–29 (2021).
Egeland, C. P. Model hominid lifeways during the Oldowan. Stone Tools Fossil Bones 80, 2 (2012).
Ferraro, J. V. et al. Earliest archaeological evidence of persistent hominin carnivory. PLoS ONE 8, e62174 (2013).
pubmed: 23637995
pmcid: 3636145
doi: 10.1371/journal.pone.0062174
Domínguez-Rodrigo, M. Taphonomy in early African archaeological sites: Questioning some bone surface modification models for inferring fossil hominin and carnivore feeding interactions. J. Afr. Earth. Sci. 108, 42–46 (2015).
doi: 10.1016/j.jafrearsci.2015.04.011
Oliver, J. S., Plummer, T. W., Hertel, F. & Bishop, L. C. Bovid mortality patterns from Kanjera South, Homa Peninsula, Kenya and FLK-Zinj, Olduvai Gorge, Tanzania: Evidence for habitat mediated variability in Oldowan hominin hunting and scavenging behavior. J. Hum. Evol. 131, 61–75 (2019).
pubmed: 31182207
doi: 10.1016/j.jhevol.2019.03.009
Pobiner, B. L. The zooarchaeology and paleoecology of early hominin scavenging. Evol. Anthropol. 29, 68–82 (2020).
pubmed: 32108400
doi: 10.1002/evan.21824
Aiello, L. C. & Wheeler, P. The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199–221 (1995).
doi: 10.1086/204350
Brains and guts in human evolution. The expensive tissue hypothesis. Braz. J. Genet. 20, 2 (1997).
Aiello, L. C., Bates, N. & Joffe, T. In defense of the expensive tissue hypothesis. In Evolutionary anatomy of the primate cerebral cortex 57–78 (Cambridge University Press, 2001).
doi: 10.1017/CBO9780511897085.006
Aiello, L. C. Notes on the implications of the expensive tissue hypothesis for human biological and social evolution. Guts Brains 2, 17–28 (2007).
Konarzewski, M., Goncerzewicz, A., Knapska, E., Dzik, J. & Rkiewicz, T. G. Energetic costs of cognitive abilities: Testing the expensive tissue hypothesis. Authorea. https://doi.org/10.22541/au.159069206.66900218 (2020).
doi: 10.22541/au.159069206.66900218
Roebroeks, W. Guts and brains: An integrative approach to the hominin record (Amsterdam University Press, 2007).
doi: 10.5117/9789087280147
Pontzer, H. Ecological energetics in early homo. Curr. Anthropol. 53, S346–S358 (2012).
doi: 10.1086/667402
Antón, S. C., Potts, R. & Aiello, L. C. Human evolution. Evolution of early Homo: An integrated biological perspective. Science 345, 1236828 (2014).
pubmed: 24994657
doi: 10.1126/science.1236828
de Heinzelin, J. et al. Environment and behavior of 2.5-million-year-old Bouri hominids. Science 284, 625–629 (1999).
pubmed: 10213682
doi: 10.1126/science.284.5414.625
Domínguez-Rodrigo, M., Pickering, T. R., Semaw, S. & Rogers, M. J. Cutmarked bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: Implications for the function of the world’s oldest stone tools. J. Hum. Evol. 48, 109–121 (2005).
pubmed: 15701526
doi: 10.1016/j.jhevol.2004.09.004
Navarrete, A., van Schaik, C. P. & Isler, K. Energetics and the evolution of human brain size. Nature 480, 91–93 (2011).
pubmed: 22080949
doi: 10.1038/nature10629
Potts, R. Early Hominid Activities at Olduvai (AldineTransaction, 1988).
Binford, L. R. Bones: Ancient Men and Modern Myths (Academic Press, 2014).
Isaac, G. The food-sharing behavior of protohuman hominids. Sci. Am. 238, 90–108 (1978).
pubmed: 418504
doi: 10.1038/scientificamerican0478-90
Blumenschine, R. J. Percussion marks, tooth marks, and experimental determinations of the timing of hominid and carnivore access to long bones at FLK Zinjanthropus, Olduvai Gorge, Tanzania. J. Hum. Evol. 29, 21–51 (1995).
doi: 10.1006/jhev.1995.1046
Capaldo, S. D. Experimental determinations of carcass processing by Plio-Pleistocene hominids and carnivores at FLK 22 (Zinjanthropus). Olduvai Gorge, Tanzania. J. Hum. Evol. 33, 555–597 (1997).
pubmed: 9403079
doi: 10.1006/jhev.1997.0150
Selvaggio, M. M. Carnivore tooth marks and stone tool butchery marks on scavenged bones: Archaeological implications. J. Hum. Evol. 27, 215–228 (1994).
doi: 10.1006/jhev.1994.1043
Pante, M. C., Blumenschine, R. J., Capaldo, S. D. & Scott, R. S. Validation of bone surface modification models for inferring fossil hominin and carnivore feeding interactions, with reapplication to FLK 22, Olduvai Gorge, Tanzania. J. Hum. Evol. 63, 395–407 (2012).
pubmed: 22192864
doi: 10.1016/j.jhevol.2011.09.002
Pobiner, B. L. New actualistic data on the ecology and energetics of hominin scavenging opportunities. J. Hum. Evol. 80, 1–16 (2015).
pubmed: 25563408
doi: 10.1016/j.jhevol.2014.06.020
Martínez-Navarro, B. Early Pleistocene Faunas of Eurasia and Hominin Dispersals. In Out of Africa I: The First Hominin Colonization of Eurasia (eds Fleagle, J. G. et al.) 207–224 (Springer, 2010).
doi: 10.1007/978-90-481-9036-2_13
Navarro, B. M. & Palmqvist, P. Presence of the African MachairodontMegantereon whitei (Broom, 1937)(Felidae, Carnivora, Mammalia) in the Lower Pleistocene Site of Venta Micena (Orce, Granada, Spain), with some Considerations on the Origin, Evolution and Dispersal of the Genus. J. Archaeol. Sci. 22, 569–582 (1995).
doi: 10.1006/jasc.1994.0054
Arribas, A. & Palmqvist, P. On the ecological connection between sabre-tooths and hominids: Faunal dispersal events in the lower pleistocene and a review of the evidence for the first human arrival in Europe. J. Archaeol. Sci. 26, 571–585 (1999).
doi: 10.1006/jasc.1998.0346
Espigares, M. P. et al. The earliest cut marks of Europe: A discussion on hominin subsistence patterns in the Orce sites (Baza basin, SE Spain). Sci. Rep. 9, 2 (2019).
doi: 10.1038/s41598-019-51957-5
Blumenschine, R. J. Early hominid scavenging opportunities: implications of carcass availability in the Serengeti and Ngorongoro ecosystems Vol. 283 (British Archaeological Reports, 1986).
doi: 10.30861/9780860543657
Stanford, C. B. & Bunn, H. T. Meat-Eating and Human Evolution (Oxford University Press, 2001).
Parkinson, J. A. Revisiting the hunting-versus-scavenging debate at FLK Zinj: A GIS spatial analysis of bone surface modifications produced by hominins and carnivores in the FLK 22 assemblage, Olduvai Gorge Tanzania. Palaeogeogr. Palaeoclimatol. Palaeoecol. 511, 29–51 (2018).
doi: 10.1016/j.palaeo.2018.06.044
Pickering, T. R. Rough and Tumble: Aggression, Hunting, and Human Evolution (University of California Press, 2013).
doi: 10.1525/9780520955127
Domínguez-Rodrigo, M. & Pickering, T. R. Early hominid hunting and scavenging: a zooarcheological review. Evol. Anthropol. 12, 275–282 (2003).
doi: 10.1002/evan.10119
Domínguez-Rodrigo, M. et al. On meat eating and human evolution: A taphonomic analysis of BK4b (Upper Bed II, Olduvai Gorge, Tanzania), and its bearing on hominin megafaunal consumption. Quat. Int. 322–323, 129–152 (2014).
doi: 10.1016/j.quaint.2013.08.015
Domínguez-Rodrigo, M., Bunn, H. T. & Yravedra, J. A critical re-evaluation of bone surface modification models for inferring fossil hominin and carnivore interactions through a multivariate approach: Application to the FLK Zinj archaeofaunal assemblage (Olduvai Gorge, Tanzania). Quat. Int. 322–323, 32–43 (2014).
doi: 10.1016/j.quaint.2013.09.042
Organista, E. et al. Did Homo erectus kill a Pelorovis herd at BK (Olduvai Gorge)? A taphonomic study of BK5. Archaeol. Anthropol. Sci. 2, 1–24 (2015).
Organista, E. et al. Biotic and abiotic processes affecting the formation of BK Level 4c (Bed II, Olduvai Gorge) and their bearing on hominin behavior at the site. Palaeogeogr. Palaeoclimatol. Palaeoecol. https://doi.org/10.1016/j.palaeo.2017.03.001 (2017).
doi: 10.1016/j.palaeo.2017.03.001
Dominguez-Rodrigo, M. & Pickering, T. R. The meat of the matter: An evolutionary perspective on human carnivory. Azania 52, 4–32 (2017).
doi: 10.1080/0067270X.2016.1252066
Domínguez-Rodrigo, M. Hunting and scavenging by early humans: The state of the debate. J. World Prehist. 16, 1–54 (2002).
doi: 10.1023/A:1014507129795
Capaldo, S. D. Methods, marks, and models for inferring hominid and carnivore behavior. J. Hum. Evol. 35, 317–320 (1998).
pubmed: 9782099
doi: 10.1006/jhev.1998.0242
Lyman, R. L. Archaeofaunas and butchery studies: A taphonomic perspective. Adv. Archeol. Method Theory 10, 249–337 (1987).
doi: 10.1016/B978-0-12-003110-8.50008-6
James, E. C. & Thompson, J. C. On bad terms: Problems and solutions within zooarchaeological bone surface modification studies. Environ. Archaeol. 20, 89–103 (2015).
doi: 10.1179/1749631414Y.0000000023
Domínguez-Rodrigo, M. Are all Oldowan Sites Palimpsests? If so, what can they tell us about Hominid Carnivory? In Interdisciplinary Approaches to the Oldowan (eds Hovers, E. & Braun, D. R.) 129–147 (Springer, 2009).
doi: 10.1007/978-1-4020-9060-8_11
Pizarro-Monzo, M. et al. Do human butchery patterns exist? A study of the interaction of randomness and channelling in the distribution of cut marks on long bones. J. R. Soc. Interface 18, 20200958 (2021).
pubmed: 33499767
doi: 10.1098/rsif.2020.0958
pmcid: 7879749
Beauchamp, G. Social Predation: How Group Living Benefits Predators and Prey (Elsevier, 2013).
Nishimura, K. Kleptoparasitism and cannibalism. Encyclopedia of Animal Behavior, M. D. Breed & J. Moore eds. 253–258 (2010).
doi: 10.1016/B978-0-08-045337-8.00279-5
Domínguez-Rodrigo, M. A study of carnivore competition in riparian and open habitats of modern savannas and its implications for hominid behavioral modelling. J. Hum. Evol. 40, 77–98 (2001).
pubmed: 11161955
doi: 10.1006/jhev.2000.0441
Gidna, A. O., Kisui, B., Mabulla, A., Musiba, C. & Domínguez-Rodrigo, M. An ecological neo-taphonomic study of carcass consumption by lions in Tarangire National Park (Tanzania) and its relevance for human evolutionary biology. Quat. Int. 322–323, 167–180 (2014).
doi: 10.1016/j.quaint.2013.08.059
Schaller, G. B. The Serengeti Lion; a Study of Predator-Prey Relations. Chicago University Press, Chicago (1972).
Ungar, P. S. Dental evidence for the reconstruction of diet in African early Homo. Curr. Anthropol. 53, S318–S329 (2012).
doi: 10.1086/666700
Zink, K. D. & Lieberman, D. E. Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans. Nature 531, 500–503 (2016).
pubmed: 26958832
doi: 10.1038/nature16990
Fonseca-Azevedo, K. & Herculano-Houzel, S. Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution. Proc. Natl. Acad. Sci. U.S.A. 109, 18571–18576 (2012).
pubmed: 23090991
pmcid: 3494886
doi: 10.1073/pnas.1206390109
Domínguez-Rodrigo, M. et al. Earliest modern human-like hand bone from a new >1.84-million-year-old site at Olduvai in Tanzania. Nat. Commun. 6, 7987 (2015).
pubmed: 26285128
doi: 10.1038/ncomms8987
Herries, A. I. R. et al. Contemporaneity of Australopithecus, Paranthropus, and early Homo erectus in South Africa. Science 368, 2 (2020).
doi: 10.1126/science.aaw7293
Bramble, D. M. & Lieberman, D. E. Endurance running and the evolution of Homo. Nature 432, 345–352 (2004).
pubmed: 15549097
doi: 10.1038/nature03052
Lieberman, D. E., Bramble, D. M., Raichlen, D. A. & Shea, J. J. Brains, Brawn, and the Evolution of Human Endurance Running Capabilities. In The First Humans – Origin and Early Evolution of the Genus Homo 77–92 (Springer, 2009).
doi: 10.1007/978-1-4020-9980-9_8
Roach, N. T. & Richmond, B. G. Clavicle length, throwing performance and the reconstruction of the Homo erectus shoulder. J. Hum. Evol. 80, 107–113 (2015).
pubmed: 25439706
doi: 10.1016/j.jhevol.2014.09.004
Larson, S. G. Evolutionary transformation of the hominin shoulder. Evol. Anthropol. 16, 172–187 (2007).
doi: 10.1002/evan.20149
Larson, S. G. Evolution of the Hominin Shoulder: Early Homo. In The First Humans—Origin and Early Evolution of the Genus Homo 65–75 (Springer, 2009).
doi: 10.1007/978-1-4020-9980-9_7
Roach, N. T., Venkadesan, M., Rainbow, M. J. & Lieberman, D. E. Elastic energy storage in the shoulder and the evolution of high-speed throwing in Homo. Nature 498, 483–486 (2013).
pubmed: 23803849
pmcid: 3785139
doi: 10.1038/nature12267
Domínguez-Rodrigo, M. et al. Earliest porotic hyperostosis on a 1.5-million-year-old hominin, Olduvai Gorge, Tanzania. PLoS ONE 7(10), e46414. https://doi.org/10.1371/journal.pone.0046414 (2012).
doi: 10.1371/journal.pone.0046414
pubmed: 23056303
pmcid: 3463614
Wiedeman, A. M. et al. Dietary choline intake: Current state of knowledge across the life cycle. Nutrients 10, 2 (2018).
doi: 10.3390/nu10101513
Derbyshire, E. Could we be overlooking a potential choline crisis in the United Kingdom?. BMJ Nutr. Prev. Health 2, 86–89 (2019).
pubmed: 33235962
pmcid: 7664488
doi: 10.1136/bmjnph-2019-000037
Hoberg, E. P. Taenia tapeworms: Their biology, evolution and socioeconomic significance. Microbes Infect. 4, 859–866 (2002).
pubmed: 12270733
doi: 10.1016/S1286-4579(02)01606-4
Hoberg, E. P. Phylogeny of Taenia: Species definitions and origins of human parasites. Parasitol. Int. 55(Suppl), S23-30 (2006).
pubmed: 16371252
doi: 10.1016/j.parint.2005.11.049
Finch, C. E. & Stanford, C. B. Meat-adaptive genes and the evolution of slower aging in humans. Q. Rev. Biol. 79, 3–50 (2004).
pubmed: 15101252
doi: 10.1086/381662
Finch, C. E. & Stanford, C. B. Lipoprotein genes and diet in the evolution of human intelligence and longevity. In Brain and Longevity 33–67 (Springer, 2003).
doi: 10.1007/978-3-642-59356-7_3
Zaramela, L. S. et al. Gut bacteria responding to dietary change encode sialidases that exhibit preference for red meat-associated carbohydrates. Nat. Microbiol. 4, 2082–2089 (2019).
pubmed: 31548686
pmcid: 6879853
doi: 10.1038/s41564-019-0564-9
Lomangino, K. Gut bacteria, red meat, and CVD. Clin. Nutr. INSIGHT 39, 7–8 (2013).
doi: 10.1097/01.NMD.0000441195.18508.b4
Senghor, B., Sokhna, C., Ruimy, R. & Lagier, J.-C. Gut microbiota diversity according to dietary habits and geographical provenance. Hum. Microb. J. 7–8, 1–9 (2018).
doi: 10.1016/j.humic.2018.01.001
Flower, T. P., Child, M. F. & Ridley, A. R. The ecological economics of kleptoparasitism: Pay-offs from self-foraging versus kleptoparasitism. J. Anim. Ecol. 82, 245–255 (2013).
pubmed: 22943364
doi: 10.1111/j.1365-2656.2012.02026.x
Broom, M. & Ruxton, G. D. Evolutionarily stable kleptoparasitism: Consequences of different prey types. Behav. Ecol. 14, 23–33 (2003).
doi: 10.1093/beheco/14.1.23
Carbone, C. et al. Feeding success of African wild dogs (Lycaon pictus) in the Serengeti: The effects of group size and kleptoparasitism. J. Zool. 266, 153–161 (2005).
doi: 10.1017/S0952836905006710
Vucetich, J. A., Peterson, R. O. & Waite, T. A. Raven scavenging favours group foraging in wolves. Anim. Behav. 67, 1117–1126 (2004).
doi: 10.1016/j.anbehav.2003.06.018
Mills, M. G. L. Kalahari Hyenas: Comparative Behavioral Ecology of Two Species (Blackburn Press, 2003).
Werdelin, L. & Lewis, M. E. Temporal change in functional richness and evenness in the eastern African plio-pleistocene carnivoran guild. PLoS ONE 8, e57944 (2013).
pubmed: 23483948
pmcid: 3590191
doi: 10.1371/journal.pone.0057944
Faurby, S., Silvestro, D., Werdelin, L. & Antonelli, A. Brain expansion in early hominins predicts carnivore extinctions in East Africa. Ecol. Lett. 23, 537–544 (2020).
pubmed: 31943670
pmcid: 7079157
doi: 10.1111/ele.13451
De Cuyper, A. et al. Predator size and prey size-gut capacity ratios determine kill frequency and carcass production in terrestrial carnivorous mammals. Oikos 128, 13–22 (2019).
doi: 10.1111/oik.05488
Vézina, A. F. Empirical relationships between predator and prey size among terrestrial vertebrate predators. Oecologia 67, 555–565 (1985).
pubmed: 28311041
doi: 10.1007/BF00790027
Tsai, C., Hsieh, C. & Nakazawa, T. Predator–prey mass ratio revisited: Does preference of relative prey body size depend on individual predator size?. Funct. Ecol. 30, 1979–1987 (2016).
doi: 10.1111/1365-2435.12680
Portalier, S. M. J., Fussmann, G. F., Loreau, M. & Cherif, M. The mechanics of predator-prey interactions: First principles of physics predict predator-prey size ratios. Funct. Ecol. 33, 323–334. https://doi.org/10.1101/313239 (2019).
doi: 10.1101/313239
Loveridge, A. J. et al. Changes in home range size of African lions in relation to pride size and prey biomass in a semi-arid savanna. Ecography https://doi.org/10.1111/j.1600-0587.2009.05745.x (2009).
doi: 10.1111/j.1600-0587.2009.05745.x
Faith, T., Rowan, J., Du, A. & Barr, A. The uncertain case for human-driven extinctions prior to Homo sapiens. Quatern. Res. 96, 80–104 (2020).
doi: 10.1017/qua.2020.51
Maxwell, S. J., Hopley, P., Upchurch, P. & Soligo, C. Sporadic sampling, not climatic forcing, drives observed early hominin diversity. Proc. Natl. Acad. Sci. 115, 4891–4896 (2018).
pubmed: 29686074
pmcid: 5948983
doi: 10.1073/pnas.1721538115
Viranta, S. Geographic and temporal ranges of middle and late miocene carnivores. J. Mammal. 84, 1267–1278 (2003).
doi: 10.1644/BJK-035
Domínguez-Rodrigo, M., Egeland, C. P., Cobo, L., Baquedano, E., Hulbert, R. Sabertooth carcass consumption behavior and the dynamics of Pleistocene large carnivoran guilds. Quaternary Science Review (under review).
Thompson, J. C., Carvalho, S., Marean, C. W. & Alemseged, Z. Origins of the human predatory pattern: The transition to large-animal exploitation by early hominins. Curr. Anthropol. 60, 1–23 (2019).
doi: 10.1086/701477
Domínguez-Rodrigo, M., Alcalá, L. & Luque, L. Peninj: A Research Project on the Archaeology of Human Origins (1995–2005) (Oxbow, 2009).
Domínguez-Rodrigo, M. et al. Unraveling hominin behavior at another anthropogenic site from Olduvai Gorge (Tanzania): New archaeological and taphonomic research at BK, Upper Bed II. J. Hum. Evol. 57, 260–283 (2009).
pubmed: 19632702
doi: 10.1016/j.jhevol.2009.04.006
Pickering, T. R., Domínguez-Rodrigo, M., Egeland, C. P. & Brain, C. K. New data and ideas on the foraging behaviour of early hominids at Swartkrans Member 3, South Africa. S. Afr. J. Sci. 100, 215–219 (2004).