Cited by 112Primate Behavior and EcologyEvolution and Paleontology StudiesMorphological variations and asymmetry

Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution

Open access
Smaers, J. B., Soligo, C.·2013·Proceedings of the Royal Society B: Biological Sciences

Abstract

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.

AI snapshot

Written from the paper’s full text.

TL;DR

Across 17 anthropoid primates, mosaic brain reorganization explains more neural diversity than changes in relative brain size, with seven principal components explaining up to 90.4% of variation. Great apes and humans show derived investment in prefrontal white matter, prefronto-striatal, and cortico-cerebellar systems inferred to originate in the ape ancestral lineage around 30–20 Ma.

Key findings

  • Phylogenetic PCA of relative brain size plus 20 brain structures/areas yielded seven principal components explaining up to 90.4% of neural structure variation. PC1 was dominated by relative brain size and accounted for 25.8%; subsequent size-independent PCs were PC2 prefrontal white matter (18.7%), PC3 hippocampal formation (14.7%), PC4 prefronto-striatal formation (12.7%), PC5 paleocortex (7.7%), PC6 motor execution structures (6.0%), and PC7 motor learning structures (4.6%).
  • Across more than 40 Myr of anthropoid evolution, mosaic changes contributed more to explaining neural diversity than changes in relative brain size.
  • Great apes and humans were differentiated by joint investment in prefrontal white matter, prefronto-striatal, and cortico-cerebellar systems alongside increased absolute brain size; this pattern was inferred to originate in the ape ancestral lineage approximately 30–20 Ma.
  • Some mosaic patterns showed significantly increased variation in lineages where brain size decreased: PC2 (F = 0.0037, p < 0.0001), PC3 (F = 0.0066, p < 0.0002), and PC6 (F = 0.0395, p = 0.0067).

Methods

  • Sample: 17 anthropoid primate species including humans; brain structure volumes came from serially sectioned post-mortem brains following published protocols and from the literature; the phylogeny was taken from the 10kTrees project, v. 3.
  • Analyses: phylogenetic reduced major axis regressions with a likelihood-fitted lambda model controlled brain size for body size and brain structure size for brain size; residuals were entered into a phylogenetically controlled principal components analysis; PC scores were used to estimate ancestral states and lineage-specific evolutionary rates via a variable rates method based on an adaptive peak model.
  • Rate variation was compared between lineages indicating brain size increase (minimum rate of 0.1) and lineages indicating brain size decrease (maximum rate of −0.1) using an F-test for equality of variance; model accuracy was checked against fossil brain size estimates at three phylogenetic locations.

Limitations

  • The paper does not include a dedicated limitations section.
  • Evident from the text: the sample is limited to 17 anthropoid species, so broad claims about anthropoid brain evolution rest on this taxon sample; data are post-mortem/histological and literature-derived, which may constrain structure coverage and comparability.
  • Evident from the text: the variable rates method’s accuracy was tested only by comparing estimated ancestral brain size to fossil estimates at three nodes (e.g., *Australopithecus afarensis* fossil estimate 434cc versus method estimate 385cc), not for PC scores or individual brain structures; the authors also note that further work should investigate other heteromodal association areas.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1098/rspb.2013.0269

Cites

75 of 75 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 79 cited sources checked · 0 supported · 0 flagged

  • Findingnone given
    § 3. Discussion

    The origin of the great ape grade shift in prefrontal white matter evolution is inferred to date back to the dawn of the ape radiation (at least 20 Ma).

    “The origin of the great ape grade shift in prefrontal white matter evolution is inferred to date back to the dawn of the ape radiation (at least 20 Ma).”
    Quote in the paperSubstantial claim
  • Findingown data
    § 3. Discussion

    Across more than 40 Myr of anthropoid evolution, different neocortical and cerebellar areas varied in their contributions to different mosaic patterns.

    “We further find that, across more than 40 Myr of anthropoid evolution, different neocortical and cerebellar areas varied in their contributions to different mosaic patterns.”
    Quote in the paperSubstantial claim
  • Findingown data
    § 3. Discussion

    The principal component that contributes most to explaining evolutionary changes in primate brain reorganization indicates high loadings for prefrontal white matter.

    “The principal component that we find to contribute most to explaining evolutionary changes in primate brain reorganization indicates high loadings for prefrontal white matter (table 1).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    Different mosaic patterns are differentially selected for when brains increase or decrease in size.

    “and different mosaic patterns are differentially selected for when brains increase or decrease in size.”
    Quote in the paperSubstantial claim
  • Findingown data
    § 2. Results

    PC3 (14.7%) involves the hippocampal formation (hippocampus and entorhinal cortex).

    “PC3 (14.7%) involves the hippocampal formation (hippocampus and entorhinal cortex)”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 20
  • May combine two claims. 20
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data
    § 2. Results

    PC5 (7.7%) involves the paleocortex.

    “PC5 (7.7%) the paleocortex”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data
    § 2. Results

    Principal component 1 (PC1) is dominated by variation in relative brain size and accounts for up to 25.8 per cent of overall variation in brain evolution.

    “Principal component 1 (PC1) is dominated by variation in relative brain size and accounts for up to 25.8 per cent of overall variation in brain evolution (table 1).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § 3. Discussion

    Phylogenetic mapping of PC2 scores and brain size shows that great apes stand out in their combined investment in both prefrontal white matter and absolute brain size, in that prefrontal white matter keeps track with a substantial increase in brain size, with humans at the extreme of this pattern.

    “Phylogenetic mapping of PC2 scores and brain size shows that great apes stand out in their combined investment in both prefrontal white matter and absolute brain size, in that prefrontal white matter keeps track with a substantial increase in brain size, with humans at the extreme of this pattern (figure 1a).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given
    § 4. Material and methods

    The sample includes brain size values spanning 40 orders of magnitude (32.8cc for Pithecia monachus and 39.7 for Miopithecus talapoin compared with 1418.9cc for our sample of humans).

    “Considering that our sample includes brain size values spanning 40 orders of magnitude (32.8cc for the New World monkey Pithecia monachus and 39.7 for the Old World monkey Miopithecus talapoin compared with 1418.9cc for our sample of humans)”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data
    § 3. Discussion

    The hippocampus-entorhinal formation does not indicate a clade-specific pattern in combination with an emphasis on absolute brain size, but displays particular variation in lineages where brain size has decreased.

    “The hippocampus–entorhinal formation does not indicate a clade-specific pattern in combination with an emphasis on absolute brain size (see electronic supplementary material, S2), but displays particular variation in lineages where brain size has decreased (figure 2).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § 3. Discussion

    Phylogenetic mapping of PC6 and PC7 reveals opposite patterns of investment across species with a joint investment in the cortico-cerebellar system and absolute brain size separating the ape from the monkey radiation between 30 and 20 Ma.

    “Phylogenetic mapping of PC6 and PC7 reveals opposite patterns of investment across species with a joint investment in the cortico-cerebellar system and absolute brain size separating the ape from the monkey radiation between 30 and 20 Ma (figure 1c).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § 3. Discussion

    Great apes combine increased investment in the cortico-cerebellar system with a decreased investment in the descending motor pathway.

    “Specifically, great apes combine increased investment in the cortico-cerebellar system with a decreased investment in the descending motor pathway (see electronic supplementary material, S2).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § 3. Discussion

    Great apes stand out in a joint emphasis on the prefronto-striatal formation and absolute brain size; a trend that is inferred to originate with the dawn of the ape radiation.

    “Great apes stand out in a joint emphasis on the prefronto-striatal formation and absolute brain size; a trend that is inferred to originate with the dawn of the ape radiation (figure 1b).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    A comparative correlation exists between absolute brain size and cognitive ability in non-human primates.

    “a comparative correlation between absolute brain size and cognitive ability in non-human primates [8]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Deaner RO, Isler K, Burkart J, van Schaik C. 2007. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 70, 115–124 10.1159/000102973 (doi:10.1159/000102973) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation
    § 1. Introduction

    Mosaic variation in relative size of individual brain structures has been shown to predict various aspects of behavioural capacity across the animal kingdom.

    “and predict various aspects of behavioural capacity across the animal kingdom [13–16]”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [13] Dunbar RIM, Shultz S. 2007. Evolution in the social brain. Science 317, 1344–1347 10.1126/science.1145463 (doi:10.1126/science.1145463) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [14] Huber R, van Staaden MJ, Kaufman LS, Liem KF. 1997. Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav. Evol. 50, 167–182 10.1159/000113330 (doi:10.1159/000113330) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [15] DeVoogd T, Krebs JR, Healy SD, Purvis A. 1993. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses among oscine birds. Proc. R. Soc. B 254, 75–82 10.1098/rspb.1993.0129 (doi:10.1098/rspb.1993.0129) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [16] Iwaniuk AN, Wylie DRW. 2007. Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus lentiformis mesencephali. J. Comp. Neurol. 500, 211–221 10.1002/cne.21098 (doi:10.1002/cne.21098) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    A comparative correlation exists between relative brain size and survival in novel environments in different orders across the animal kingdom.

    “between relative brain size and survival in novel environments in different orders across the animal kingdom [2,9,10]”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [2] Sol D, Bacher S, Reader SM, Lefebvre L. 2008. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172, S63–S71 10.1086/588304 (doi:10.1086/588304) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [9] Amiel JJ, Tingley R, Shine R. 2011. Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS ONE 6, e18277. 10.1371/journal.pone.0018277 (doi:10.1371/journal.pone.0018277) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [10] Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L. 2005. Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl Acad. Sci. USA 102, 5460–5465 10.1073/pnas.0408145102 (doi:10.1073/pnas.0408145102) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S1 (asserted), S4 (based).

    Premisenone given
    § 1. Introduction

    The relative importance of relative brain size and mosaic changes in explaining variation in brain evolution has not been established.

    “there are three elements that are fundamental to our understanding of these two aspects of brain evolution that have not been established: (i) What is the relative importance of relative brain size and mosaic changes in explaining variation in brain evolution?”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Premisereasoning
    § 1. Introduction

    Previous work has demonstrated that the neural system adapts in both size-dependent and size-independent ways.

    “previous work has demonstrated that the neural system adapts in both size-dependent and size-independent ways.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S1 (asserted), S4 (based).

    Premisenone given
    § 1. Introduction

    The temporal origin, rate and process underlying evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life have not been established.

    “(iii) What are the temporal origin, rate and process underlying evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life?”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    In primates, the evolution of brain size (both absolute and relative to body size) shows complex patterns of change involving both increases and decreases along different branches of the primate phylogeny.

    “In primates, the evolution of brain size (both in terms of absolute size and relative to body size) shows complex patterns of change involving both increases and decreases along different branches of the primate phylogeny [6,7].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [6] Montgomery SH, Capellini I, Barton RA, Mundy NI. 2010. Reconstructing the ups and downs of primate brain evolution: implications for adaptive hypotheses and Homo floresiensis. BMC Biol. 8, 9. 10.1186/1741-7007-8-9 (doi:10.1186/1741-7007-8-9) [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [7] Smaers JB, Dechmann DKN, Goswami A, Soligo C, Safi K. 2012. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18 006–18 011 10.1073/pnas.1212181109 (doi:10.1073/pnas.1212181109) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    The overall size of the brain plays an important part in neural adaptation.

    “The overall size of the brain plays an important part in neural adaptation”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] Kaas JH. 2006. Evolution of the neocortex. Curr. Biol. 16, R910–R914 10.1016/j.cub.2006.09.057 (doi:10.1016/j.cub.2006.09.057) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S1 (asserted), S4 (based).

    Premisenone given
    § 1. Introduction

    Which mosaic changes contribute most to explaining diversity in brain organization across species has not been established.

    “(ii) Which mosaic changes contribute most to explaining diversity in brain organization across species?”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    Mosaic variation in relative size of individual brain structures has been shown to reflect anatomical connectivity patterns.

    “This (mosaic) variation has been shown to reflect anatomical connectivity patterns [11,12]”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [11] Smaers JB, Steele J, Zilles K. 2011. Modeling the evolution of cortico-cerebellar systems in primates. In New perspectives on neurobehavioral evolution (eds Johnson JI, Zeigler HP, Hof PR.), pp. 176–190 New York: Annals of the New York Academy of Sciences. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [12] Whiting BA, Barton RA. 2003. The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10 10.1016/s0047-2484(02)00162-8 (doi:10.1016/s0047-2484(02)00162-8) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    Allometric approaches per se reveal useful information on brain structure evolution.

    “Although allometric approaches per se reveal useful information on brain structure evolution”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [3] de Winter W, Oxnard CE. 2001. Evolutionary radiations and convergences in the structural organization of the mammalian brain. Nature 409, 710–714 10.1038/35055547 (doi:10.1038/35055547) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [18] Willemet R. 2012. Understanding the evolution of mammalian brain structures: the need for a (new) cerebrotype approach. Brain Sci. 2, 203–224 10.3390/brainsci2020203 (doi:10.3390/brainsci2020203) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § 1. Introduction

    As absolute brain size increases, interacting neurons are located further apart and the brain is likely to become more modular in organization.

    “as the absolute size of the brain increases, interacting neurons are located further apart and the brain is likely to become more modular in organization [5]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [5] Kaas JH. 2006. Evolution of the neocortex. Curr. Biol. 16, R910–R914 10.1016/j.cub.2006.09.057 (doi:10.1016/j.cub.2006.09.057) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 3. Discussion

    The prefrontal cortex is generally considered to provide an infrastructure for synthesizing a diverse range of information that lays the foundation for the complex forms of behaviour observed in primates.

    “This brain structure is generally considered to provide ‘an infrastructure for synthesizing a diverse range of information that lays the foundation for the complex forms of behaviour observed in primates’ [49, p. 59].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [49] Miller EK. 2000. The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59–65 10.1038/35036228 (doi:10.1038/35036228) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 3. Discussion

    Recent functional connectivity research evidenced preferential distant connectivity of heteromodal association areas, with some regions in the prefrontal cortex (medial PFC) displaying both high local and high distant functional connectivity.

    “Recent functional connectivity research evidenced the preferential distant connectivity of heteromodal association areas, with some regions in the prefrontal cortex (medial PFC) displaying both high local (evidencing modularity) and high distant (evidencing multimodality) functional connectivity [51].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [51] Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BTT, Buckner RL. 2010. The organization of local and distant functional connectivity in the human brain. PLoS Comp. Biol. 6, e1000808. 10.1371/journal.pcbi.1000808 (doi:10.1371/journal.pcbi.1000808) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 2. Results

    Because olfactory bulb and medulla volume are considered to have experienced the least amount of change across anthropoid evolution, and brain size the most, PC1 can primarily be interpreted as reflecting changes in relative brain size.

    “Because olfactory bulb and medulla volume are considered to have experienced the least amount of change across anthropoid evolution, and brain size the most, this component can primarily be interpreted as reflecting changes in relative brain size.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Olfactory bulb and medulla volume have experienced the least amount of change across anthropoid evolution.
  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning
    § 1. Introduction

    This approach significantly increases the resolution of evolutionary inferences and allows for more detailed interpretations of the evolutionary history of particular biological traits.

    “This approach hereby significantly increases the resolution of evolutionary inferences and allows for more detailed interpretations of the evolutionary history of particular biological traits.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § 1. Introduction

    The method that underlies this approach infers variable rates of evolution for all individual lineages without a priori parametrization and provides realistic trait value estimates for extinct species.

    “The method that underlies this approach [23] infers variable rates of evolution for all individual lineages without a priori parametrization and provides realistic trait value estimates for extinct species.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [23] Smaers JB, Vinicius L. 2009. Inferring macro-evolutionary patterns using an adaptive peak model of evolution. Evol. Ecol. Res. 11, 991–1015 [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 3. Discussion

    The prefrontal cortex is a multimodal structure involved in social cognition, moral judgements, clan mentality, introspection as well as goal-directed and stimulus-driven attention.

    “The prefrontal cortex is a multimodal structure involved in social cognition [44], moral judgements [45], clan mentality [46], introspection [47] as well as goal-directed and stimulus-driven attention [48].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [44] Powell JL, Lewis PA, Dunbar RIM, Garcia-Finana M, Roberts N. 2010. Orbital prefrontal cortex volume correlates with social cognitive competence. Neuropsychologia 48, 3554–3562 10.1016/j.neuropsychologia.2010.08.004 (doi:10.1016/j.neuropsychologia.2010.08.004) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [45] Forbes CE, Grafman J. 2010. The role of the human prefrontal cortex in social cognition and moral judgment. An. Rev. Neurosci. 33, 299–324 [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [46] Krienen FM, Tu P-C, Buckner RL. 2010. Clan mentality: evidence that the medial prefrontal cortex responds to close others. J. Neurosci. 30, 13 906–13 915 10.1523/jneurosci.2180-10.2010 (doi:10.1523/jneurosci.2180-10.2010) [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. Material and methods

    Australopithecus afarensis is close to the ancestral node of chimpanzees and humans and has an estimated fossil brain size of 434cc.

    “Australopithecus afarensis is considered to be close to the ancestral node of chimpanzees and humans and has an estimated fossil brain size of 434cc [71]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [71] Fleagle JG. 1999. Primate adaptation and evolution. San Diego, CA: Academic Press [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 3. Discussion

    Putative developmental regularities in the evolution of brain structures in primates do not contribute markedly to explaining neural system diversity across species and/or are commonly offset by mosaic reorganization.

    “suggesting that putative developmental regularities in the evolution of brain structures in primates [65,66] do not contribute markedly to explaining neural system diversity across species and/or are commonly offset by mosaic reorganization.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [65] Finlay BL, Darlington RB, Nicastro N. 2001. Developmental structure in brain evolution. Behav. Brain Sci. 24, 263–308 10.1017/S0140525X01003958 (doi:10.1017/S0140525X01003958) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [66] Finlay BL, Darlington RB. 1995. Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584 10.1126/science.7777856 (doi:10.1126/science.7777856) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 3. Discussion

    Symmetry of brain reorganization in the context of increases versus decreases in absolute brain size has not been extensively studied, but preliminary evidence from the Chiroptera suggests there is asymmetry in the link between brain reorganization and cognitive capacity due to the different ecological niches available to species with different overall sizes.

    “Symmetry of brain reorganization in the context of increases versus decreases in absolute brain size has not been extensively studied, but preliminary evidence from the Chiroptera suggests there is asymmetry in the link between brain reorganization and cognitive capacity due to the different ecological niches available to species with different overall sizes [59].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [59] Safi K, Seid MA, Dechmann DKN. 2005. Bigger is not always better: when brains get smaller. Biol. Lett. 1, 283–286 10.1098/rsbl.2005.0333 (doi:10.1098/rsbl.2005.0333) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 3. Discussion

    Both the hippocampus-entorhinal and prefronto-striatal formations comprise different memory systems involved in forms of learning in which stimulus-response associations or habits are incrementally and sequentially acquired (striatal) and more cognitive or declarative memory (hippocampal).

    “congruent with suggestions that both comprise different memory systems [53,54] involved in forms of learning in which stimulus-response associations or habits are incrementally and sequentially acquired (striatal) [55–57] and more cognitive or declarative memory (hippocampal) [53,58].”
    Quote in the paperSubstantial claim0 of 6 sources checked
    • cites [53] Packard MG, Knowlton BJ. 2002. Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25, 563–593 10.1146/annurev.neuro.25.112701.142937 (doi:10.1146/annurev.neuro.25.112701.142937) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [54] Sherry DF, Schacter DL. 1987. The evolution of multiple memory systems. Psychol. Rev. 94, 439–454 10.1037/0033-295x.94.4.439 (doi:10.1037/0033-295x.94.4.439) [DOI] [Google Scholar]

      Not checked in the free run.

    • cites [55] Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J, Lehericy S, Benali H. 2009. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61–75 10.1016/j.bbr.2008.11.012 (doi:10.1016/j.bbr.2008.11.012) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [56] Fernandez-Ruiz J, Wang J, Aigner TG, Mishkin N. 2001. Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc. Natl Acad. Sci. USA 98, 4196–4201 10.1073/pnas.061022098 (doi:10.1073/pnas.061022098) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [57] Knowlton BJ, Mangels JA, Squire LR. 1996. A neostriatal habit learning system in humans. Science 273, 1399–1402 10.1126/science.273.5280.1399 (doi:10.1126/science.273.5280.1399) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [58] Schacter DL, Addis DR, Buckner RL. 2007. Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657–661 10.1038/nrn2213 (doi:10.1038/nrn2213) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § 4. Material and methods

    Oreopithecus is derived from the great apes stem lineage, after its divergence from the gibbon lineage, and has an estimated fossil brain size of 383cc.

    “Oreopithecus is considered to be derived from the great apes stem lineage, after its divergence from the gibbon lineage, and has an estimated fossil brain size of 383cc [71,72]”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [71] Fleagle JG. 1999. Primate adaptation and evolution. San Diego, CA: Academic Press [Google Scholar]

      Not checked in the free run.

    • cites [72] Straus WL, Schon MA. 1960. Cranial capacity of Oreopithecus bambolii. Science 132, 670–672 10.1126/science.132.3428.670 (doi:10.1126/science.132.3428.670) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § 4. Material and methods

    Proconsul is most often considered to be derived from the ape stem lineage, after its divergence from the Old World monkey lineage, and has an estimated fossil brain size of 162cc.

    “Proconsul is most often considered to be derived from the ape stem lineage, after its divergence from the Old World monkey lineage, and has an estimated fossil brain size of 162cc [73]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [73] Martin RD. 1990. Primate origins and evolution. London, UK: Chapman & Hall [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 3. Discussion

    Functionally, PC6 and PC7 can roughly be associated with the execution of motor actions and the acquisition of new complex motor sequences.

    “Functionally, these two components can roughly be associated with the execution of motor actions and the acquisition of new complex motor sequences.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 3. Discussion

    The increased variation in PC6 when brain size decreases may be due to smaller primates being confronted with a more diverse array of physical environments placing particular pressure on basic motor execution (such as locomotion).

    “further confirming our interpretation that this may be due to smaller primates being confronted with a more diverse array of physical environments placing particular pressure on basic motor execution (such as locomotion).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Smaller primates tend to be more agile, allowing them to inhabit a more diverse array of physical environments, placing particular pressure on spatial memory and basic motor execution.
  • May combine two claims.

    Interpretationown data
    § 3. Discussion

    A clade-specific investment in particular brain formations (prefrontal white matter, prefronto-striatal and higher motor control) in combination with increased absolute brain size differentiates great apes (and humans) from other primates.

    “Overall, our phylogenetic analysis infers that a clade-specific investment in particular brain formations (prefrontal white matter, prefronto-striatal and higher motor control) in combination with increased absolute brain size differentiates great apes (and humans) from other primates (figure 1).”
    Quote in the paperSubstantial claim
35 of 35
  • The paper relies on this without support.

    Olfactory bulb and medulla volume have experienced the least amount of change across anthropoid evolution.

    “Because olfactory bulb and medulla volume are considered to have experienced the least amount of change across anthropoid evolution, and brain size the most, this component can primarily be interpreted as reflecting changes in relative brain size.”
  • The paper relies on this without support.

    Smaller primates tend to be more agile, allowing them to inhabit a more diverse array of physical environments, placing particular pressure on spatial memory and basic motor execution.

    “For physiological reasons, smaller primates tend to be more agile, allowing them to inhabit a more diverse array of physical environments, possibly placing particular pressure on spatial memory.”
  • The paper relies on this without support.

    The variable rates method's accuracy far exceeds what can be attained with alternative methods.

    “this level of accuracy far exceeds what can be attained with alternative methods”
3 of 3

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?

  • The cortical reorganization hypothesis suggests that selection for absolutely larger brains, and concomitant cortical reorganization, was the predominant mechanism supporting cognitive evolution.

    “The cortical reorganization hypothesis suggests that selection for absolutely larger brains-and concomitant cortical reorganization-was the predominant mechanism supporting cognitive evolution (77, 91, 100-106, 120).”

    From The evolution of self-control. (2014) · cites this paper as [91]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Reported brain-size range is not 40 orders of magnitude

    Minor

    The stated smallest and largest brain sizes differ by a factor of about 43, or approximately 1.6 orders of magnitude-not 40 orders of magnitude.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 4

  1. Smaers JB, The evolution of human handedness
  2. 10.1073/090504197 · DOI
  3. 10.1152/jn.00339.2011 · DOI · Paper page
  4. Zilles K, 2011, Resources and technological advances for studies of neurobehavioral evolution, E94

Cited by

Sorted by citations

Authors
Smaers, J. B., & Soligo, C.
Affiliations
University College London (GB)
Corresponding author
Smaers, J. B.
Venue
Proceedings of the Royal Society B: Biological Sciences
Published
2013-05-22
Volume
280
Issue
1759
Pages
20130269
ISSN
  • 0080-4649 (ISSN-L)
  • 0962-8452
  • 1471-2954
OpenAlex
W2002762636
Cited by
112
References
75
Citations by year
2026: 3 · 2025: 7 · 2024: 7 · 2023: 6 · 2022: 5 · 2021: 9 · 2020: 10 · 2019: 9 · 2018: 3 · 2017: 8 · 2016: 15 · 2015: 10 · 2014: 14 · 2013: 6
FWCI
22.23
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the Royal Society B Biological Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
Natural Environment Research Council (NE/H022937/1)
Topics
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
Keywords
primate brain evolution, brain reorganization, relative brain size, anthropoid primates, prefrontal cortex, brain structure volume, lineage-specific evolution, brain systems, motor control, learning
MeSH terms
Animals, Haplorhini, Cerebellum, Biological Evolution, Female, Male, Motor Cortex, Phylogeny, Primates, Multivariate Analysis, Prefrontal Cortex, Principal Component Analysis

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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

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