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The Evolution of Self-Control PNAS PLUS The evolution of self-control PNAS PLUS Evan L. MacLeana,1, Brian Harea,b, Charles L. Nunna, Elsa Addessic, Federica Amicid, Rindy C. Andersone, Filippo Aurelif,g, Joseph M. Bakerh,i, Amanda E. Baniaj, Allison M. Barnardk, Neeltje J. Boogertl, Elizabeth M. Brannonb,m, Emily E. Brayn, Joel Braya, Lauren J. N. Brentb,o, Judith M. Burkartp, Josep Calld, Jessica F. Cantlonk, Lucy G. Chekeq, Nicola S. Claytonq, Mikel M. Delgador, Louis J. DiVincentis, Kazuo Fujitat, Esther Herrmannd, Chihiro Hiramatsut, Lucia F. Jacobsr,u, Kerry E. Jordanv, Jennifer R. Laudew, Kristin L. Leimgruberx, Emily J. E. Messerl, Antonio C. de A. Mouray, Ljerka Ostojicq, Alejandra Picardz, Michael L. Platta,b,o,aa, Joshua M. Plotnikq,bb, Friederike Rangecc,dd, Simon M. Readeree, Rachna B. Reddyff, Aaron A. Sandelff, Laurie R. Santosx, Katrin Schumannd, Amanda M. Seedl, Kendra B. Sewalle, Rachael C. Shawq, Katie E. Slocombez, Yanjie Sugg, Ayaka Takimotot, Jingzhi Tana, Ruoting Taol, Carel P. van Schaikp, Zsófia Virányicc, Elisabetta Visalberghic, Jordan C. Wadew, Arii Watanabeq, Jane Widnessx, Julie K. Younghh, Thomas R. Zentallw, and Yini Zhaogg Departments of aEvolutionary Anthropology, aaNeurobiology, and mPsychology and Neuroscience, and bCenter for Cognitive Neuroscience, oDuke Institute for Brain Sciences, Duke University, Durham, NC 27708; cIstituto di Scienze e Tecnologie della Cognizione Consiglio Nazionale delle Ricerche, 00197 Rome, Italy; dDepartment of Developmental and Comparative Psychology, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany; eDepartment of Biology, Duke University, Durham, NC 27704; fInstituto de Neuroetologia, Universidad Veracruzana, Xalapa, CP 91190, Mexico; gResearch Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores University, Liverpool L3 3AF, United Kingdom; hCenter for Interdisciplinary Brain Sciences Research and iDepartment of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA 94305; jCenter for Animal Care Sciences, Smithsonian National Zoological Park, Washington, DC 20008; kDepartment of Brain and Cognitive Science and sDepartment of Comparative Medicine, Seneca Park Zoo, University of Rochester, Rochester, NY 14620; lDepartment of Psychology and Neuroscience, University of St. Andrews, St. Andrews KY16 9JP, Scotland; nDepartment of Psychology, University of Pennsylvania, Philadelphia, PA 19104; pAnthropological Institute and Museum, University of Zurich, 8057 Zurich, Switzerland; qDepartment of Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom; rDepartment of Psychology and uHelen Wills Neuroscience Institute, University of California, Berkeley, CA 94720; tGraduate School of Letters, Kyoto University, Kyoto 606-8501, Japan; Departments of vPsychology and hhWildland Resources, Utah State University, Logan, UT 84322; wDepartment of Psychology, University of Kentucky, Lexington, KY 40506; xDepartment of Psychology, Yale University, New Haven, CT 06520; yDepartamento Engenharia e Meio Ambiente, Universidade Federal da Paraiba, 58059-900, João Pessoa, Brazil; zDepartment of Psychology, University of York, Heslington, York YO10 5DD, United Kingdom; bbThink Elephants International, Stone Ridge, NY 12484; ccMesserli Research Institute, University of Veterinary Medicine Vienna, 1210 Vienna, Austria; ddWolf Science Center, A-2115 Ernstbrunn, Austria; eeDepartment of Biology, McGill University, Montreal, QC, Canada H3A 1B1; ffDepartment of Anthropology, University of Michigan, Ann Arbor, MI 48109; and ggDepartment of Psychology, Peking University, Beijing 100871, China COGNITIVE SCIENCES PSYCHOLOGICAL AND Edited by Jon H. Kaas, Vanderbilt University, Nashville, TN, and approved March 21, 2014 (received for review December 30, 2013) Cognition presents evolutionary research with one of its greatest how cognition varies across species, previous research has largely challenges. Cognitive evolution has been explained at the proxi- relied on proxies for cognition (e.g., brain size) or metaanalyses mate level by shifts in absolute and relative brain volume and at when testing hypotheses about cognitive evolution (76–92). The the ultimate level by differences in social and dietary complexity. lack of cognitive data collected with similar methods across large However, no study has integrated the experimental and phyloge- samples of species precludes meaningful species comparisons that netic approach at the scale required to rigorously test these ex- can reveal the major forces shaping cognitive evolution across planations. Instead, previous research has largely relied on various species, including humans (48, 70, 89, 93–98). measures of brain size as proxies for cognitive abilities. We ex- perimentally evaluated these major evolutionary explanations by Significance quantitatively comparing the cognitive performance of 567 indi- viduals representing 36 species on two problem-solving tasks Although scientists have identified surprising cognitive flexi- measuring self-control. Phylogenetic analysis revealed that abso- bility in animals and potentially unique features of human lute brain volume best predicted performance across species and psychology, we know less about the selective forces that favor accounted for considerably more variance than brain volume con- cognitive evolution, or the proximate biological mechanisms trolling for body mass. This result corroborates recent advances in underlying this process. We tested 36 species in two problem- evolutionary neurobiology and illustrates the cognitive consequen- solving tasks measuring self-control and evaluated the leading ces of cortical reorganization through increases in brain volume. hypotheses regarding how and why cognition evolves. Across Within primates, dietary breadth but not social group size was a species, differences in absolute (not relative) brain volume best strong predictor of species differences in self-control. Our results predicted performance on these tasks. Within primates, dietary implicate robust evolutionary relationships between dietary breadth, breadth also predicted cognitive performance, whereas social absolute brain volume, and self-control. These findings provide a sig- group size did not. These results suggest that increases in ab- nificant first step toward quantifying the primate cognitive phenome solute brain size provided the biological foundation for evo- and explaining the process of cognitive evolution. lutionary increases in self-control, and implicate species dif- ferences in feeding ecology as a potential selective pressure psychology | behavior | comparative methods | inhibitory control | favoring these skills. executive function Author contributions: E.L.M., B.H., and C.L.N. designed research; E.L.M., B.H., E.A., ince Darwin, understanding the evolution of cognition has F. Amici, R.C.A., F. Aureli, J. M. Baker, A.E.B., A.M.B., N.J.B., E.M.B., E.E.B., J.B., L.J.N.B., Sbeen widely regarded as one of the greatest challenges for J. M. Burkart, J.C., J.F.C., L.G.C., N.S.C., M.M.D., L.J.D., K.F., E.H., C.H., L.F.J., K.E.J., J.R.L., K.L.L., E.J.E.M., A.C.d.A.M., L.O., A.P., M.L.P., J.M.P., F.R., S.M.R., R.B.R., A.A.S., L.R.S., K.S., evolutionary research (1). Although researchers have identified A.M.S., K.B.S., R.C.S., K.E.S., Y.S., A.T., J.T., R.T., C.P.v.S., Z.V., E.V., J.C.W., A.W., J.W., J.K.Y., surprising cognitive flexibility in a range of species (2–40) and T.R.Z., and Y.Z. performed research; E.L.M. and C.L.N. analyzed data; and E.L.M., B.H., and potentially derived features of human psychology (41–61), we know C.L.N. wrote the paper. much less about the major forces shaping cognitive evolution (62– The authors declare no conflict of interest. 71). With the notable exception of Bitterman’s landmark studies This article is a PNAS Direct Submission. conducted several decades ago (63, 72–74), most research com- 1To whom correspondence should be addressed. E-mail: [email protected]. paring cognition across species has been limited to small taxonomic This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. samples (70, 75). With limited comparable experimental data on 1073/pnas.1323533111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1323533111 PNAS Early Edition | 1of9 Downloaded by guest on September 29, 2021 To address these challenges we measured cognitive skills for studies showing a positive correlation between a species’ typical self-control in 36 species of mammals and birds (Fig. 1 and group size and the neocortex ratio (80, 81, 85–87, 129, 142–145), Tables S1–S4) tested using the same experimental procedures, and cognitive differences between closely related species with different evaluated the leading hypotheses for the neuroanatomical under- group sizes (130, 137, 146, 147), and evidence for cognitive con- pinnings and ecological drivers of variance in animal cognition. At vergence between highly social species (26, 31, 148–150). The the proximate level, both absolute (77, 99–107) and relative brain foraging hypothesis posits that dietary complexity, indexed by field size (108–112) have been proposed as mechanisms supporting reports of dietary breadth and reliance on fruit (a spatiotemporally cognitive evolution. Evolutionary increases in brain size (both ab- distributed resource), was the primary driver of primate cognitive solute and relative) and cortical reorganization are hallmarks of the evolution (151–154). This hypothesis is supported by studies human lineage and are
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