The Expensive Brain: A framework for explaining evolutionary changes in brain size
Open accessAbstract
To explain variation in relative brain size among homoiothermic vertebrates, we propose the Expensive Brain hypothesis as a unifying explanatory framework. It claims that the costs of a relatively large brain must be met by any combination of increased total energy turnover or reduced energy allocation to another expensive function such as digestion, locomotion, or production (growth and reproduction). Focusing on the energetic costs of brain enlargement, a comparative analysis of the largest mammalian sample assembled to date shows that an increase in brain size leads to larger neonates among all mammals and a longer period of immaturity among monotokous precocial species, but not among the polytokous altricial ones, who instead reduce their litter size. Relatively large brained mammals, altricial and precocial, also show reduced annual fertility rates as compared to their smaller brained relatives, but allomaternal energy inputs allow some cooperatively breeding altricial carnivores to produce even more offspring in a shorter time despite having a relatively large brain. Thus, the Expensive Brain framework explains why brain size is linked to life history pace in some, but not all mammalian lineages. This framework encompasses other hypotheses of energetic constraints on brain size variation and is also compatible with the Brain Malnutrition Risk hypothesis, but the absence of a mammal-wide correlation between brain size and immature period argues against the Needing-to-Learn explanation for slower development among large brained mammals.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Increased brain size in socially complex species may be associated with reduced brain operation costs.
“Therefore, increased brain size in socially complex species may be associated with reduced brain operation costs, contrasting with the assumption that increased brain size increases metabolic costs (Aiello and Wheeler, 1995;Isler and van Schaik, 2009).”
From When and Why Did Human Brains Decrease in Size? A New Change-Point Analysis and Insights From Brain Evolution in Ants (2021) · cites this paper as Isler and van Schaik, 2009
An accelerated metabolic rate in the hominin lineage would be consistent with humans' high rate of reproduction and large brains relative to other apes.
“An accelerated metabolic rate in the hominin lineage would be consistent with humans’ high rate of reproduction (7) and large brains (9, 11) relative to other apes.”
From Metabolic adaptation for low energy throughput in orangutans. (2010) · cites this paper as [11]
Cites
Phylogenies and the Comparative Method
Felsenstein, J. (1985) · The American Naturalist · doi:10.1086/284325 · Cited by 9,793 · see citing works
Mammal Species of the World: A Taxonomic and Geographic Reference
Schmid, R., Wilson, D. E., & Reeder, D. M. (1993) · Taxon · doi:10.2307/1223169 · Cited by 5,384 · see citing works
The comparative method in evolutionary biology
(1992) · Choice Reviews Online · doi:10.5860/choice.29-5104 · Cited by 4,926 · see citing works
The Comparative Method in Evolutionary Biology
Harvey, P. H., & Pagel, M. D. (1991) · doi:10.1093/oso/9780198546412.001.0001 · Cited by 4,337 · see citing works
Nowak, R. (2018) · doi:10.1353/book.59141 · Cited by 4,102 · see citing works
Mammal species of the world: a taxonomic and geographic reference
(2006) · Choice Reviews Online · doi:10.5860/choice.44-1281 · Cited by 2,996 · see citing works
The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution
Aiello, L. C., & Wheeler, P. (1995) · Current Anthropology · doi:10.1086/204350 · Cited by 2,291 · see citing works
Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts
Garland, T., Harvey, P. H., & Ives, A. R. (1992) · Systematic Biology · doi:10.1093/sysbio/41.1.18 · Cited by 2,151 · see citing works
The delayed rise of present-day mammals
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007) · Nature · doi:10.1038/nature05634 · Cited by 2,082 · see citing works
Cellular energy utilization and molecular origin of standard metabolic rate in mammals
Rolfe, D. F., & Brown, G. C. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.3.731 · Cited by 2,021 · see citing works
Evolution of the Brain and Intelligence.
Radinsky, L., & Jerison, H. J. (1975) · Evolution · doi:10.2307/2407154 · Cited by 1,974 · see citing works
Dunbar, R., & Shultz, S. (2007) · Science · doi:10.1126/science.1145463 · Cited by 1,580 · see citing works
Linked Regularities in the Development and Evolution of Mammalian Brains
Finlay, B. L., & Darlington, R. B. (1995) · Science · doi:10.1126/science.7777856 · Cited by 1,217 · see citing works
Purvis, A., & Rambaut, A. (1995) · Computer applications in the biosciences · doi:10.1093/bioinformatics/11.3.247 · Cited by 1,126 · see citing works
Big brains, enhanced cognition, and response of birds to novel environments
Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P., & Lefebvre, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408145102 · Cited by 917 · see citing works
Mammalian basal metabolic rate is proportional to body mass <sup>2/3</sup>
White, C. R., & Seymour, R. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0436428100 · Cited by 720 · see citing works
Relative brain size and basal metabolic rate in terrestrial vertebrates
Martin, R. D. (1981) · Nature · doi:10.1038/293057a0 · Cited by 711 · see citing works
Human Growth: A Comprehensive Treatise
Carithers, H. A. (1987) · JAMA · doi:10.1001/jama.1987.03390050112036 · Cited by 687 · see citing works
Encyclopedia of Biostatistics.
Kemp, C. D., Armitage, P., & Coulton, T. (1998) · Biometrics · doi:10.2307/2533871 · Cited by 674 · see citing works
Brains, Innovations and Evolution in Birds and Primates
Lefebvre, L., Reader, S. M., & Sol, D. (2004) · Brain, Behavior and Evolution · doi:10.1159/000076784 · Cited by 666 · see citing works
A method for the analysis of comparative data
Pagel, M. D. (1992) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80637-x · Cited by 661 · see citing works
Mink, J. W., Blumenschine, R. J., & Adams, D. B. (1981) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1981.241.3.r203 · Cited by 597 · see citing works
Deaner, R. O., Isler, K., Burkart, J., & van Schaik, C. (2007) · Brain, Behavior and Evolution · doi:10.1159/000102973 · Cited by 549 · see citing works
Self-citationMCDANIEL, M. (2005) · Intelligence · doi:10.1016/j.intell.2004.11.005 · Cited by 527 · see citing works
On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance
García‐Berthou, E. (2001) · Journal of Animal Ecology · doi:10.1046/j.1365-2656.2001.00524.x · Cited by 511 · see citing works
Sacher, G. A., & Staffeldt, E. F. (1974) · The American Naturalist · doi:10.1086/282938 · Cited by 451 · see citing works
The Zoogeography of Mammalian Basal Metabolic Rate
Lovegrove, B. G. (2000) · The American Naturalist · doi:10.1086/303383 · Cited by 430 · see citing works
Lovegrove, B. G. (2003) · Journal of Comparative Physiology B · doi:10.1007/s00360-002-0309-5 · Cited by 350 · see citing works
Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set
Isler, K., Christopher Kirk, E., Miller, J. M. A., Albrecht, G. A., Gelvin, B. R., & Martin, R. D. (2008) · Journal of Human Evolution · doi:10.1016/j.jhevol.2008.08.004 · Cited by 320 · see citing works
Self-citationMetabolic costs of brain size evolution
Isler, K., & van Schaik, C. P. (2006) · Biology Letters · doi:10.1098/rsbl.2006.0538 · Cited by 317 · see citing works
Self-citationThe Origin AND Diversification Of Language
Swadesh, M. (2017) · Routledge eBooks · doi:10.4324/9781315133621 · Cited by 304 · see citing works
Applications of Phylogenetically Independent Contrasts: A Mixed Progress Report
Ricklefs, R. E., & Starck, J. M. (1996) · Oikos · doi:10.2307/3545598 · Cited by 289 · see citing works
Relative Brain Size and Metabolism in Mammals
Armstrong, E. (1983) · Science · doi:10.1126/science.6407108 · Cited by 252 · see citing works
Comparative Primate Socioecology
(1999) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542466 · Cited by 248 · see citing works
Energy metabolism, brain size and longevity in mammals.
Hofman, M. A. (1983) · The Quarterly Review of Biology · doi:10.1086/413544 · Cited by 241 · see citing works
A comment on phylogenetic correction
Rohlf, F. J. (2006) · Evolution · doi:10.1554/05-550.1 · Cited by 239 · see citing works
The Origin and Diversification of Language
Fitch, W. T. (1999) · American Anthropologist · doi:10.1525/aa.1999.101.4.864 · Cited by 232 · see citing works
Scaling of the Mammalian Brain: the Maternal Energy Hypothesis
Martin, R. D. (1996) · Physiology · doi:10.1152/physiologyonline.1996.11.4.149 · Cited by 226 · see citing works
Primate life histories and socioecology
Kappeler, P. M., & Pereira, M. E. (2003) · Cited by 223 · see citing works
Big-brained birds survive better in nature
Sol, D., Székely, T., Liker, A., & Lefebvre, L. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3765 · Cited by 223 · see citing works
Costs of encephalization: the energy trade-off hypothesis tested on birds
Isler, K., & van Schaik, C. (2006) · Journal of Human Evolution · doi:10.1016/j.jhevol.2006.03.006 · Cited by 217 · see citing works
Self-citationBrain weight and life-span in primate species.
Allman, J. M., McLaughlin, T., & Hakeem, A. Y. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.1.118 · Cited by 212 · see citing works
Barrickman, N. L., Bastian, M. L., Isler, K., & van Schaik, C. P. (2007) · Journal of Human Evolution · doi:10.1016/j.jhevol.2007.08.012 · Cited by 211 · see citing works
Self-citationEvolutionary Anatomy of the Primate Cerebral Cortex
(2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511897085 · Cited by 196 · see citing works
White, C. R., & Seymour, R. S. (2004) · Physiological and Biochemical Zoology · doi:10.1086/425186 · Cited by 183 · see citing works
Problems of allometric scaling analysis: examples from mammalian reproductive biology
Martin, R. D., Genoud, M., & Hemelrijk, C. K. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01566 · Cited by 166 · see citing works
Pontzer, H., & Wrangham, R. W. (2004) · Journal of Human Evolution · doi:10.1016/j.jhevol.2003.12.006 · Cited by 163 · see citing works
Evolution of the Brain and Intelligence
Gould, S. J. (1974) · Science · doi:10.1126/science.185.4149.400.a · Cited by 160 · see citing works
An optimum body size for mammals? Comparative evidence from bats
Jones, K. E., & Purvis, A. (1997) · Functional Ecology · doi:10.1046/j.1365-2435.1997.00149.x · Cited by 150 · see citing works
Socioecology and the evolution of primate reproductive rates
Ross, C., & Jones, K. E. (1999) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542466.007 · Cited by 148 · see citing works
HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING
Pagel, M. D., & Harvey, P. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb02513.x · Cited by 145 · see citing works
Brain Size and Its Relation to the Rate of Metabolism in Mammals
McNab, B. K., & Eisenberg, J. F. (1989) · The American Naturalist · doi:10.1086/284907 · Cited by 143 · see citing works
Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin)
Bauchinger, U., Wohlmann, A., & Biebach, H. (2005) · Zoology · doi:10.1016/j.zool.2005.03.003 · Cited by 132 · see citing works
Karasov, W. H., Pinshow, B., Starck, J. M., & Afik, D. (2004) · Physiological and Biochemical Zoology · doi:10.1086/381465 · Cited by 110 · see citing works
Why are there so few smart mammals (but so many smart birds)?
Isler, K., & van Schaik, C. P. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0469 · Cited by 108 · see citing works
Self-citationDietary constraints on encephalization in primates
Fish, J. L., & Lockwood, C. A. (2003) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10136 · Cited by 105 · see citing works
Affording Larger Brains: Testing Hypotheses of Mammalian Brain Evolution on Bats
Jones, K. E., & MacLarnon, A. M. (2004) · The American Naturalist · doi:10.1086/421334 · Cited by 105 · see citing works
Phylogenetically independent comparisons and primate phylogeny
Purvis, A., & Webster, A. J. (1999) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542466.005 · Cited by 100 · see citing works
The evolutionary ecology of the primate brain
Barton, R. A. (1999) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542466.010 · Cited by 98 · see citing works
Primate Life Histories and Socioecology
Meikle, D. B. (2003) · Ethology · doi:10.1046/j.1439-0310.2003.00950.x · Cited by 96 · see citing works
Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.
Iwaniuk, A. N., Nelson, J. E., & Pellis, S. M. (2001) · Journal of comparative psychology · doi:10.1037/0735-7036.115.1.29 · Cited by 93 · see citing works
Problems of ontogeny and phylogeny in brain-size evolution
Deacon, T. W. (1990) · International Journal of Primatology · doi:10.1007/bf02192870 · Cited by 80 · see citing works
(2004) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542299 · Cited by 75 · see citing works
The Evolution of thought: evolutionary origins of great ape intelligence
(2005) · Choice Reviews Online · doi:10.5860/choice.42-2813 · Cited by 61 · see citing works
In defense of the Expensive Tissue Hypothesis
Aiello, L. C., Bates, N., & Joffe, T. H. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511897085.006 · Cited by 59 · see citing works
How Mammals Produce Large-Brained Offspring
Pagel, M. D., & Harvey, P. (1988) · Evolution · doi:10.2307/2408910 · Cited by 48 · see citing works
In the mind's eye : multidisciplinary approaches to the evolution of human cognition
Nowell, A. (2001) · International Monographs in Prehistory eBooks · Cited by 19 · see citing works
Life histories and the evolution of large brain size in great apes
Ross, C. (2004) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542299.011 · Cited by 16 · see citing works
Evolutionary anatomy of the primate cerebral cortex
Keverne, B. (2001) · American Journal of Human Biology · doi:10.1002/ajhb.10022 · Cited by 13 · see citing works
Künkele, J., Kraus, C., & Trillmich, F. (2005) · Physiological and Biochemical Zoology · doi:10.1086/425197 · Cited by 12 · see citing works
Welche quantitativen Beziehungen bestehen bei Saugetieren zwischen Schadelkapazitat und Hirnvolumen?
Röhrs, M., & Ebinger, P. (2001) · Biodiversity Heritage Library (Smithsonian Institution) · doi:10.5281/zenodo.13526636 · Cited by 9 · see citing works
Kuzawa, C. W. (1998) · doi:10.1002/(sici)1096-8644(1998)107:27+
Flagged first, then by citations
Cited by
Sorted by citations
The evolution of self-control.
MacLean, E. L., Hare, B., Nunn, C. L., Addessi, E., Amici, F., Anderson, R. C., Aureli, F., Baker, J. M., Bania, A. E., Barnard, A. M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323533111 · Cited by 819 · see citing works
Self-citationCooperative Breeding and Human Cognitive Evolution
Burkart, J. M., Hrdy, S. B., & Van Schaik, C. P. (2009) · Evolutionary Anthropology: Issues, News, and Reviews · doi:10.1002/evan.20222 · Cited by 646 · see citing works
Energetics and the evolution of human brain size
Navarrete, A., van Schaik, C. P., & Isler, K. (2011) · Nature · doi:10.1038/nature10629 · Cited by 469 · see citing works
Self-citationHow does cognition evolve? Phylogenetic comparative psychology
MacLean, E. L., Matthews, L. J., Hare, B. A., Nunn, C. L., Anderson, R. C., Aureli, F., Brannon, E. M., Call, J., Drea, C. M., Emery, N. J., et al. (2012) · Animal Cognition · doi:10.1007/s10071-011-0448-8 · Cited by 260 · see citing works
Self-citationBODDY, A. M., McGOWEN, M. R., SHERWOOD, C. C., GROSSMAN, L. I., GOODMAN, M., & WILDMAN, D. E. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02491.x · Cited by 207 · see citing works
Maternal investment, life histories and the costs of brain growth in mammals
Barton, R. A., & Capellini, I. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019140108 · Cited by 208 · see citing works
Brain Plasticity and Human Evolution
Sherwood, C. C., & Gómez-Robles, A. (2017) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-102215-100009 · Cited by 170 · see citing works
Brain ontogeny and life history in Pleistocene hominins
Hublin, J.-J., Neubauer, S., & Gunz, P. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0062 · Cited by 173 · see citing works
Primate energy expenditure and life history
Pontzer, H., Raichlen, D. A., Gordon, A. D., Schroepfer-Walker, K. K., Hare, B., O’Neill, M. C., Muldoon, K. M., Dunsworth, H. M., Wood, B. M., Isler, K., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316940111 · Cited by 165 · see citing works
Self-citationIsler, K., & van Schaik, C. P. (2012) · Current Anthropology · doi:10.1086/667623 · Cited by 144 · see citing works
Self-citationPaying the brain's energy bill
Padamsey, Z., & Rochefort, N. L. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102668 · Cited by 114 · see citing works
Metabolic adaptation for low energy throughput in orangutans.
Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C., & Wich, S. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001031107 · Cited by 105 · see citing works
DeSilva, J. M., Traniello, J. F. A., Claxton, A. G., & Fannin, L. D. (2021) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2021.742639 · Cited by 86 · see citing works
“Therefore, increased brain size in socially complex species may be associated with reduced brain operation costs, contrasting with the assumption that increased brain size increases metabolic costs (Aiello and Wheeler, 1995; Isler and van Schaik, 2009).”
BackgroundPlacentation and Maternal Investment in Mammals
Capellini, I., Venditti, C., & Barton, R. A. (2011) · The American Naturalist · doi:10.1086/657435 · Cited by 81 · see citing works
Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis
Miller, I. F., Barton, R. A., & Nunn, C. L. (2019) · eLife · doi:10.7554/elife.41250 · Cited by 70 · see citing works
Kuipers, R. S., Joordens, J. C. A., & Muskiet, F. A. J. (2012) · Nutrition Research Reviews · doi:10.1017/s0954422412000017 · Cited by 43 · see citing works
Brain Size Growth and Life History in Human Evolution
Leigh, S. R. (2012) · Evolutionary Biology · doi:10.1007/s11692-012-9168-5 · Cited by 43 · see citing works
Macho, G. A., & Lee-Thorp, J. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102794 · Cited by 41 · see citing works
Being fat and smart: A comparative analysis of the fat-brain trade-off in mammals
Heldstab, S. A., van Schaik, C. P., & Isler, K. (2016) · Journal of Human Evolution · doi:10.1016/j.jhevol.2016.09.001 · Cited by 37 · see citing works
Self-citationBalcarcel, A. M., Veitschegger, K., Clauss, M., & Sánchez-Villagra, M. R. (2021) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2021.0813 · Cited by 35 · see citing works
Allomaternal care, brains and fertility in mammals: who cares matters
Heldstab, S. A., Isler, K., Burkart, J. M., & van Schaik, C. P. (2019) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-019-2684-x · Cited by 29 · see citing works
Self-citation
- Authors
- Isler, K., & van Schaik, C. P.
- Affiliations
- University of Zurich (CH)
- Corresponding author
- Isler, Karin
- ORCID
- Isler, Karin
- Venue
- Journal of Human Evolution
- Publisher
- Elsevier BV
- Published
- 2009-10
- Volume
- 57
- Issue
- 4
- Pages
- 392-400
- ISSN
- 0047-2484 (ISSN-L)
- OpenAlex
- W2061008199
- Cited by
- 474
- References
- 72
- Citations by year
- 2026: 33 · 2025: 33 · 2024: 26 · 2023: 32 · 2022: 38 · 2021: 33 · 2020: 36 · 2019: 26 · 2018: 27 · 2017: 28 · 2016: 38 · 2015: 25 · 2014: 24 · 2013: 12 · 2012: 27
- FWCI
- 21.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.zora.uzh.ch
- Licence
- Locations
- Journal of Human Evolution (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- brain size evolution, energy allocation, precociality, altriciality, litter size, fertility rate, allomaternal care, cooperative breeding, developmental delay, vertebrate brain evolution
- MeSH terms
- Aging, Animals, Brain, Breeding, Biological Evolution, Female, Growth, Humans, Learning, Litter Size, Male, Mammals, Organ Size, Phylogeny, Primates, Least-Squares Analysis, Malnutrition
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review