ArticlePDF Available

Neocortex evolution in primates: The 'social brain' is for females

Article

Neocortex evolution in primates: The 'social brain' is for females

Abstract and Figures

According to the social intelligence hypothesis, relative neocortex size should be directly related to the degree of social complexity. This hypothesis has found support in a number of comparative studies of group size. The relationship between neocortex and sociality is thought to exist either because relative neocortex size limits group size or because a larger group size selects for a larger neocortex. However, research on primate social evolution has indicated that male and female group sizes evolve in relation to different demands. While females mostly group according to conditions set by the environment, males instead simply go where the females are. Thus, any hypothesis relating to primate social evolution has to analyse its relationship with male and female group sizes separately. Since sex-specific neocortex sizes in primates are unavailable in sufficient quantity, I here instead present results from phylogenetic comparative analyses of unsexed relative neocortex sizes and female and male group sizes. These analyses show that while relative neocortex size is positively correlated with female group size, it is negatively, or not at all correlated with male group size. This indicates that the social intelligence hypothesis only applies to female sociality.
Content may be subject to copyright.
Biol. Lett. (2005) 1, 407–410
doi:10.1098/rsbl.2005.0362
Published online 24 August 2005
Neocortex evolution in
primates: the ‘social brain’
is for females
Patrik Lindenfors
*
,†
Department of Biology, University of Virginia, Gilmer Hall,
Charlottesville, VA 22904-4328, USA
*( patrik.lindenfors@virginia.edu)
Temporary address: P.O. Box 19423, 202 KNH-Nairobi, Kenya.
According to the social intelligence hypothesis,
relative neocortex size should be directly related
to the degree of social complexity. This hypo-
thesis has found support in a number of com-
parative studies of group size. The relationship
between neocortex and sociality is thought to
exist either because relative neocor tex size
limits group size or because a larger group size
selects for a larger n eocor tex. However,
research on primate social evolution has indi-
cated that male and female group sizes evolve
in relation to different demands. While females
mostly group according to conditions set by the
environment, males instead simply go where the
females are. Thus, any hypothesis relating to
primate social evolution has to analyse its
relationship with male and female group sizes
separately. Since sex- specific neocortex sizes in
primates are unavailable in sufficient quantity,
I here instead present results from phylogenetic
comparative analyses of unsexed relative neo-
cortex sizes and female and male group sizes.
These analyses show that while relative
neocor tex size is positively cor related with
female group size, it is negatively, or not at all
correlated with male group size. This indicates
that the social intelligence hypothesis only
applies to female sociality.
Keywords: sexual dimorphism;
phylogenetic comparative methods; sexual selection
1. INTRODUCTION
The neocortex is the brain structure that handles
the more demanding cognitive and social skills
(Innocenti & Kaas 1995; Kaas 1995). Animals with
large general brain sizes also tend to have dispropor-
tionally large neocortices (Finlay & Darlington
1995), but this relationship is not just simply
allometric. Instead, selective processes can select for
brain structures similar in function yet at different
locations in the brain. In primates, for example, the
visual cortex and the lateral geniculate—both
involved in the visual system—have been modified
through demands from frugivory on visual compe-
tence (Barton 1998; Barton & Harvey 2000; de
Winter & Oxnard 2001). Hence, a single selection
pressure may select for enlargement of several brain
components. Nevertheless, if one wants to investigate
the evolution of higher cognitive functions, the
neocortex is the structure to focus on.
The social intelligence hypothesis states that rela-
tive neocortex size should be related to the degree of
social complexity (Byrne & Whiten 1988). This is
because more complex social networks place higher
cognitive demands on individuals and thus select for
larger neocortices (Sawaguchi 1992), or conversely
because neocortex size places a limit on the number
of social interactions an individual can keep track of
and thus limits group size (Dunbar 1992; Kudo &
Dunbar 2001). When studying primate sociality,
however, the focus has more often been on the
influence of ecological factors on group size (Emlen &
Oring 1977; Altmann 1990; Lindenfors et al. 2004).
The evolution of primate sociality has largely been
seen as driven by resource defence (Wrangham 1980)
or predator avoidance (van Schaik 1983). Addition-
ally, it has been shown that ecological factors, such as
the degree of frugivory, are related to neocortex size
because a large part of the neocortex is involved in
visual processing (Barton 1996, 1998). Also, larger
brains consume more energy, placing demands for an
energy-rich diet. Hence, ecology, social group size
and relative neocortex size all relate to each other in a
triangle of hypotheses.
An insight from research on primate sociality,
however, is that social evolution in primates is driven
by different processes in males and females. While
female reproductive success is linked to the acqui-
sition of resources and protection from predators,
males gain from monopolizing access to females
(Emlen & Oring 1977; Altmann 1990; Lindenfors
et al.2004). Thus, one would expect that social
selection pressures on neocortex size should be
different in males and females. If relative neocortex
size limits group size (Dunbar 1992; Kudo & Dunbar
2001), this should limit female group size more than
male group size—if nothing else, simply because there
aremorefemalesthanmalesinprimategroups
(Lindenfors et al. 2004; Nunn 1999). Also, separate
dominance hierarchies are not seldom maintained for
males and females in primate groups (Smuts et al.
1987), indicating that males should have fewer
intrasexual interactions to keep track of than females.
If it is assumed that causality is reversed, in that
increased social complexity is what selects for a larger
relative neocortex (Sawaguchi 1992), this can still
place stronger selection on neocortex size in females
than in males. This because selection should be
highest in the sex where the value of keeping track of
social interactions is higher. Two patterns indicate
that this would be females. First, most haplorhine
primates are matrilocal, where females stay in the
social network where they were born whereas males
migrate to new social groups upon reaching adult-
hood (Smuts et al. 1987). Second, about two-thirds
of haplorhine primates are polygynous (Lindenfors &
Tullberg 1998), where intrasexual interactions
between males to a large degree consist of competing
with other males over access to females. This is not to
say that males have no social interactions or even that
social interactions are unimportant to males, only
that the value of social interactions, and of keeping
track of them, most probably is higher in primate
females than in males.
Received 18 May 2005
Accepted 4 July 2005
407 q 2005 The Royal Society
2. MATERIAL AND METHODS
Data on neocortex volumes, brain volumes, body mass, and group
sizes were taken from the literature (Stephan et al. 1981; Smith &
Jungers 1997; Nunn & Barton 2000). No information was available
concerning the sexes of the animals whose brains were measured
and hence the present analysis presents results concerning species-
typical relative neocortex sizes. Though data exists for strepsirhine
primates, these were not included here because all but four of these
species were solitary.
Since the hypothesis to be investigated concerned the size of the
neocortex relative to the total brain, total brain size was included as
an independent variable in all regression models. Different
measures of relative neocortex size produce different results
(Deaner et al. 2000), but using the ratio of neocortex volume to
total brain volume produced similar results to the approach
favoured here. Residuals from neocortex—total brain volume
regression were used to construct figure 1, but not in any analyses.
All variables were log-transformed prior to analysis.
I used a phylogeny made with a super-tree technique combining
a large number of source phylogenies (Purvis & Webster 1999).
This phylogeny is a consensus tree utilizing all information
published up until its construction, and it thus unites knowledge
gathered from both molecular and morphological phylogenies.
Hypothesis testing was done using phylogenetic independent con-
trasts (Felsenstein 1985) as implemented in the computer program
P
DAP (Garland et al. 1993). Diagnostics showed that branch lengths
needed no adjustment (Garland et al. 1992).
3. RESULTS
Neocortex size is tightly correlated with total brain size
(F
1,19
Z11 814, BZ 1.050, R
2
Z0.998, p/0.001).
Total brain size was therefore included in all further
regression models. To test if the social intelligence
hypothesis applies equally to males and females, I first
analysed the relationship between relative neocortex
size and female and male group size separately.
While female group size was significantly correlated
with relative neocortex volume (partial regression
coefficients t
18
Z3.078, BZ 0.021, pZ0.006), male
group size was not (partial regression coefficients
t
18
Z1.125, BZ0.007, pZ0.275). This is in spite of
the fact that male and female group sizes—as also
shown elsewhere with larger datasets (Nunn 1999;
Lindenfors et al.2004)—are highly correlated
(F
1,19
Z21.753, BZ0.990, R
2
Z0.534, pZ0.0002).
A multiple regression model including both male
and female group size showed that relative neocortex
volume was significantly correlated with female
group size, while only a tendency of a correlation
( pZ0.069) was found with male group size (figure 1;
table 1). Somewhat surprisingly, the latter tendency
was negative. Given the correlation between male and
female group size, one could expect collinearity
problems in the multiple regression analysis, but
tolerance values of 0.366 for male group size and
0.344 for female indicated that this posed no
problem. Thus, male group size, despite being closely
tied to female group size (Nunn 1999; Lindenfors
et al. 2004), is not correlated with neocortex size by
itself, and is even indicated to have a negative
influence on relative neocortex size after accounting
for female group size.
If neocortex size scales positively with female
group size and negatively with male group size, this
could indicate that the underlying process is not
selection from increasing social demands, but instead
involves sexual selection on males (Sawaguchi 1997),
which is expected to be more intense in species where
more females and fewer males are included in a social
group (Darwin 1871). A large neocortex would in
this scenario be beneficial to males by e.g. making
them able to outsmart other males in intrasexual
competition, or due to female choice, where females
then simply would prefer more ‘cerebral’ males. To
investigate this possibility, I included body mass
dimorphism as a surrogate measure of sexual selec-
tion in the statistical models. Dimorphism did not
correlate significantly with relative neocortex volume
either when including only brain size (partial
regression coefficients t
18
Z K 1.748, BZK 0.031,
pZ 0.098), or when also including female group
size (partial regression coefficients of dimorphism
t
17
ZK1.255, BZK0.020, pZ0.226).
Using the Akaike information criterion (AIC;
Quinn & Keough 2002) for selecting between differ-
ent multiple regression models—initially including
total brain size, male and female group size, male
and female body mass, and body mass dimorphism
as independent variables in the model—showed
that the best regression model should include only
total brain size and female group size (table 2;
Table 1. Multiple regression of relative neocortex volume
on male and female group size.
(Full model F
3,17
Z6574.7, R
2
Z0.999, p/0.001.)
Bt(18) p-level
total brain size 1.035 118.158 0.000
male group size K0.014 K1.940 0.069
female group size 0.037 3.552 0.002
0.20
0.10
0.15
0.05
0.10
0.15
0.05
0.20
0
0.50
0.40
0.30
0.20
0.10
0
0.10
0.20
log (male group size) contrasts
log (female group size contrasts)
residual neocortex size
0.30
0.20
0.10
0
0.10
0.20
Figure 1. The relationship of relative neocortex volume and
male and female group size. Relative neocortex size is for
this figure calculated as residuals from a neocortex—brain
size regression. Multiple regression analysis shows that
relative neocortex volume scales positively with female
group size and that a tendency exists for relative neocortex
volume to scale negatively with male group size.
408 P. Lindenfors Neocortex evolution in primates
Biol. Lett. (2005)
AICZK 126.101). The AIC statistic only differed
slightly with that also including male group size (table
1; AICZK126.514) while the gap was wider to other
alternative models.
4. DISCUSSION
The comparative analysis presented here indicates
that brain evolution proceeds in accordance with the
social demands of females, because the size of the
neocortex in both sexes is larger in species with larger
female social networks. In this scenario, large relative
neocortex size in males could be the result of a
genetic correlation between the sexes, or of the
possible importance for both sexes of keeping track of
female social interactions. Note, however, that at
present no data exist to examine if neocortex size
differs between the sexes in primates.
Nevertheless, sex-specific predictions can be made
from the results presented here. For example, relative
neocortex size should be larger in females than in
males in more social primate species. Also, females in
social species should be expected to be relatively
better than males at tasks relating to sociality.
Other hypotheses exist regarding the evolution of
relative neocortex size, primarily concerning the
relationship with diet (Barton 1996, 1998). These
hypotheses propose that frugivory selects for a larger
neocortex through higher demands placed on the
visual system. Though it has been shown that diet
also influences neocortex size, it is highly unlikely
that this influence is sex-specific. On the other hand,
sex-specific factors beside group sizes may be of
importance for neocortex evolution. It has been
shown in terrestrial carnivores that degree of maternal
care correlates with larger female total brain size
(Gittleman 1994). Further sex-specific data on differ-
ent brain structures in primates and other mammals
could shed light on such questions.
There is no a priori reason to suspect that the
pattern reported here only applies to primates. In any
animal that is social, it is important for an individual’s
well-being and—in extreme cases—survival, to keep
track of social interactions and dominance hierar-
chies. Where opportunities exist for males to monop-
olize females, however, the advantages of doing so
would quickly outweigh the advantages of keeping
track of more fine-tuned social interactions. Intra-
male competition could thus counter the evolution of
neocortex size by making selection for larger neocor-
tices female-specific.
I wish to thank Charles L. Nunn, Birgitta S. Tullberg,
Johan Lind, John L. Gittleman and two anonymous
reviewers for comments on previous drafts of this manu-
script. This study was supported by the Swedish Research
Council.
Altmann, J. 1990 Primate males go where the females are.
Anim. Behav. 39, 193–195.
Barton, R. A. 1996 Neocortex size and behavioural ecology
in primates. Proc. R. Soc. B 263, 173–177.
Barton, R. A. 1998 Visual specialization and brain evolution
in primates. Proc. R. Soc. B 265, 1933–1937. (doi:10.
1098/rspb.1998.0523.)
Barton, R. A. & Harvey, P. H. 2000 Mosaic evolution of
brain structure in mammals. Nature 405, 1055–1058.
(doi:10.1038/35016580.)
Byrne, R. & Whiten, A. (eds) 1988 Machiavellian intelli-
gence. Oxford: Clarendon Press.
Darwin, C. 1871 The descent of man and selection in relation
to sex. London: Murray.
Deaner, R. O., Nunn, C. L. & van Schaik, C. P. 2000
Comparative tests of primate cognition: different scaling
methods produce different results. Brain. Behav. Evol.
55, 44–52. (doi:10.1159/000006641.)
de Winter, W. & Oxnard, C. E. 2001 Evolutionary
radiations and convergences in the structural organiz-
ation of mammalian brains. Nature 409, 710–714.
(doi:10.1038/35055547.)
Dunbar, R. I. M. 1992 Neocortex size as a constraint on
group size in primates. J. Hum. Evol. 20, 469–493.
(doi:10.1016/0047-2484(92)90081-J.)
Emlen, S. T. & Oring, L. W. 1977 Ecology, sexual selection,
and the evolution of mating systems. Science 197,
215–223.
Felsenstein, J. 1985 Phylogenies and the comparative
method. Am. Nat. 125, 1–15. (doi:10.1086/284325.)
Finlay, B. L. & Darlington, R. B. 1995 Linked regularities
in the development and evolution of mammalian brains.
Science 268, 1578–1584.
Garland Jr, T., Harvey, P. H. & Ives, A. R. 1992 Procedures
for the analysis of comparative data using phylogeneti-
cally independent contrasts. Syst. Biol. 41, 18–31.
Garland Jr, T., Dickerman, A. W., Janis, C. M. & Jones,
J. A. 1993 Phylogenetic analysis of covariance by
computer stimulation. Syst. Biol. 42, 265–292.
Gittleman, J. L. 1994 Female brain size and parental care
in carnivores. Proc. Natl Acad. Sci. USA 91, 5495–5497.
Innocenti, G. M. & Kaas, J. H. 1995 The cortex. Trends
Neurosci. 18, 371–372. (doi:10.1016/0166-2236(95)
93931-M.)
Kaas, J. H. 1995 The evolution of isocortex. Brain. Behav.
Evol. 46, 187–196.
Kudo, H. & Dunbar, R. I. M. 2001 Neocortex size and
social network size in primates. Anim. Behav. 62,
711–722. (doi:10.1006/anbe.2001.1808.)
Lindenfors, P. & Tullberg, B. S. 1998 Phylogenetic analyses
of primate size evolution: the consequences of sexual
selection. Biol. J. Linn. Soc. 64, 413–447. (doi:10.1006/
bijl.1998.0237.)
Lindenfors, P., Fro¨berg, L. & Nunn, C. L. 2004 Females
drive primate social evolution. Proc. R. Soc. B.
271(Suppl. 3), S101–S103. (doi:10.1098/rsbl.2003.0114.)
Nunn, C. L. 1999 The number of males in primate social
groups: a comparative test of the socioecological model.
Behav. Ecol. Sociobiol. 46, 1–13. (doi:10.1007/
s002650050586.)
Nunn, C. L. & Barton, R. A. 2000 Allometric slopes and
independent contrasts: a comparative test of Kleiber’s
law in primate ranging patterns. Am. Nat. 156, 519–533.
(doi:10.1086/303405.)
Table 2. Multiple regression of relative neocortex volume
on total brain size and female group size.
(Full model F
2,18
Z8547.8, R
2
Z0.999, p/0.001.)
Bt(18) p-level
total brain size 1.043 125.083 0.000
female group size 0.021 3.079 0.006
Neocortex evolution in primates P. Lindenfors 409
Biol. Lett. (2005)
Purvis, A. J. & Webster, A. 1999 Phylogenetically indepen-
dent comparisons and primate phylogeny. In Comparative
primate socioecology (ed. P. C. Lee), pp. 44–70. Cambridge
University Press.
Quinn, G. P. & Keough, M. J. 2002 Experimental design and
data analysis for biologists. New York: Cambridge Univer-
sity Press.
Sawaguchi, T. 1992 The size of the neocortex in relation to
ecology and social structure in moneys and apes. Folia
Primatol. 58, 131–145.
Sawaguchi, T. 1997 Possible involvement of sexual selection
in neocortical evolution of monkeys and apes. Folia
Primatol. 68, 96–99.
Smith, R. J. & Jungers, W. L. 1997 Body mass in
comparative primatology. J. Hum. Evol. 32, 523–559.
(doi:10.1006/jhev.1996.0122.)
Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham,
R. W. & Struhsaker, T. T. (eds) 1987 Primate societies.
University of Chicago Press.
Stephan, H., Frahm, H. & Baron, G. 1981 New and revised
data on volumes of brain structures in insectivores and
primates. Folia Primatol. 35, 1–29.
van Schaik, C. P. 1983 Why are diurnal primates living in
groups? Behaviour 87, 120–143.
Wrangham, R. W. 1980 An ecological model of female-
bonded primate groups. Behavior 75, 262–300.
410 P. Lindenfors Neocortex evolution in primates
Biol. Lett. (2005)
... where sexual selection is high compared to species where it is relaxed (26,27,10,28). ...
... All data used in this study were collected from published literature and are presented in the Appendix. Most studies on primate brain evolution have relied on a classic data set on primate brains provided (3), for example (31,32,48,49,41,36,25,50,19,35,47,38,51,52,53,54,55,26,27,56,44,57,58,59,14,60,20,61,62,63,39,64). Data on brain and neocortex size used in this study were obtained by pooling (3) and new data from (5). ...
... pair-bonding (20), tactical deception (25), we use group size as it is the most common used approximation of social complexity (e.g. 69,51,26,27,54,38,30,39). In this study both male and female group sizes are used because it has previously been shown that female rather than male group size correlate positively with neocortex volume in primates (26; 27), suggesting that it is social demands on females that mainly drives primate brain evolution. ...
Preprint
Full-text available
Primate brains differ in size and architecture. Hypotheses to explain this variation are numerous and many tests have been carried out. However, after body size has been accounted for there is little left to explain. The proposed explanatory variables for the residual variation are many and covary, both with each other and with body size. Further, the data sets used in analyses have been small, especially in light of the many proposed predictors. Here we report the complete list of models that results from exhaustively combining six commonly used predictors of brain and neocortex size. This provides an overview of how the output from standard statistical analyses changes when the inclusion of different predictors is altered. By using both the most commonly tested brain data set and a new, larger data set, we show that the choice of included variables fundamentally changes the conclusions as to what drives primate brain evolution. Our analyses thus reveal why studies have had troubles replicating earlier results and instead have come to such different conclusions. Although our results are somewhat disheartening, they highlight the importance of scientific rigor when trying to answer difficult questions. It is our position that there is currently no empirical justification to highlight any particular hypotheses, of those adaptive hypotheses we have examined here, as the main determinant of primate brain evolution.
... Demands of sociality are different between males and females. This should produce detectable differences in relative brain size or brain component size between species where sexual selection is high compared to species where it is relaxed [10,[26][27][28][29][30]. ...
... pair-bonding [20], tactical deception [25], we use group size as it is the most common used approximation of social complexity (e.g. [26,27,32,40,41,53,56,70]). In this study both male and female group sizes are used because it has previously been shown that female rather than male group size correlate positively with neocortex volume in primates [26,27], suggesting that it is social demands on females that mainly drives primate brain evolution. ...
... [26,27,32,40,41,53,56,70]). In this study both male and female group sizes are used because it has previously been shown that female rather than male group size correlate positively with neocortex volume in primates [26,27], suggesting that it is social demands on females that mainly drives primate brain evolution. ...
Article
Full-text available
Primate brains differ in size and architecture. Hypotheses to explain this variation are numerous and many tests have been carried out. However, after body size has been accounted for there is little left to explain. The proposed explanatory variables for the residual variation are many and covary, both with each other and with body size. Further, the data sets used in analyses have been small, especially in light of the many proposed predictors. Here we report the complete list of models that results from exhaustively combining six commonly used predictors of brain and neocortex size. This provides an overview of how the output from standard statistical analyses changes when the inclusion of different predictors is altered. By using both the most commonly tested brain data set and the inclusion of new data we show that the choice of included variables fundamentally changes the conclusions as to what drives primate brain evolution. Our analyses thus reveal why studies have had troubles replicating earlier results and instead have come to such different conclusions. Although our results are somewhat disheartening, they highlight the importance of scientific rigor when trying to answer difficult questions. It is our position that there is currently no empirical justification to highlight any particular hypotheses, of those adaptive hypotheses we have examined here, as the main determinant of primate brain evolution.
... Estimates for primate diet breadth were taken from [42]. We note that a key aspect of primate social structure is the number of adult females in a group [81]. However, as the number of females in primate groups is highly correlated with group size across the full range of primate species [82], we use total group size in all analyses. ...
Article
Characterizing non-human primate social complexity and its cognitive bases has proved challenging. Using principal component analyses, we show that primate social, ecological and reproductive behaviours condense into two components: socioecological complexity (including most social and ecological variables) and reproductive cooperation (comprising mainly a suite of behaviours associated with pairbonded monogamy). We contextualize these results using a meta-analysis of 44 published analyses of primate brain evolution. These studies yield two main consistent results: cognition, sociality and cooperative behaviours are associated with absolute brain volume, neocortex size and neocortex ratio, whereas diet composition and life history are consistently associated with relative brain size. We use a path analysis to evaluate the causal relationships among these variables, demonstrating that social group size is predicted by the neocortex, whereas ecological traits are predicted by the volume of brain structures other than the neocortex. That a range of social and technical behaviours covary, and are correlated with social group size and brain size, suggests that primate cognition has evolved along a continuum resulting in an increasingly flexible, domain-general capacity to solve a range of socioecological challenges culminating in a capacity for, and reliance on, innovation and social information use in the great apes and humans. This article is part of the theme issue ‘Cognition, communication and social bonds in primates’.
... The number 150 was established by extrapolating a regression line describing the relationship between group size and relative neocortex size in primates, to humans. [1,2,5,6] That there exists a correlation between group size and relative neocortex size has been replicated in several studies (e. g. [7][8][9][10][11][12][13][14]), though in some cases only for female primates [15,16], but often not finding a significant relationship (making an estimate of Dunbar's number unachievable) [11,14,17,18]. However, the replication studies are of somewhat limited value as most studies have used the same brain data. ...
Article
Full-text available
A widespread and popular belief posits that humans possess a cognitive capacity that is limited to keeping track of and maintaining stable relationships with approximately 150 people. This influential number, 'Dunbar's number', originates from an extrapolation of a regression line describing the relationship between relative neocortex size and group size in primates. Here, we test if there is statistical support for this idea. Our analyses on complementary datasets using different methods yield wildly different numbers. Bayesian and generalized least-squares phylogenetic methods generate approximations of average group sizes between 69-109 and 16-42, respectively. However, enormous 95% confidence intervals (4-520 and 2-336, respectively) imply that specifying any one number is futile. A cognitive limit on human group size cannot be derived in this manner.
... sex-specific coevolutionary relationship between the primate brain and social complexity (the social brain hypothesis [130,131]). ...
Article
Never before have we experienced social isolation on such a massive scale as we have in response to COVID-19. Yet we know that the social environment has a dramatic impact on our sense of life satisfaction and well-being. In times of distress, crisis, or disaster, human resilience depends on the richness and strength of social connections, as well as active engagement in groups and communities. Over recent years, evidence emerging from various disciplines has made it abundantly clear: loneliness may be the most potent threat to survival and longevity. Here, we highlight the benefits of social bonds, choreographies of bond creation and maintenance, as well as the neurocognitive basis of social isolation and its deep consequences for mental and physical health.
... Recent evidence speaks to a sex-specific extension of the social brain hypothesis. The neocortex size of primates correlates with group size in females better than it does for males, which suggests sex-specific selection pressures during natural selection (6). On the other hand, the reproductive success of male primates correlated with the size of their neocortex (7). ...
Article
Full-text available
In human and nonhuman primates, sex differences typically explain much interindividual variability. Male and female behaviors may have played unique roles in the likely coevolution of increasing brain volume and more complex social dynamics. To explore possible divergence in social brain morphology between men and women living in different social environments, we applied probabilistic generative modeling to ~10,000 UK Biobank participants. We observed strong volume effects especially in the limbic system but also in regions of the sensory, intermediate, and higher association networks. Sex-specific brain volume effects in the limbic system were linked to the frequency and intensity of social contact, such as indexed by loneliness, household size, and social support. Across the processing hierarchy of neural networks, different conditions for social interplay may resonate in and be influenced by brain anatomy in sex-dependent ways.
... The Machiavellian intelligence or social brain hypothesis argues that the neocortex expanded as hominin groups and social networks became larger and more complex. Across monkeys and apes, neocortex volume, measured as size of neocortex relative to total brain size, relates specifically to female group size, and not male group size, suggesting that female social demands have driven the evolution of intelligence ( Lindenfors, 2005). Coevolving with increased social complexity -and increased costs for mothers -was the capacity for tactical deception (Byrne & Corp, 2004) -and hence for manipulation of "fictions"; while dominant individuals were less and less able to maintain reproductive dominance against Machiavellian alliances (Pawlowski, Lowen, & Dunbar, 1998). ...
Chapter
Full-text available
Are there constraints on the social conditions that could have given rise to language and symbolic cognition? Language has emerged in no other species than humans, suggesting a profound obstacle to its evolution. If language is seen as an aspect of cognition, limitations can be expected in terms of computational capacity. But if it is seen it as fundamentally for communication, then the problems will be found in terms of social relationships. Below a certain threshold of cooperation and trust, no language or symbolic communication could evolve (Knight & Lewis, 2017a); this has been termed a “platform of trust” (Wacewicz, 2017).... In this chapter, I argue that quite specific social conditions were prerequisite for the evolution of language- and symbol-ready hominins. One of the requirements differentiating our ancestors from other African apes was a switch to mainly female philopatry – females living with their relatives, rather than dispersing at sexual maturity – coevolving with an increasing tendency to egalitarianism....How did increasing egalitarianism affect males and potentially “feminize” male behavior for cooperative offspring care? How were male and female relations affected in the evolution of genus Homo and Homo sapiens?
... The Social Intelligence hypothesis, inspired a tremendous research interest, with the majority of research focusing on the linkage between social complexity (e.g. group size) and intelligence (Dunbar 1998;Reader & Laland 2002). Studies in primates suggest that measures of social complexity indeed correlate with neocortex size and reproductive success (Dunbar 1992; Kudo & Dunbar 2001;Lindenfors 2005;Pawłowskil et al. 1998). In addition, the nature of social relationships in primates seems to relate to brain size, irrespectively of group stability and social dynamics (Dunbar 1992; Shultz & Dunbar 2010). ...
... That brain size correlates with social behavior today is evidenced by both behavioral and neurobiological data. Neurobiological comparisons between different primates have indicated positive relationships between relative brain and/or neocortex size and mean group size (Dunbar 1992(Dunbar , 1998Dunbar and Shultz 2007), although some authors have highlighted that this pattern might differ between sexes (e.g., Lindenfors 2005) and across group cohesion metrics (Lehmann and Dunbar 2009). Behavioral data demonstrates that primate species that live complex social lives also have sophisticated cognitive skills, such as social learning (e.g., Bonnie and de Waal 2006), cooperation (e.g., Melis et al. 2006;Boesch 1994;Burkart et al. 2007;Burkart and van Schaik 2010), and possibly a theory of mind (e.g., Call and Tomasello 2008). ...
Chapter
The Machiavellian intelligence hypothesis and the social brain hypothesis have revolutionized traditional views on how primate cognition can be studied. Beyond the study of individual problem-solving capacities of various primates, these hypotheses have demonstrated the close relationship between the complexity of primate social life and the emergence of more sophisticated cognitive skills. The social brain hypothesis demonstrated the existence of a close correlation between the volume of the neocortex and the number of individuals in primate social groups. The amount of studies in this area have increased dramatically and have successfully enhanced our understanding of the evolutionary roots of complex social phenomena, including theory of mind, cultural transmission, social learning, and shared attention. The cognitive capacities present in primates also underlie the evolution of cognitive capacities in humans. This chapter introduces present avenues taken in research on primate social cognition, and it walks the reader through the chapters of this volume.
Chapter
Dusky dolphins (Lagenorhynchus obscurus) exhibit highly flexible foraging and social strategies. Studies in three distinct environments offer a natural experiment for understanding influences shaping dusky dolphin societies. In shallow bays off Patagonia, Argentina, dusky dolphins form small traveling groups during the day in search of small, schooling fish, but fission-fusion of large groups enhances predator detection/avoidance and mating opportunities. Predation risk is also minimized by resting in small groups near shore at night. In the deep open waters off Kaikoura, New Zealand, large mixed age and sex groups and satellite mating and nursery groups occur. Loosely coordinated subgroups forage nocturnally on the deep scattering layer. Large group formation is again an anti-predation strategy. In the shallow wintertime habitat of Admiralty Bay, New Zealand, coordinated bait-ball foraging occurs but in smaller groups than off Patagonia. Outside of the breeding season and in the absence of predation risk, Admiralty Bay grouping patterns are driven by opportunities to secure prey and social partners. Compared to many other delphinids, dusky dolphins are more gregarious yet more loosely bonded. The social brain hypothesis helps to explain the evolution of large relative brain size and complex sociality in dusky dolphins. Bycatch, habitat loss, climate change, and whale-watching are current threats to the species. Application of new technology and research on female behavior, culture, and lesser-studied populations will help to fill knowledge gaps and advance conservation strategies.
Article
Full-text available
We have analysed the relationship between primate mating system, size and size dimorphism by utilizing several phylogenetically based methods. An independent contrast analysis of male and female size (log weight) showed that these are tightly correlated and that size dimorphism is not a simple allometric function of size. We found no relationship between mating system and sexual dimorphism in strepsirhines but a strong relationship in haplorhines. By matched-pairs analysis, where sister groups were matched according to whether the mating system predicted higher or lower intrasexual selection for male size, haplorhine species in more polygynous clades (with a predicted higher sexual selection) were significantly more dimorphic, had larger males, and also, but to a lesser degree, larger females. Both independent contrast and matched-pairs analyses are non-directional and correlational. By using a directional test we investigated how a transition in mating system affects size and dimorphism. Here, each observation is the sum of changes in dimorphism or size in a clade that is defined by a common origin of a mating system. Generally, dimorphism, as well as male and female size, increased after an expected increase in sexual selection, and decreased after an expected decrease in sexual selection. The pattern was, however, not significant for all of the alternative character reconstructions. In clades with an expected increase in sexual selection, male size increased more than female size. This pattern was significant for all character reconstructions. The directional investigation indicates that the magnitude of change in haplorhine dimorphism is larger after an increase in sexual selection than after a decrease, and, for some reconstructions, that the magnitude of size increase is larger than the magnitude of size decrease for both sexes. Possible reasons for these patterns are discussed, as well as their implications as being one possible mechanism behind Cope's rule, i.e. general size increase in many phylogenetic lineages.
Book
1. Introduction 2. Estimation 3. Hypothesis testing 4. Graphical exploration of data 5. Correlation and regression 6. Multiple regression and correlation 7. Design and power analysis 8. Comparing groups or treatments - analysis of variance 9. Multifactor analysis of variance 10. Randomized blocks and simple repeated measures: unreplicated two-factor designs 11. Split plot and repeated measures designs: partly nested anovas 12. Analysis of covariance 13. Generalized linear models and logistic regression 14. Analyzing frequencies 15. Introduction to multivariate analyses 16. Multivariate analysis of variance and discriminant analysis 17. Principal components and correspondence analysis 18. Multidimensional scaling and cluster analysis 19. Presentation of results.
Article
At the most fundamental level, the size of an animal’s home range is determined by its energy needs. In the absence of confounding variables, home range size should therefore scale with body mass according to Kleiber's exponent for metabolic rate of 0.75. Comparative studies in a wide range of taxa have failed to confirm this prediction: home range size has commonly been found to scale with an exponent significantly >0.75. We develop a comparative measure of metabolic needs that incorporates both mass‐specific metabolic rate and social‐group size. We test the prediction that home range size in primates scales isometrically with this measure when an appropriate linear model is applied to data corrected for phylogenetic bias. Analyses using species values as data points indicate an exponent consistent with Kleiber’s law. This result is misleading, however, because ecological factors confound the analysis, and the slopes within some ecologically homogeneous taxa are steeper. Accordingly, in analyses based on independent contrasts with reduced major axis, slopes are significantly greater than predicted by Kleiber's law. We examine the effects of other variables, and we find that systematic variation in substrate use, home range overlap, and diet account for the steeper than expected relationship between home range size and metabolic needs based on Kleiber’s law. We therefore conclude that the scaling of home range size is subject to Kleiber's law but in combination with other factors. These results emphasize that the study of allometry requires detailed attention to statistical models and control of confounding variables.
Article
There are 2 main competing theories on the evolution of group living in diurnal non-human primates. 1) Predation avoidance favours group living; there are only disadvantages to feeding in a group and feeding competition increases with group size. 2) There is a feeding advantage to group living deriving from communal defence of high-quality food patches; predation is not important. A critical test is proposed: the theories differ in the predicted relationship between a female's birth rate and the size of the group in which she lives. An additional test is concerned with the predicted relationship between population density relative to food availability and average group size. Finally, a critical test is proposed of the hypothesis that increasing group size should lead to reduced predation risk by comparing demographic patterns between areas where predators are still present and where they have disappeared. In all 3 tests, results provide strong support for the predation-feeding competition theory and are clearly unfavourable for the theory postulating feeding advantages to group living. Such feeding advantages may, however, gain prominence under some conditions.-from Author
Article
In the current resurgence of interest in the biological basis of animal behavior and social organization, the ideas and questions pursued by Charles Darwin remain fresh and insightful. This is especially true of The Descent of Man and Selection in Relation to Sex, Darwin's second most important work. This edition is a facsimile reprint of the first printing of the first edition (1871), not previously available in paperback. The work is divided into two parts. Part One marshals behavioral and morphological evidence to argue that humans evolved from other animals. Darwin shoes that human mental and emotional capacities, far from making human beings unique, are evidence of an animal origin and evolutionary development. Part Two is an extended discussion of the differences between the sexes of many species and how they arose as a result of selection. Here Darwin lays the foundation for much contemporary research by arguing that many characteristics of animals have evolved not in response to the selective pressures exerted by their physical and biological environment, but rather to confer an advantage in sexual competition. These two themes are drawn together in two final chapters on the role of sexual selection in humans. In their Introduction, Professors Bonner and May discuss the place of The Descent in its own time and relation to current work in biology and other disciplines.
Article
A model suggests that female-bonded (FB) groups have evolved as a result of competition for high-quality food patches containing a limited number of feeding sites. These relationships are beneficial based on cooperative relationships among females. These relationships are beneficial because cooperators act together to supplant others from preferred food patches. Ecological data support the model for most FB species, but not for Theropithecus gelada or Colobus guereza, whose foods are not found in high-quality patches with limited feeding sites. Non-FB species conform to expectation, either because they do not use high-quality patches, or because feeding competition has disruptive effects during periods of food scarcity. Multi-male groups tend to be found in non-territorial FB species. The presence of several males per group is suggested to benefit females by raising the competitive ability of the group in inter-group interactions. Competitive relationships among females are more strongly marked in FB groups.-from AuthorTheropithecus gelada Colobus guereza
Article
At the most fundamental level, the size of an animal's home range is determined by its energy needs. In the absence of confounding variables, home range size should therefore scale with body mass according to Kleiber's exponent for metabolic rate of 0.75. Comparative studies in a wide range of taxa have failed to confirm this prediction: home range size has commonly been found to scale with an exponent significantly 10.75. We develop a comparative mea- sure of metabolic needs that incorporates both mass-specific meta- bolic rate and social-group size. We test the prediction that home range size in primates scales isometrically with this measure when an appropriate linear model is applied to data corrected for phylo- genetic bias. Analyses using species values as data points indicate an exponent consistent with Kleiber's law. This result is misleading, however, because ecological factors confound the analysis, and the slopes within some ecologically homogeneous taxa are steeper. Ac- cordingly, in analyses based on independent contrasts with reduced major axis, slopes are significantly greater than predicted by Kleiber's law. We examine the effects of other variables, and we find that systematic variation in substrate use, home range overlap, and diet account for the steeper than expected relationship between home range size and metabolic needs based on Kleiber's law. We therefore conclude that the scaling of home range size is subject to Kleiber's law but in combination with other factors. These results emphasize that the study of allometry requires detailed attention to statistical models and control of confounding variables.
Article
Ridley (1986) emet une hypothese selon laquelle il existe une relation entre la saisonnalite de la reproduction et le nombre de mâles contenus dans un groupe de primates. Cet article discute cette hypothese
Article
Primates use social grooming to service coalitions and it has been suggested that these directly affect the fitness of their members by allowing them to reduce the intrinsic costs associated with living in large groups. We tested two hypotheses about the size of grooming cliques that derive from this suggestion: (1) that grooming clique size should correlate with relative neocortex size and (2) that the size of grooming cliques should be proportional to the size of the groups they have to support. Both predictions were confirmed, although we show that, in respect of neocortex size, there are as many as four statistically distinct grades within the primates (including humans). Analysis of the patterns of grooming among males and females suggested that large primate social groups often consist of a set of smaller female subgroups (in some cases, matrilinearly based coalitions) that are linked by individual males. This may be because males insert themselves into the interstices between weakly bonded female subgroups rather than because they actually hold these subunits together.