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Brains, Innovations and Evolution in Birds and Primates
Open accessAbstract
Several comparative research programs have focused on the cognitive, life history and ecological traits that account for variation in brain size. We review one of these programs, a program that uses the reported frequency of behavioral innovation as an operational measure of cognition. In both birds and primates, innovation rate is positively correlated with the relative size of association areas in the brain, the hyperstriatum ventrale and neostriatum in birds and the isocortex and striatum in primates. Innovation rate is also positively correlated with the taxonomic distribution of tool use, as well as interspecific differences in learning. Some features of cognition have thus evolved in a remarkably similar way in primates and at least six phyletically-independent avian lineages. In birds, innovation rate is associated with the ability of species to deal with seasonal changes in the environment and to establish themselves in new regions, and it also appears to be related to the rate at which lineages diversify. Innovation rate provides a useful tool to quantify inter-taxon differences in cognition and to test classic hypotheses regarding the evolution of the brain.
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“Among birds, those that are larger-brained (corvids, parrots and owls) are also considered the most intelligent (Lefebvre et al., 2004).”
From The human brain in numbers: a linearly scaled-up primate brain (2009) · cites this paper as Lefebvre et al., 2004
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“In contrast, the encephalization hypothesis argues that an increase in brain volume relative to body size was of primary importance (108, 110, 111, 123).”
From The evolution of self-control. (2014) · cites this paper as [110]
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BackgroundVision, touch and object manipulation in Senegal parrots Poicephalus senegalus
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BackgroundInfluence of personality, age, sex, and estrous state on chimpanzee problem-solving success
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“The success of such innovative species in new environments (Lefebvre et al., 2004) may have allowed them to radiate rapidly into vacant niches.”
BackgroundInfluentialDisentangling the influences of multiple thalamic nuclei on prefrontal cortex and cognitive control
Phillips, J. M., Kambi, N. A., Redinbaugh, M. J., Mohanta, S., & Saalmann, Y. B. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.042 · Cited by 75
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“Measures of cognition are often correlated with one another (Lefebvre et al. 2004), suggesting that selection may act on some measure of general intelligence rather than on innovativeness per se.”
InfluentialTool-use in the brown bear (Ursus arctos)
Deecke, V. B. (2012) · Animal Cognition · doi:10.1007/s10071-012-0475-0 · Cited by 70
“…tool-use requires advanced cognitive and perceptual faculties, it is commonly used as an indicator for advanced physical intelligence (Emery and Clayton 2009; Seed and Byrne 2010), and has been linked to increased brain size in several taxa (e.g., Reader and Laland 2002; Lefebvre et al. 2004).”
Learning in non‐avian reptiles 40 years on: advances and promising new directions
Szabo, B., Noble, D. W. A., & Whiting, M. J. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12658 · Cited by 69
“(7) Responding to change Responding flexibly to environmental stimuli and adapting rapidly to change is important for survival in unpredictable environments (Lefebvre et al., 2004).”
BackgroundStereological estimation of total cell numbers in the human cerebral and cerebellar cortex
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“It has been proposed that neurons are responsible for the evolution of intelligence, in that species with larger brains and more neurons generally have a larger range and versatility of behaviors than those with smaller brains (Lefebvre et al., 2004; Sol et al., 2005).”
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“To control for such potential bias, we estimated research effort by counting the number of publications resulting from a keyword-based search using species’ names in Web of Science, as done in other studies (Nunn et al., 2003; Lefebvre et al., 2004; Garamszegi and Møller, 2012).”
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“…Reader, & Sol, 2004), impact upon species’ fitness and ecology (Giraldeau, Caraco, & Valone, 1994; Reader & Laland, 2002; van Schaik & Pradhan, 2003; Lefebvre et al., 2004), and potential utility as a proxy measure for cognitive ability and behavioural flexibility (Sol, Timmermans, & Lefebvre,…”
BackgroundThe metabolic costs of cognition
Jamadar, S. D., Behler, A., Deery, H. A., & Breakspear, M. J. (2025) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2024.11.010 · Cited by 81
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BackgroundResultInfluentialSocial Complexity as a Driver of Communication and Cognition
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“However, in taxa such as birds, sciurid mammals, toothed whales, and ungulates, aspects of social complexity such as the number of social alliances, social competition among groups, or the number of different social roles within a group may better describe the selective pressures of the social environment and thus be…”
BackgroundRelative Brain Size and Its Relation with the Associative Pallium in Birds
Sayol, F., Lefebvre, L., & Sol, D. (2016) · Brain Behavior and Evolution · doi:10.1159/000444670 · Cited by 70
“Comparative evidence suggests that taxonomic variation in the size of the primate isocortex and the avian associative pallium is associated with variation in a suite of correlated, domain-general cognitive abilities [Lefebvre et al., 2004; Reader et al., 2011] that include feeding innovation and tool use [Timmermans e…”
BackgroundSelf-citationHigh associative neuron numbers could drive cognitive performance in corvid species
Ströckens, F., Neves, K., Kirchem, S., Schwäb, C., Herculano‐Houzel, S., & Güntürkün, O. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25298 · Cited by 67
“…arcopallium/amygdala complex, and hippocampal formation noncorvids falls in linewith studies showing that the relative size of the mesopallium is increased in species with more flexible and innovative behavior (Lefebvre et al., 2002, 2004;Mehlhorn,Hunt et al., 2010; Timmermans et al., 2000).”
BackgroundEnvironmental and genetic determinants of innovativeness in a natural population of birds
Quinn, J. L., Cole, E. F., Reed, T. E., & Morand‐Ferron, J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0184 · Cited by 73
Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds
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“…size has been linked to a wide range of benefits, including increased survival, adaptability to novel environments, innovation propensity, variability of habitats occupied, invasiveness, and sociability (Lefebvre et al. 2004; Lefebvre and Sol 2008; Sol 2009; Sol et al. 2007, 2010; Lefebvre 2013).”
BackgroundThe temporal dependence of exploration on neotic style in birds
O’Hara, M., Mioduszewska, B., von Bayern, A. M. P., Auersperg, A. M. I., Bugnyar, T., Wilkinson, A., Huber, L., & Gajdon, G. K. (2017) · Scientific Reports · doi:10.1038/s41598-017-04751-0 · Cited by 65
Clayton, N. S., & Emery, N. J. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.020 · Cited by 64
Parrots have evolved a primate-like telencephalic-midbrain-cerebellar circuit
Gutiérrez‐Ibáñez, C., Iwaniuk, A. N., & WYLIE, D. R. W. (2018) · Scientific Reports · doi:10.1038/s41598-018-28301-4 · Cited by 68
Design principles of the human brain
Hofman, M. A. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00018-0 · Cited by 64
Explaining the Paradox of Neophobic Explorers: The Social Information Hypothesis
Forss, S., Koski, S. E., & van Schaik, C. P. (2017) · International Journal of Primatology · doi:10.1007/s10764-017-9984-7 · Cited by 63
“Moreover, as innovation rates are linked to large relative brain size (Deaner et al. 2007; Lefebvre et al. 2004; Overington et al. 2009; Reader et al. 2011), large-brained species are often thought to be driven to explore novelty.”
BackgroundCortés‐Avizanda, A., Almaraz, P., Carrete, M., Sánchez‐Zapata, J. A., Delgado‐Huertas, A., Hiraldo, F., & Donázar, J. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021016 · Cited by 65
“the ability of individuals to express distinct behaviours in different contexts through innovation and learning processes [13–14], might also influence the balance between migratory and resident strategies in environments with sharp seasonal changes [15].”
BackgroundIntegrating brain, behavior, and phylogeny to understand the evolution of sensory systems in birds
WYLIE, D. R. W., Gutiérrez‐Ibáñez, C., & Iwaniuk, A. N. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00281 · Cited by 63
Do Successful Invaders Exist? Pre-Adaptations to Novel Environments in Terrestrial Vertebrates
Sol, D. (2007) · Springer eBooks · doi:10.1007/978-3-540-36920-2_8 · Cited by 61
“Behavioral flexibility may aid establishment through, for example, the ready adoption of unexploited new food resources (Lefebvre et al. 2004), the adjustment of breeding to the prevailing environmental conditions (Arcese et al.”
BackgroundSelf-citationSpeciation, diversity, and Mode 1 technologies: The impact of variability selection
Grove, M. L. (2011) · Journal of Human Evolution · doi:10.1016/j.jhevol.2011.04.005 · Cited by 61
“Results linking behavioural flexibility to success in novel environments have been provided by Sol, Lefebvre, and colleagues in both birds and mammals (e.g., Sol and Lefebvre, 2000; Sol et al., 2002, 2005a,b, 2008; Lefebvre et al., 2004), and it is worthy of note that innovative propensity in each of these cases is po…”
BackgroundManger, P. R. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.041 · Cited by 60
Meulman, E. J. M., Seed, A. M., & Mann, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0050 · Cited by 58
“All of these have been shown to correlate with slow life histories and brain encephalization [68–71].”
BackgroundSocial carnivores outperform asocial carnivores on an innovative problem
Borrego, N., & Gaines, M. S. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.013 · Cited by 60
“Innovation is associated with cognitive complexity, and in primates, innovation is positively correlated with relative brain size (Lefebvre et al., 2004; Manrique, V€olter, & Call, 2013; Sol, Duncan, Blackburn, Cassey, & Lefebvre, 2005).”
BackgroundLew‐Levy, S., Milks, A. G., Lavi, N., Pope, S. M., & Friesem, D. E. (2020) · Evolutionary Human Sciences · doi:10.1017/ehs.2020.35 · Cited by 62
“Although innovative behaviours, including tool use and modification, have been described in other species (see Griffin & Guez, 2014 for review; Lefebvre et al., 2004; Overington et al., 2009; Reader et al., 2011), psychologists are often concerned with understanding the unique cognitive and…”
Farris, S. M. (2008) · Brain Behavior and Evolution · doi:10.1159/000139457 · Cited by 64
“…Behavioral ecologies that require complex sensory processing, decision-making, place memory and learning are associated with the evolution of larger brains and/ or higher brain regions in birds and mammals [Krebs et al., 1989; Reader and Laland, 2002; Lefebvre et al., 2004; Sol et al., 2005a].”
BackgroundInfluentialMartin, C., & Wainwright, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071164 · Cited by 58
“1) 24 44 [2 9, 77 ,1 23 ]”
BackgroundInnovation and behavioral flexibility in wild redfronted lemurs (Eulemur rufifrons)
Huebner, F., & Fichtel, C. (2015) · Animal Cognition · doi:10.1007/s10071-015-0844-6 · Cited by 58
“These studies revealed that innovation rates correlate with relative brain size in both taxa, with more innovative species having enlarged associative brain areas (Lefebvre et al. 1997, 2004; Timmermans et al. 2000; Reader and Laland 2002).”
BackgroundKolb, E. M., Rezende, E. L., Holness, L. F., Radtke, A., Lee, S. K., Obenaus, A., & Garland, T. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.076000 · Cited by 66
“A number of hypotheses have been generated to explain how selection may have driven changes in brain size (Francis, 1995; Barton and Harvey, 2000; de Winter and Oxnard, 2001; Hutcheon et al., 2002; Byrne and Corp, 2004; Lefebvre et al., 2004; Marino, 2005; Sol et al., 2005; Lefebvre and Sol, 2008; Rehkämper et al., 20…”
BackgroundAcrobatic Courtship Display Coevolves with Brain Size in Manakins (Pipridae)
Lindsay, W. R., Houck, J. T., Giuliano, C. E., & Day, L. B. (2015) · Brain Behavior and Evolution · doi:10.1159/000369244 · Cited by 60
Caldwell, C. A., & Whiten, A. (2004) · Animal Cognition · doi:10.1007/s10071-003-0192-9 · Cited by 57
“Combined with the relative difficulty of training marmoset demonstrators in the first place, this may provide tentative support for the proposals made by Reader and Lefebvre (2001) and Lefebvre et al. (2003) , that social learning emerges as part of a more general package of cognitive flexibility, predicted by factors…”
Backgroundvan Horik, J. O., & Emery, N. J. (2011) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.144 · Cited by 57
Life history, cognition and the evolution of complex foraging niches
Schuppli, C., Graber, S. M., Isler, K., & van Schaik, C. P. (2016) · Journal of Human Evolution · doi:10.1016/j.jhevol.2015.11.007 · Cited by 55
Sexual selection uncouples the evolution of brain and body size in pinnipeds
Fitzpatrick, J. L., Almbro, M., González‐Voyer, A., HAMADA, S., Pennington, C., Scanlan, J. C., & Kolm, N. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02520.x · Cited by 55
Distinct evolutionary patterns of brain and body size during adaptive radiation
Gonzalez-Voyer, A., Winberg, S., & Kolm, N. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00705.x · Cited by 52
“…the two traits, such as a scaling relationship of body surface area to brain volume (Jerison 1973), metabolic constraints limiting brain size (Martin 1981), or strong genetic correlations between brain and body size resulting in brain size evolving simply through a correlated response to…”
BackgroundGriffin, A. S. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0544 · Cited by 61
Finlay, B. L., Hinz, F. I., & Darlington, R. B. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0344 · Cited by 58
A meta-analysis of interindividual differences in innovation
Amici, F., Widdig, A., Lehmann, J., & Majolo, B. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.07.008 · Cited by 58
“Most of the first 57 studies on this topic reported anecdotal accounts of innovation in wild populations (e.g. birds: 58 Lefebvre et al., 1997, 2004; Sol et al., 2005a, 2005b; primates: Hosey et al., 1997; Lefebvre et al., 59 2004; Reader & Laland, 2001).”
Dunking behaviour in Carib grackles
Morand‐Ferron, J., Lefebvre, L., Reader, S. M., Sol, D., & Elvin, S. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2004.01.016 · Cited by 54
“When systematically collected, observations of this type have been useful in testing links between innovative cognition, neurobiology, ecology and evolution in birds and primates (Reader & Laland 2002, 2003; Lefebvre et al. 2004).”
Self-citationBrain Size and the Diversification of Body Size in Birds
Sol, D., & Price, T. D. (2008) · The American Naturalist · doi:10.1086/589461 · Cited by 52
Self-citation
Metadata
- Authors
- Lefebvre, L., Reader, S. M., & Sol, D.
- Affiliations
- McGill University (CA)
- Venue
- Brain, Behavior and Evolution
- Publisher
- S. Karger AG
- Published
- 2004
- Volume
- 63
- Issue
- 4
- Pages
- 233-246
- ISSN
- 0006-8977 (ISSN-L)
- 1421-9743
- OpenAlex
- W2112831044
- Cited by
- 666
- References
- 132
- Citations by year
- 2026: 15 · 2025: 22 · 2024: 22 · 2023: 28 · 2022: 35 · 2021: 57 · 2020: 28 · 2019: 26 · 2018: 38 · 2017: 41 · 2016: 57 · 2015: 35 · 2014: 31 · 2013: 24 · 2012: 43
- FWCI
- 3.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain Behavior and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Vocal Communication and Behavior
- Keywords
- behavioral innovation, brain size, cognition, birds, primates, hyperstriatum ventrale, neostriatum, neocortex, striatum, tool use, learning, seasonal adaptation, range expansion, diversification rates, brain evolution, comparative cognition
- MeSH terms
- Animals, Birds, Brain, Biological Evolution, Primates
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