Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling

There is a well‐established allometric relationship between brain and body mass in mammals. Deviation of relatively increased brain size from this pattern appears to coincide with enhanced cognitive abilities. To examine whether there is a phylogenetic structure to such episodes of changes in encephalization across mammals, we used phylogenetic techniques to analyse brain mass, body mass and encephalization quotient (EQ) among 630 extant mammalian species. Among all mammals, anthropoid primates and odontocete cetaceans have significantly greater variance in EQ, suggesting that evolutionary constraints that result in a strict correlation between brain and body mass have independently become relaxed. Moreover, ancestral state reconstructions of absolute brain mass, body mass and EQ revealed patterns of increase and decrease in EQ within anthropoid primates and cetaceans. We propose both neutral drift and selective factors may have played a role in the evolution of brain–body allometry.

[1]  K. Allen,et al.  Dietary quality and encephalization in platyrrhine primates , 2012, Proceedings of the Royal Society B: Biological Sciences.

[2]  M. Norconk,et al.  Relative Brain Size, Gut Size, and Evolution in New World Monkeys , 2011, Anatomical record.

[3]  Ana Navarrete,et al.  Energetics and the evolution of human brain size , 2011, Nature.

[4]  T. J. Robinson,et al.  Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification , 2011, Science.

[5]  S. Herculano‐Houzel Brains matter, bodies maybe not: the case for examining neuron numbers irrespective of body size , 2011, Annals of the New York Academy of Sciences.

[6]  Robin I. M. Dunbar,et al.  Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality , 2010, Proceedings of the National Academy of Sciences.

[7]  R. Barton,et al.  Placentation and Maternal Investment in Mammals , 2010, The American Naturalist.

[8]  Paul M. Thompson,et al.  On the Genetic Architecture of Cortical Folding and Brain Volume in Primates , 2022 .

[9]  R. Barton,et al.  Phylogeny and metabolic scaling in mammals. , 2010, Ecology.

[10]  N. Mundy,et al.  Reconstructing the ups and downs of primate brain evolution: implications for adaptive hypotheses and Homo floresiensis , 2010, BMC Biology.

[11]  C. Lovejoy,et al.  The Great Divides: Ardipithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes , 2009, Science.

[12]  C. Lovejoy,et al.  The Ardipithecus ramidus Skull and Its Implications for Hominid Origins , 2009, Science.

[13]  C. V. van Schaik,et al.  The Expensive Brain: a framework for explaining evolutionary changes in brain size. , 2009, Journal of human evolution.

[14]  T. Clutton‐Brock,et al.  Brain size and ecology in small mammals , 2009 .

[15]  J. J. Flynn,et al.  Brain-size evolution and sociality in Carnivora , 2009, Proceedings of the National Academy of Sciences.

[16]  Patrick R Hof,et al.  Von Economo Neurons in the Elephant Brain , 2009, Anatomical record.

[17]  B. Hart,et al.  Large brains and cognition: Where do elephants fit in? , 2008, Neuroscience & Biobehavioral Reviews.

[18]  R. Martin,et al.  Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. , 2008, Journal of human evolution.

[19]  J. Felsenstein Comparative Methods with Sampling Error and Within‐Species Variation: Contrasts Revisited and Revised , 2008, The American Naturalist.

[20]  C. Sherwood,et al.  A natural history of the human mind: tracing evolutionary changes in brain and cognition , 2008, Journal of anatomy.

[21]  Victoria Seher,et al.  Socially learned foraging behaviour in wild black bears, Ursus americanus , 2008, Animal Behaviour.

[22]  Robert E. Shadwick,et al.  Big gulps require high drag for fin whale lunge feeding , 2007 .

[23]  J. J. Flynn,et al.  THE EVOLUTION OF ENCEPHALIZATION IN CANIFORM CARNIVORANS , 2007, Evolution; international journal of organic evolution.

[24]  Y. Attia,et al.  A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae) , 2007, Proceedings of the National Academy of Sciences.

[25]  L. Lefebvre,et al.  Cetaceans Have Complex Brains for Complex Cognition , 2007, PLoS biology.

[26]  Andrew Whiten,et al.  The evolution of animal ‘cultures’ and social intelligence , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[28]  C. V. van Schaik,et al.  Metabolic costs of brain size evolution , 2006, Biology Letters.

[29]  R. Barton Primate brain evolution: Integrating comparative, neurophysiological, and ethological data , 2006 .

[30]  G. Tartarelli,et al.  Trajectories and Constraints in Brain Evolution in Primates and Cetaceans , 2006 .

[31]  J. Shoshani,et al.  Elephant brain Part I: Gross morphology, functions, comparative anatomy, and evolution , 2006, Brain Research Bulletin.

[32]  J. J. Flynn,et al.  Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record. , 2006, Systematic biology.

[33]  K. Safi,et al.  Bigger is not always better: when brains get smaller , 2005, Biology Letters.

[34]  J. Niven Brain Evolution: Getting Better All the Time? , 2005, Current Biology.

[35]  G. Roth,et al.  Evolution of the brain and intelligence , 2005, Trends in Cognitive Sciences.

[36]  D. Kruska On the Evolutionary Significance of Encephalization in Some Eutherian Mammals: Effects of Adaptive Radiation, Domestication, and Feralization , 2005, Brain, Behavior and Evolution.

[37]  D. McShea,et al.  Origin and evolution of large brains in toothed whales. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[38]  Kate E. Jones,et al.  Affording Larger Brains: Testing Hypotheses of Mammalian Brain Evolution on Bats , 2004, The American Naturalist.

[39]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[40]  J. M. Hutcheon,et al.  A Comparative Analysis of Brain Size in Relation to Foraging Ecology and Phylogeny in the Chiroptera , 2002, Brain, Behavior and Evolution.

[41]  L. Marino Convergence of Complex Cognitive Abilities in Cetaceans and Primates , 2002, Brain, Behavior and Evolution.

[42]  M. F. Williams Primate encephalization and intelligence. , 2002, Medical hypotheses.

[43]  K. Laland,et al.  Social intelligence, innovation, and enhanced brain size in primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  K. Milton Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae , 1998, International Journal of Primatology.

[45]  Lori Marino,et al.  A Comparison of Encephalization between Odontocete Cetaceans and Anthropoid Primates , 1998, Brain, Behavior and Evolution.

[46]  M. Pagel Inferring evolutionary processes from phylogenies , 1997 .

[47]  R. Martin Scaling of the Mammalian Brain: the Maternal Energy Hypothesis , 1996 .

[48]  J. Downing,et al.  CRC Handbook of Mammalian Body Masses , 1995 .

[49]  L. Aiello,et al.  The Expensive-Tissue Hypothesis: The Brain and the Digestive System in Human and Primate Evolution , 1995, Current Anthropology.

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

[51]  W. Maddison Squared-Change Parsimony Reconstructions of Ancestral States for Continuous-Valued Characters on a Phylogenetic Tree , 1991 .

[52]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[53]  J. P. Hickie Relative Brain Size in Marine Mammals , 1986, The American Naturalist.

[54]  E. Armstrong Relative brain size in monkeys and prosimians. , 1985, American journal of physical anthropology.

[55]  H. J. Jerison Animal intelligence as encephalization. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[57]  Bernard Wood,et al.  Food Acquisition and Processing in Primates , 1984 .

[58]  H. Mchenry THE PATTERN OF HUMAN EVOLUTION: Studies on Bipedalism, Mastication, and Encephalization , 1982 .

[59]  R. Martin,et al.  Relative brain size and basal metabolic rate in terrestrial vertebrates , 1981, Nature.

[60]  R. Bronson Brain weight‐body weight relationships in 12 species of nonhuman primates , 1981 .

[61]  D. Chivers,et al.  Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet , 1980, Journal of morphology.

[62]  T. Clutton‐Brock,et al.  Brain size and ecology in small mammals and primates. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[63]  L. Radinsky,et al.  Evolution of Brain Size in Carnivores and Ungulates , 1978, The American Naturalist.

[64]  H. J. Jerison,et al.  Evolution of the Brain and Intelligence , 1973 .

[65]  S. Gould,et al.  Size and Scaling in Human Evolution , 1974, Science.

[66]  T. Ohta Mutational pressure as the main cause of molecular evolution and polymorphism , 1974, Nature.

[67]  T. Ohta Slightly Deleterious Mutant Substitutions in Evolution , 1973, Nature.

[68]  S. Gould Geometric Similarity in Allometric Growth: A Contribution to the Problem of Scaling in the Evolution of Size , 1971, The American Naturalist.

[69]  J. Huxley Relative growth and form transformation , 1950, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[70]  P. Pye-Smith The Descent of Man, and Selection in Relation to Sex , 1871, Nature.

[71]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[72]  P. Hedrick Genetics of Population , 2011 .

[73]  Chet C. Sherwood,et al.  Neuronal morphology in the African elephant (Loxodonta africana) neocortex , 2010, Brain Structure and Function.

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

[75]  Daniel S. Falster,et al.  User's guide to SMATR : standardised major axis tests and routines version 2.0, copyright 2006 , 2006 .

[76]  Tomoko Ohta,et al.  Evolution by nearly-neutral mutations , 2004, Genetica.

[77]  Robin I. M. Dunbar,et al.  Neocortex size predicts group size in carnivores and some insectivores , 1998 .

[78]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[79]  D. Kruska Mammalian Domestication and its Effect on Brain Structure and Behavior , 1988 .

[80]  Robert D. Martin,et al.  Body Size, Brain Size and Feeding Strategies , 1984 .

[81]  R. Holloway,,et al.  The Relativity of Relative Brain Measures and Hominid Mosaic Evolution , 1982 .

[82]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[83]  R. Cutler Evolution of longevity in ungulates and carnivores. , 1979, Gerontology.

[84]  R. Nowak,et al.  Walker's mammals of the world , 1968 .

[85]  J. Huxley A discussion on the measurement of growth and form; relative growth and form transformation. , 1950, Proceedings of the Royal Society of London. Series B, Biological sciences.

[86]  C. Darwin The descent of man, and Selection in relation to sex, Vol 1. , 1871 .