Cited by 344Primate Behavior and EcologyAnimal Behavior and ReproductionEvolutionary Psychology and Human Behavior

The evolution of the social brain: anthropoid primates contrast with other vertebrates

Open access
Shultz, Susanne, Dunbar, R.I.M·2007·Proceedings of the Royal Society B: Biological Sciences

Abstract

The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living. We test predictions arising from the hypothesis using comparative data from birds and four mammalian orders (Carnivora, Artiodactyla, Chiroptera and Primates) and show that, across all non-primate taxa, relative brain size is principally related to pairbonding, but with enduring stable relationships in primates. We argue that this reflects the cognitive demands of the behavioural coordination and synchrony that is necessary to maintain stable pairbonded relationships. However, primates differ from the other taxa in that they also exhibit a strong effect of group size on brain size. We use data from two behavioural indices of social intensity (enduring bonds between group members and time devoted to social activities) to show that primate relationships differ significantly from those of other taxa. We suggest that, among vertebrates in general, pairbonding represents a qualitative shift from loose aggregations of individuals to complex negotiated relationships, and that these bonded relationships have been generalized to all social partners in only a few taxa (such as anthropoid primates).

AI snapshot

Written from the paper’s full text.

TL;DR

The paper tests the social brain hypothesis across birds and four mammalian orders, finding that relative brain size in non-primate taxa is principally associated with pairbonding rather than group size. Primates differ: they show a strong group-size effect on brain size, and anthropoid primates uniquely generalize bonded relationships to all social partners.

Key findings

  • Primates showed a positive correlation between group size and relative brain size (λ=0.80, F1,40=8.14, p<0.01), whereas this relationship was not significant in artiodactyls (λ=0.63, F1,67=0.30, p=0.58) or carnivores (λ=0.11, F1,84=0.07, p=0.80).
  • Social system was significantly associated with relative brain size in all three focal taxa: primates (F3,38=12.47, p<0.001), carnivores (F3,82=3.10, p=0.03), and artiodactyls (F3,65=2.86, p=0.04). Pairbonded species had larger relative brains than non-pairbonded species in carnivores (t=−2.86, p=0.0025), ungulates (t=−2.53, p=0.0007), and birds (t=−5.67, p<0.001), but not in bats (t=−1.34, p=0.095) or primates (t=−0.13, p=0.445).
  • Bonded relationships were unusually common in anthropoid primates: the four taxa differed significantly (Χ²6=19.74, p=0.003), anthropoids differed from the other three combined (Χ²2=8.49, p=0.01), while strepsirhine primates did not differ from ungulates and carnivores combined (Χ²2=1.89, p=0.39).
  • Anthropoid primates devoted significantly more time to social activity than ungulates (F1,39=9.59, p=0.004); when adjusted for group size, pairbonded species devoted significantly more time to social activities than harem-based or multimale species in both ungulates and primates.

Methods

  • Comparative dataset: 86 carnivore, 69 artiodactyl, and 45 primate species with anatomical brain volume data, plus 135 bird species and 54 bat species from other analyses. Species were assigned to social categories (solitary, pairbonded, harem/single sex, multimale) and ecological factors (diet, habitat, strata, activity).
  • Phylogenetic generalized least squares (PGLS) in R using APE estimated residual brain size controlling for body size and phylogeny; minimum adequate models (MAMs) used forward and backward stepwise selection.
  • Social intensity was assessed by classifying 205 genera as female–female bonded, pairbonded, or non-bonded from species descriptions, with 93% inter-observer agreement (κ=0.87, τ=14.59, p<0.001); activity budget data for primates and artiodactyls came from the literature.

Limitations

  • The paper states possible confounds from ecological and life-history variables, but MAMs confirmed social system independently predicted brain size in all taxa. It also considers alternatives: a bat brain–testis trade-off, which the authors argue is better explained by both covarying with mating system, and biparental care, which they argue does not explain the pairbonding effect across taxa.
  • The paper notes phylogeny uncertainty but reports that analyses with and without phylogenetic correction for the mating-system analysis gave the same results.
  • Evident from the text: the study is comparative and correlational, so it cannot establish causation; social-time data are available only for a subset of species and use a broad definition of social activity; the bat pairbonding result is not statistically significant (p=0.095); and primates are described as a clear outlier relative to other taxa.

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

Integrity signals

Registry

Crossref · 10.1098/rspb.2007.0693

Cites

48 of 48 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 44 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § 3. Results

    The pattern of pairbonded species having the largest brain sizes is closely paralleled in both birds and bats.

    “and this pattern is closely paralleled in both birds and bats.”
    Quote in the paperNot a substantial claim
  • Findingown data
    § 3. Results

    Bonded relationships are unusually common in anthropoid primates.

    “are unusually common in anthropoid primates (figure 4).”
    Quote in the paperSubstantial claim
  • Findingown data
    § 3. Results

    Pairbonded species have significantly larger relative brains than non-pairbonded species in all taxa except bats and primates.

    “pairbonded species have significantly larger relative brains than non-pairbonded species in all taxa except bats and primates”
    Quote in the paperSubstantial claim
  • Findingown data
    § 4. Discussion

    Irrespective of any ecological and life-history covariates, social system independently influences brain size in all taxa.

    “However, the MAMs analysis confirms that, irrespective of any ecological and life-history covariates, social system independently influences brain size in all taxa.”
    Quote in the paperSubstantial claim
  • Findingown data
    § 3. Results

    Anthropoids differ from all three other taxa combined in sociality.

    “anthropoids differ from all the three combined (Χ22=8.49, p=0.01).”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 15
  • May combine two claims. 13
  • The quote only partly states this claim. 1
  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing), S4 (based). May combine two claims. The quote only partly states this claim.

    Findingown data
    § 3. Results

    All five taxa exhibit a consistent trend in the same direction, with pairbonded species having larger relative brains.

    “All the five taxa exhibit a consistent trend in the same direction”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S4 (based).

    Findingnone given
    § 3. Results

    Bonded relationships (female-female bonds or pairbonds) are rare in mammals as a whole.

    “bonded relationships (defined as having either female–female bonds or pairbonds; see §2), which are rare in mammals as a whole”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data
    § 4. Discussion

    Primates exhibit a strong signature for a quantitative group size effect on brain size, but all other taxa (including birds and a wide range of non-primate mammals) do not.

    “Our analyses reveal a marked contrast between primates and all the other taxa (including both birds and a wide range of non-primate mammals) in that primates exhibit a strong signature for a quantitative group size effect on brain size, but all the other taxa do not.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation
    § Abstract

    The social brain hypothesis proposes that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living.

    “The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Jolly 1966

      Not checked in the free run.

    • cites Byrne & Whiten 1988

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    • cites Dunbar 1992, 1998

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

    Premisecitation
    § 2. Material and methods

    The four-way categorization of social systems is standard in the primate literature.

    “This four-way categorization of social systems is standard in the primate literature (Smuts et al. 1987)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Smuts et al. 1987

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  • May combine two claims.

    Premisecitation
    § 1. Introduction

    In primates, alternative indices of social complexity such as deception rates, mating strategies, grooming clique size and coalition rates all correlate with relative brain size.

    “alternative indices of social complexity such as deception rates (Byrne & Whiten 1988), mating strategies (Pawlowski et al. 1998), grooming clique size (Kudo & Dunbar 2001) and coalition rates (Dunbar & Shultz 2007) all correlate with relative brain size.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Byrne & Whiten 1988

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    • cites Pawlowski et al. 1998

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    • cites Kudo & Dunbar 2001

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

    Study design and conductown data
    § 2. Material and methods

    Inter-observer agreement for 205 genera was 93% (κ=0.87, τ=14.59, p<0.001).

    “our overall agreement for 205 genera was 93% (κ=0.87, τ=14.59, p<0.001).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cohen 1960

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data
    § 2. Material and methods

    Minimum adequate models were constructed to check whether ecological factors were confounds with social measures.

    “As a second step to check whether ecological factors were confounds with our social measures, we constructed minimum adequate models (MAMs; table 2) using forward and backward stepwise selection”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation
    § 2. Material and methods

    Various ecological factors are associated with brain size.

    “As various ecological factors have been shown to be associated with brain size (Harvey et al. 1980; Reader & Laland 2002)”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Harvey et al. 1980

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    • cites Reader & Laland 2002

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  • Classified as probably not a substantial claim.

    Premisecitation
    § 1. Introduction

    The cognitive demands imposed by social complexity was proposed as an explanation for why primates have unusually large brains for their body size.

    “Several decades ago, the cognitive demands imposed by social complexity was proposed as an explanation for why primates have unusually large brains for their body size (Jolly 1966; Byrne & Whiten 1988).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Jolly 1966

      Not checked in the free run.

    • cites Byrne & Whiten 1988

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  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning
    § 4. Discussion

    In lifelong monogamous mating relationships, it is imperative that the risk of cuckoldry is minimized and that individuals optimize mate choice.

    “making it imperative that the risk of cuckoldry is minimized and that individuals optimize mate choice”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation
    § 3. Results

    It has been widely assumed that managing polygamous mating relationships is cognitively more taxing.

    “it has been widely assumed that managing polygamous mating relationships is cognitively more taxing (e.g. Gittleman 1986).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gittleman 1986

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisecitation
    § 1. Introduction

    The essence of the social brain hypothesis is that the need to solve ecological problems in a social context, rather than in a demographic vacuum, imposes significant cognitive demands.

    “The essence of the SBH is that the need to solve (ecological) problems in a social context, rather than in a demographic vacuum, imposes significant cognitive demands.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dunbar 1992, 1998

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. Discussion

    Maintaining a lasting pairbond entails inevitable conflict between partners over resources, parental investment decisions and time budgets, which necessitates an ability to resolve conflicts and coordinate scheduling.

    “maintaining a lasting bond entails inevitable conflict between partners over resources, parental investment decisions and time budgets, which in turn necessitates an ability to resolve conflicts and coordinate scheduling (Dunbar & Dunbar 1980)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Dunbar & Dunbar 1980

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  • Classified as probably not a substantial claim.

    Premisecitation
    § 2. Material and methods

    The key factor in primate sociality has long been thought to be female-bondedness.

    “the key factor in primate sociality has long been thought to be female-bondedness (Wrangham 1980)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wrangham 1980

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  • Classified as probably not a substantial claim.

    Study design and conductown data
    § 2. Material and methods

    Each of us independently classified all primate, carnivore and ungulate genera as a function of the kinds of bonds exhibited by females.

    “Each of us independently classified all primate, carnivore and ungulate (artiodactyl) genera as a function of the kinds of bonds exhibited by females”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductcitation
    § 2. Material and methods

    PGLS analysis was used to estimate residual brain size controlling for body size and phylogeny.

    “we employed phylogenetic generalized least squares (PGLS) analysis (Grafen 1989) to estimate residual brain size controlling for body size and phylogeny (as a fixed factor)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Grafen 1989

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 4. Discussion

    For bats, rather than polygamous species trading brain tissue for larger testes, monogamous species require more brain volume.

    “A more plausible alternative explanation for their bat results is thus that, rather than polygamous species trading brain tissue for larger testes, monogamous species require more brain volume.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § 4. Discussion

    Wolves (and other group-living canids), callitrichids and many lemurid prosimians have social groups based around breeding pairs.

    “Possible examples of this type of sociality are wolves (and other group-living canids), callitrichids and many lemurid prosimians (van Schaik & Kappeler 1993), all of whose social groups are based around breeding pairs.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites van Schaik & Kappeler 1993

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 4. Discussion

    There is a qualitative difference (at least in terms of cognitive demands) between bonded and non-bonded social systems, suggesting that there may be two separate evolutionary routes between asociality, aggregations and bonded social systems.

    “Additionally, there is a qualitative difference (at least in terms of cognitive demands) between bonded and non-bonded social systems, suggesting that there may be two separate evolutionary routes between asociality, aggregations and bonded social systems.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductcitation
    § 4. Discussion

    The phylogenies used are the most recent and widely accepted; the primate phylogeny (Purvis 1995) is standard and not in serious dispute.

    “We have used those that are the most recent and widely accepted; indeed, that for primates (Purvis 1995) is the standard phylogeny used in all comparative analyses, and is not in serious dispute.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Purvis 1995

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  • May combine two claims.

    Premisecitation
    § 4. Discussion

    Both brain and testis sizes are strongly associated with mating system, while the relationship between relative brain and testis sizes is much weaker.

    “Pitnick et al. (2006) themselves show that both brain and testis sizes are strongly associated with mating system, while the relationship between relative brain and testis sizes is much weaker.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Pitnick et al. (2006)

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  • May combine two claims.

    Study design and conductreasoning
    § 4. Discussion

    For orders where there is disagreement, it usually concerns the insertion points of major taxonomic groups rather than the detailed arrangement of species within families, and such disagreements are likely to affect only a handful of high-level nodes and have limited statistical impact on the results.

    “For those orders where there is disagreement, this usually concerns the insertion points of major taxonomic groups, rather than the detailed arrangement of species within families; since such disagreements are likely to affect only a handful of high-level nodes in the phylogeny, they will have rather limited statistical impact on the results.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation
    § 4. Discussion

    Many anthropoid primate species have large social groups with a stable structure of related individuals, often based on matrilineal or patrilineal kinship, as well as coalition and grooming relationships between genetically unrelated individuals.

    “many anthropoid primate species, in particular, have large social groups with a stable structure of related individuals, often based on matrilineal or patrilineal kinship, as well as coalition and grooming relationships between genetically unrelated individuals: Smuts et al. 1987; Dunbar 1988”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Smuts et al. 1987

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    • cites Dunbar 1988

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  • May combine two claims.

    Interpretationreasoning
    § 4. Discussion

    The rarity of female-bonded social systems in non-primates and their relative commonness in primates might explain why primates exhibit a much stronger quantitative signature for group size than other taxa.

    “Although female-bonded social systems appear to be relatively common in primates, they seem to have happened only in isolated and rather exceptional cases among non-primates (e.g. elephants, equids). This might explain why primates exhibit a much stronger quantitative signature for group size than other taxa.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Female-bonded social systems are relatively common in primates but occur only in isolated and exceptional cases among non-primates.
25 of 25
  • The paper relies on this without support.

    In bonded groups, animals need to maintain relationships with their social partners.

    “A key problem faced by animals that live in bonded groups is the need to maintain relationships with their social partners.”
  • The authors state this as an assumption.

    Time invested in social activity is a valid measure of investment in social relationships.

    “we here use the amount of time invested in social activity as a measure of investment in social relationships.”
  • The paper relies on this without support.

    Male-bonded social systems are rare in any order.

    “male-bonded social systems are rare in any order”
  • The paper relies on this without support.

    The four-way categorization of social systems can be applied to any order.

    “it can be applied perfectly well to any order.”
  • The paper relies on this without support.

    Social grooming is a widely accepted index of bondedness in primates.

    “where social grooming is a widely accepted index”
  • The paper relies on this without support.

    With the exception of primates, there has been little attempt to define behavioural measures of bondedness in animals.

    “With the exception of primates (where social grooming is a widely accepted index), there has been little attempt to define behavioural measures of bondedness in animals.”
  • The paper relies on this without support.

    Within a social environment, individual decisions must be responsive to the decisions made by other group members and the constraints these impose.

    “Within a social environment, individual decisions must be responsive to the decisions made by other group members and the constraints these impose.”
  • The paper relies on this without support.

    The number of potential dyadic relationships is proportional to group size.

    “the number of potential dyadic relationships (interpreted as one index of social complexity) is proportional to group size.”
  • The paper relies on this without support.

    Primates are typically found in larger social groups than ungulates.

    “As this may simply reflect the fact that primates are typically found in larger social groups”
  • The paper relies on this without support.

    Female-bonded social systems are relatively common in primates but occur only in isolated and exceptional cases among non-primates.

    “Although female-bonded social systems appear to be relatively common in primates, they seem to have happened only in isolated and rather exceptional cases among non-primates (e.g. elephants, equids).”
10 of 10

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Cites

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Research works printed but not linked: 2

  1. Byrne R.W& Whiten A. 1988 Oxford UK:Oxford University Press.
  2. Smuts B.B Cheney D.L Seyfarth R.M Wrangham R.W& Struhsaker T.T. 1987 Chicago IL:University of Chicago Press.

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Authors
Shultz, S., & Dunbar, R. I. M.
Affiliations
University of Liverpool (GB)
Venue
Proceedings of the Royal Society B: Biological Sciences
Published
2007-07-25
Volume
274
Issue
1624
Pages
2429-2436
ISSN
  • 0080-4649 (ISSN-L)
  • 0962-8452
  • 1471-2954
OpenAlex
W2122836078
Cited by
344
References
48
Citations by year
2026: 8 · 2025: 11 · 2024: 26 · 2023: 19 · 2022: 19 · 2021: 34 · 2020: 25 · 2019: 18 · 2018: 19 · 2017: 26 · 2016: 21 · 2015: 14 · 2014: 15 · 2013: 12 · 2012: 28
FWCI
16.67
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)
  • Research Explorer (The University of Manchester) (submittedVersion)
Topics
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
Keywords
social brain hypothesis, brain size, anthropoid primates, group living, group size, social coordination, comparative neuroanatomy, birds, mammals, Carnivora, Artiodactyla, bats
MeSH terms
Animals, Birds, Brain, Biological Evolution, Female, Male, Mammals, Organ Size, Pair Bond, Primates, Social Behavior

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