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M.Sc. in Human Evolution and Behaviour Dissertation
Neurological sexual dimorphism and competing selection pressures
Monica Nelson
Dissertation submitted in partial fulfilment
of the requirements for the degree M.Sc. in Human Evolution and Behaviour (UCL)
of the University of London in 2011
Word Count: 18,543
UNIVERSITY COLLEGE LONDON
DEPARTMENT OF ANTHROPOLOGY
Note: This dissertation is an unrevised
examination copy for consultation only
and it should not be quoted or cited
without the permission of the
Chairman of the Board of Examiners
M.Sc. in Human Evolution and Behaviour (UCL)
i
Declaration of originality
This is to certify that the work is entirely my own and not of any other person, unless
explicitly acknowledged (including citation of published and unpublished sources).
The work has not previously been submitted in any form to the University College of
London or to any other institution for assessment for any other purpose.
Signed _________________________________________________
Date ___________________________________________________
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Abstract
Sexual selection, sexual dimorphism, and the encephalization of primates are all
extremely hot topics in the field of physical anthropology, as well as the natural
sciences more generally. With this project, the intersection of these three issues was
studied with the aim of discovering how all three have come to bring about the
differences we see in the relative brain sizes between male and female primates. The
relationship between phylogeny, body size, diet and reproductive strategy were
explored in an attempt to ascertain whether the differences, where they exist, have
evolved as the result of natural selection, sexual selection, or are simply the result of
canalization.
In order to answer the question of why relative brain size differences exist between
males and females, as well as why they are more marked in some species, a number
of statistical analyses were conducted using raw data provided by the Isler et. al.
(2010) data set.
The initial statistical tests were a series of basic pair-wise
comparisons, involving one-tailed t-tests, comparing males and females along the
dimensions listed above. Upon completion of the pair-wise analyses, a phylogenetic
generalized least squares (PGLS) analysis of 139 of the 212 usable data points was
conducted. Once the taxonomic relationships were established and phylogeny had
been controlled for, results of the pair-wise comparisons were re-evaluated in order
to ascertain whether there were any obvious trends apparent in the data. The results
of these analyses indicate that there appear to be different selection pressures
operating on males and females. It also seems to be the case that encephalization
may be a primitive trait in females, but derived in males, as the range of residual
values (based on the slope predicted by the model generated by the PGLS analysis)
for males was much wider than that for females.
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Table of Contents
CHAPTER 1 ................................................................................................................ 1
INTRODUCTION ....................................................................................................... 1
1.1: Study Background ............................................................................................. 1
1.2: Dissertation Structure ........................................................................................ 3
1.3: Aim and Objectives ........................................................................................... 4
CHAPTER 2 ................................................................................................................ 5
LITERATURE REVIEW............................................................................................. 5
2.1: Introduction ....................................................................................................... 5
2.2: Natural Selection and Sexual Selection ............................................................ 6
2.3: Sexual Dimorphism without Sexual Selection ................................................. 8
2.4: Neurological Sexual Dimorphism................................................................... 11
2.5: Encephalization and Neotonization ................................................................ 14
CHAPTER 3 .............................................................................................................. 18
DATA AND METHODS........................................................................................... 18
3.1: Introduction ..................................................................................................... 18
3.2: Data Used ........................................................................................................ 18
3.2.1: Spatial and temporal characteristics ......................................................... 19
3.3: Methods and techniques .................................................................................. 19
3.3.1: Data Analysis ............................................................................................... 20
3.3.1.1: Family ................................................................................................... 20
3.3.1.2: Body Size .............................................................................................. 21
3.3.1.3: Diet ........................................................................................................ 22
3.3.1.4: Reproductive Strategy ........................................................................... 23
RESULTS .................................................................................................................. 25
4.1: Introduction ..................................................................................................... 25
4.2: Results of Pair-wise Comparisons of Male and Female EQ ........................... 25
4.2.1: Family………………………………………………………………..26
4.2.2: Body Size…………………………………………………………….29
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4.2.3: Dietary Composition…………………………………………………30
4.2.4: Reproductive Strategy……………………………………………….31
4.3: Discussion of results…………………………………………………………31
CHAPTER 5 .............................................................................................................. 34
DISCUSSION ............................................................................................................ 34
5.1: Introduction ..................................................................................................... 34
5.2: Discussion ....................................................................................................... 34
5.2.1: Results by Family……………………………………………………33
5.2.2: Results and Body Size……………………………………………….36
5.2.3: Results and Diet……………………………………………………...37
5.2.4: Results and Reproductive Strategy…………………………………..40
5.2.5: Synthesis……………………………………………………………..42
5.2.6: Consideration of Results in light of a few major hypotheses………..46
CHAPTER 6 .............................................................................................................. 51
CONCLUSIONS ........................................................................................................ 51
6.1: Conclusions ..................................................................................................... 51
6.1.1: Is one sex more encephalized than the other?......................................49
6.1.2: Is encephalization a primitive or derived trait?...................................50
6.1.3: Is there a relationship between body size, encephalization and sex?..51
6.1.4: Correlation between encephalization and other variables analyzed?..52
6.2: Recommendations ........................................................................................... 56
REFERENCES........................................................................................................... 58
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List of Tables and Figures
Tables
Table 1: EQ by family……………………………………………….………………25
Table 2: EQ by body size……………………………………………………………31
Table 3: EQ by dietary composition……………………………..………………….31
Table 4: EQ by reproductive strategy……………………………………….………32
Figures
Figure 1: Phylogram of 139 primate species……………………………………….28
Figure 2: Scatterplot of model residuals for species and sex including slope……...29
Figure 3: Scatterplot of model residuals for species and sex by family…………....30
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CHAPTER 1
INTRODUCTION
1.1: Study Background
The encephalization of mammals, and primates in particular, has been the focal point
of many studies (Pilbeam & Gould 1974; Roth & Dicke 2005; Williams 2002;) over
the past four decades. A great deal of time and energy has gone into generating and
testing hypotheses based on the idea that the extreme encephalization seen in
hominids is a key feature, if not the key feature, in having giving modern humans an
evolutionary advantage over a number of other species. Several studies have been
done comparing rates of encephalization in birds, mammals, and primates (Roth &
Dicke 2005; Jerison 1979; Healy and Hurly 2004). Interestingly, very little work has
been done comparing rates of encephalization between males and females, though a
cursory glance at the values found in the data available (Isler et. al. 2010) indicates
that, in several species, female primates are more encephalized than males. Whether
or not relative brain size tells us anything about intelligence or means anything at all
in terms of cognitive advantage is still up for debate, but the question of whether
genuine differences in relative brain size exist between males and females is an
interesting one, especially when considered in light of current models of selection.
At least one researcher has argued that the high EQ found in modern humans, both
male and female, may be the result of repeated exposure to famine conditions
(Amen-Ra 2007), which ultimately gave rise to the neotonous proportions seen in
humans today. In support of what Amen-Ra has dubbed to as the nutritional
neurotrophic neotonization (N3) theory are the results of several experiments which
“indicate that dietary restriction promotes the preservation and generation of neurons
via induction of neurotrophic factors” (2007 p. 1147). When food becomes scarce
or less regularly available, the brain of an animal faced with these conditions
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becomes more neuronally dense. If this theory holds, it may be the case that the
extreme encephalization found in female primates is simply the result of the heavy
relative functional demands associated with oestrous, pregnancy and lactation. The
resultant nutritional compromise these conditions give rise to in fertile females,
coupled with the need to maintain a certain level of cognitive sophistication in order
to successfully meet the demands of reproduction and juvenile rearing while
navigating what are often extremely precarious environmental conditions, may
explain why so many female primates exhibit such high EQs.
The cognitive
demands associated with membership in a complex social system preclude the loss of
neural tissue so the body is reduced to offset the nutritional deficit imposed by
ecological constraints. The overall reduction in somatic tissue may ultimately result
in vastly different relative brain sizes between the sexes, even if the reduction occurs
in infinitesimally small increments over many generations. Under this model smaller
female body size then is not the result of male-male competition, female choice, or
any sort of sexual competition, but the by-product of social selection or natural
selection operating at the species level.
Earlier work done by Plavcan (2001) suggests a similar possibility.
In his
contribution to the 2001 Yearbook of Physical Anthropology Plavcan outlines a
number of explanations for dimorphism, beyond sexual selection, that may give rise
to sexually dimorphic traits. The very first of the topics he covers is body size.
Simply by virtue of being larger or smaller overall, a species may exhibit more or
less dimorphism in any number of traits. Bigger animals show greater levels of
dimorphism than smaller ones, generally speaking. The various explanations for
why this is so will be covered in greater detail in the literature review section of this
paper, but assuming this model is correct, we have yet another line of evidence in
support of a theory in which sexual dimorphism is not the result of sexual selection
and the significance of differences in EQ between the sexes may once again be
brought into question. Before these matters may be examined, however, the question
of whether female primates are actually more encephalized must be resolved.
Additionally, we must look at whether encephalization in both sexes is a primitive or
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derived trait. These two questions are the primary focus of the present research
project.
1.2: Dissertation Structure
The structure of this dissertation will follow standard guidelines as proposed by the
scientific community.
The balance of chapter one will clarify the aims and
objectives of this study. Chapter two consists of a literature review in which the
themes mentioned in the introduction above are addressed in further detail and
additional relevant concepts are explored. Section one of chapter two discusses
natural selection versus sexual selection and the relationship between these two
concepts. Section two explores how sexual dimorphism may arise in the absence of
sexual selection and section three offers a brief survey of the literature on EQ and
neurological differences between the sexes. The final section of chapter two deals
specifically with the literature on the encephalization and neotonization of females.
Chapter three provides an explanation of the methods used in this study to ascertain
whether any real differences in EQ exist between male and female primates. First,
basic statistical analyses done to ascertain whether there are any quantifiable
differences in the body, brain, and relative brain sizes of the animals studied are
described. Second, an account is given of the phylogenetic analyses done to
determine whether the differences, where they exist, are the result of phylogenetic
constraints or whether independent selection forces have been operating to facilitate
the divergent developmental trajectories.
Chapter four provides the results of the analyses detailed in chapter three and a brief
discussion of said results. Chapter five examines the results in light of the theories
examined in chapter two and discusses other possibilities that the results may
suggest. The final sections of chapter five explore how the results of this study align
with a few major hypotheses regarding encephalization.
Chapter six consists of a conclusion and recommendations for further study. A recap
of the hypotheses examined and implications of the results are considered in this
final section.
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1.3: Aim and Objectives
As explained in the introduction above, much has been made of the significance of
brain size in establishing and securing H. sapiens’ position at the top of the food
chain. The idea that bigger is better when it comes to brains has, however, undergone
a number of modifications over the past 150+ years. At present, the dominant line of
thought both inside and outside the scientific community is that what counts is
relative brain size, rather than absolute. Concurrent with the research being done on
EQ, a number of studies have been done with the aim of ascertaining whether males
and females are neurologically dimorphic (Lindenfors et. al. 2007; Renius et. al.
2008; Goldstein et. al. 2001). In the present study both topics with be addressed,
looking at the following questions:

Across the primate order, does one or the other sex exhibit a trend toward
greater encephalization?

In families where one or the other sex is more encephalized, is this trait the
result of canalization, or is it derived?

What is the relationship between overall body size and encephalization?

Is there a correlation between relative brain size and diet, body size, or
reproductive strategy?
In the next chapter the relevant literature will be reviewed and pertinent concepts will
be clarified. Following this, data on 176 primate species taken from studies
conducted over the past several decades (Isler et. al. 2008) will be statistically
analyzed both statistically with the above questions in mind.
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CHAPTER 2
LITERATURE REVIEW
2.1: Introduction
In the previous chapter a number of questions were raised in the aims section. These
questions are interesting in themselves, but the genuine significance of them is rooted
in what the answers may tell us about the major theoretical frameworks that scientists
are operating under today. There is little doubt that natural selection gives us a
correct account of how things evolve in the natural world, but the consensus that
seems to be have been reached regarding the general theory doesn’t appear to have
carried over to some of the ancillary theories and concepts that have sprung from it.
There still exists a great deal of difference of opinion regarding how best to
understand things like directional selection (Hamon, 2005; Kingslover & Diamond,
2010; Hereford et. al., 2004) and kin selection (Okasha 2009; Wilson 2011; Coyne
2011).
The widely accepted theory of sexual selection is no exception. Though
there is little dispute over whether sexual selection is a significant factor in
evolutionary processes, there is still a great deal of confusion regarding what counts
as a sexually selected trait and just how strong a force sexual selection actually is.
Moreover, what exactly the relationship is between sexual dimorphism and sexual
selection is is not terribly clear (Plavcan 2001).
In this chapter, some of the literature dealing with the issues discussed above will be
surveyed and neurological dimorphism will be considered in light of them. In the
first section the broadest concepts, those of natural and sexual selection, and the
relationship between them is explored. In the second, one of the possible results of
these two forces acting on one another, sexual dimorphism without sexual selection
is discussed. In the last two sections the relevant literature discussing neurological
dimorphism and encephalization, the traits analyzed in this study, is covered.
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2.2: Natural Selection and Sexual Selection
Though the same overarching principles that govern natural selection apply in equal
measure to sexual selection, the two processes often seem to act in opposition to one
another (Gould 1974; King 1989; Nevo & Belles 1989; Estrada & Jiggins 2008).
Variation, heritability, overpopulation, and differential fitness are factors in both
types of selection, but while sexual selection may reasonably thought of a subclass in
the class of all pressures that drive natural selection, it is often the case that sexual
selection appears to either cancel out or override to be more general interspecies
natural selection pressures such as those resulting from ecological or physiological
constraints. This one aspect of natural selection is of such key importance that
Darwin followed up his own seminal work (1859) with a second tome, The descent
of man, and selection in relation to sex (1871), which was entirely devoted to trying
to explain the mechanisms involved in it. In this section the relationship between
interspecies competition, or natural selection broadly speaking, and sexual selection
is explored.
Ultimately, the key difference between natural selection and sexual selection lies
between the species, or the population, and the individual. Natural selection and
sexual selection are not two distinct processes, but rather the same process working
at different taxon levels. Natural selection works at the interspecies level to create
new species, whereas sexual selection involves intraspecies selection. Competition at
the intraspecies level involves members of the same sex who compete to secure
reproductive opportunities (Reynolds, J. D. and Harvey, P.H. 1994; Strier 2011).
This type of competition often gives rise to phenotypically dimorphic traits between
males and females. Darwin attributed the widespread occurrence of traits that seem
to serve no purpose with regard to survival, such as bawdy colouring or heavy
ornamentation, to this type of selection (1871). Robert Trivers (1972) later refined
the hypothesis, by explicitly outlining the roles of male-male competition and female
mate choice. Since that time a number of other models of selection have been
suggested and the clarity of these earlier hypotheses has become slightly muddled.
Phenotypes once thought to be the result of sexual selection have begun to be re-
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examined and considered in light of less obvious benefits that they may confer at a
much broader level.
Traits that have historically been classified as having been evolved as a result of
sexual selection, such as canine tooth length and body mass dimorphism, are not
necessarily secondary sexual characteristics at all.
A number of researchers
(Clutton-Brock et al., 1977; Leutenegger and Kelly, 1977; Harvey et al., 1978;
Martin et al., 1994; Plavcan and van Schaik, 1994) have looked at the possibility that
these features are actually the byproduct of natural selection, resulting from the
heavier ecological demands on one sex or the other.
Even more interestingly,
certain traits that may evolve as the result of sexual selection can be lost as a result of
natural selection pressures, and traits that may have originally evolved under one or
the other type of pressure may be reinforced or exaggerated as a result of a different
pressure.
Kingslover and Diamond (2010) discuss in some detail the various mechanisms that
may limit the strength of directional selection. The points they raise, however, may
be applicable to any given type of selection. They identified five different ways in
which the selection strength may be compromised. Among the mechanisms they
discuss are 1) a limited genetic variation, 2) trade offs between different selection
pressures such as those discussed in the previous paragraph, 3) direct selection on
one trait which results in correlated, indirect selection on a trait in the opposite
direction, 4) changes in selection pressure over time and 5) the possibility that
stabilizing selection is stronger and more common than was previously thought. At
least the first three points mentioned above should be borne in mind when evaluating
sexually dimorphic traits, as it often the case that environmental constraints cap what
would otherwise be runaway sexual selection, and it is always the case with sexually
reproducing organisms that genetic variation is linked with primary sex differences.
The results from studies involving a variety of plants, insects, and animals have
shown that the points considered by Kingslover and Diamond are empirically
supported. Even in plants there exists a constant push-pull relationship between
natural and sexual selection (Bond and Maze 1999; Ashman 2003; Delph et. al.
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2004), with ecological features limiting or enhancing the extent of dimorphism in
flowering plants. Likewise, with insects (Estrada and Jiggins 2008), fish (Hamon
2005), reptiles (King 1989), birds (Karubian and Swaddle 2001) and mammals
(Gould 1974). In mimetic insects, such as butterflies and moths, natural selection
may work to enhance the effect of sexual selection, or perhaps vice versa, by
enhancing the ability of males to detect mates and predators. The biochemical
processes involved in mate recognition have simultaneously evolved to assist in
predator avoidance (Estrada and Jiggins 2008).
In fish, predators more easily
identify showy males. Therefore, when the risk of predation is high the less sexy,
duller-coloured phenotypes are more successful at both reproducing and staying alive
(Hamon 2005). The longer tail length seen in many male snakes appears to be a
byproduct of both natural and sexual selection in that longer tail length in males is
the result of morphological constraints on the entire order, or natural selection, while
shorter tail length in females enhances reproductive output, giving shorter-tailed
females an advantage over other females of their own species (King 1989). Here
sexual, selection is working on one sex while natural selection is driving the same
phenomenon in the other. In birds, a very similar scenario appears to have played
out with regard to wing length. The gap in wing size is the result of different
selection pressures on males and females. Ecological constraints work to put a cap
on female size while male-male competition has simultaneously favours broader
wingspan in males. Mammalian examples also pervade the literature, with Gould’s
famous Irish Elk example (1974) being one of the most famous. In this case, antler
size is restricted by natural selection constraints while sexual selection drives has
driven an increase size. Females prefer males with large antlers and males with large
antlers fare better in contests with other males, but once a certain limit is reached the
costs to the animal in terms of nutrition and its ability to successfully navigate the
environment are too great to allow for any further increase.
2.3: Sexual Dimorphism without Sexual Selection
Having surveyed the ways in which natural and sexual selection both work together
and in opposition to one another, this section will be devoted to examining scenarios
8
in which sexual dimorphism may arise without sexual selection as the primary
driving force. In a fairly comprehensive discussion of this topic Plavcan (2001)
states, “Dimorphism in various traits is known to be correlated with body mass, diet,
substrate, phylogeny, and even rainfall” and points out that “Each of these
correlations may reflect a variety of different mechanisms affecting the expression
and evolution of dimorphism” (p. 40). How some of these factors may influence the
development of sexual dimorphism will now be explored.
The correlation between body size and dimorphism found in many primates is not
unique to the family and has been shown to exist in a number of species. Plavcan
2001 p. 41) noted that, “Sexual dimorphism in body mass and canine tooth size is
correlated with overall body size (Clutton-Brock et al., 1977; Harvey et al., 1978;
Leutenegger and Cheverud, 1982, 1985; Gautier-Hion and Gautier, 1985; Cheverud
et al., 1985; Plavcan and van Schaik, 1992, 1994, 1997b; Pickford, 1986; Plavcan,
1999)”, explaining that with an increase in the overall size of the animals in
particular species, there is an accompanying increase in the quantitative distance
between male and female body size. Essentially, the bigger the animal in question is,
the greater the degree of dimorphism will be. In smaller animals, the difference in
size between males and females will be less than that found between males and
females in larger species. So, in large animals a larger male may be much larger than
his female counter part, simply by virtue of the fact that the animals are large, rather
than as the result of sexual selection.
The relationship between body mass and degree of dimorphism is not necessarily
allometric, however. Males may far exceed or fall below the predicted mean size for
the trait in question (such as height, weight, cranial volume, etc.) and, likewise, for
females. A number of explanations for how this may come to pass have been
suggested. Clutton-Brock et. al. (1977) have offered five ways in which dimorphism
can arise that may undermine a strictly allometric model, which are also not the
result of direct sexual selection.
First, there may be a correlated response between sexes if larger body size is selected
for in either. If ecological conditions favour an increase (or decrease) in size for
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males, then females may become larger as well and vice versa. Second, among
larger animals there are fewer species competing for the same resources. This may
in turn translate into fewer constraints on body size, especially among males.
Because competition is low at this level, males may grow unchecked regardless of
whether there is intraspecies competition, and if either sex can grow unchecked, the
gap in size between the two will widen even more than it would if both were kept in
check in the same manner and to the same extent. In this case it wouldn’t be a case of
larger size being selected for, but an absence of a selection pressure against it. Third,
there may be less cost involved with an increase in size for males. This possibility
will be taken up in further detail in the following sections, but essentially what this
means is that the metabolic demands of building and sustaining the body of a female
animal may be more costly in terms of resources than that for males, so female
growth may be limited while male is less so. The fourth mechanism suggested is a
possible reduction in feeding competition where the food quality is poor and the
species in question feeds in clumps. A marked difference in size between the sexes
may offset the natural competition for resources by reducing the caloric or nutritional
needs of the smaller sex. Here, gorillas may provide a good example. The quality of
their diet is generally quite low, they feed together, and females are significantly
smaller. The females are roughly half the size of males and, as a result, require far
few calories to meet their own metabolic demands. The fifth and final suggestion
they outline is closely tied to the third. In this case, the idea is that there is pressure
on females to remain smaller in order to reach maturity sooner. The body of any
animal can only mature as quickly as resources in the environment can provide
nourishment and facilitate growth, so a smaller adult body size is more quickly and
easily reached than a larger one.
Whether any one, or all of, the five mechanisms outlined above is empirically
supported is still up for debate, but a number of studies conducted since the paper
cited above was originally published have shown that they do seem to offer viable
alternatives, or perhaps complementary adjuncts, to the sexual selection hypotheses
(Kappeler, 1990, 1991; Godfrey et al., 1993; Mitani et al., 1996; Plavcan and van
Schaik, 1997b; Plavcan, 1999). Group size, dietary composition and quality, and
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ecological constraints do influence the extent to which dimorphism in body mass
may manifest itself in a given species.
Contrast analyses have shown there is
correlation between shifts in expected values based on allometry and these elements,
demonstrating that sexual selection alone should not be regarded as the sole
contributing factor when evaluating size differences between males and females.
Additionally, there are cases where both natural and sexual selection are working
alternately to shape a particular trait, but sexual selection is not the primary force at
work. For example, in any given species, the size of the individual animals will
influence the type of social structure that evolves for the species. This in turn
influences mating behaviour, making what may have been a trait that originally
evolved as result of natural selection pressures shift in one direction or the other
under sexual selection pressure. Plavcan provides an illustration, pointing out that “at
larger body sizes, females tend to form large groups which makes it easier for males
to try to exclude other males from access to females” (2001, p. 41). Here, the larger
body size of females may have originally evolved as a result of a correlated response
to an increase in male body size (which may have evolved as a result of any of the
natural selection mechanisms discussed above). The increase in size results in a
change in social behaviour which in turn makes it easier for males to monopolize
females, making the large male offspring of large females more successful
reproductively and perhaps more attractive as suitors of the large, clumped females.
The large body size that originally evolved as a result of natural selection pressures is
then perpetuated as a result of sexual selection. Of course these mechanisms may
also be operating in a similar manner at the level of much more specific traits or
phenotypes. Sexual dimorphism may be exhibited in something as unique as a single
tooth or even a small section of the brain. In the next section some of the literature
on neurological sexual dimorphism, as expressed via differences in the brain, will be
surveyed.
2.4: Neurological Sexual Dimorphism
Current research on the subject of neurological sexual dimorphism is predominantly
aimed at discovering differences in certain structures or substructures within the
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brain (Lindenfors et. al. 2007; Renius et. al. 2008), as well as microscopic and
biochemical dissimilarities between male and female brains (Shah et. al. 2004;
Cosgrove et. al. 2007). This has not, however, always been the case, and the larger
issue of overall differences in brain size has remained a hot topic (Gittelman 1994;
Nyborg, H. 2005). Because the main focus of this research project is brain size
dimorphism, and relative brain size more specifically, the bulk of this section will be
directed at an examination of the literature regarding overall brain size, first in terms
of gross size difference and second in terms of relative difference.
As mentioned previously, overall brain size has long been recognized as a significant
feature in animals that exhibit cognitively complex behaviours. The idea that bigger
equals better, or at least smarter, is one that goes back at least a century and a half
(Darwin 1871; Northcutt 2001). Sheer volume of grey matter does seem to correlate
with an ability to perform intellectually demanding tasks, at least in humans (Pilcher
2004; Haier et. al. 2004). We also have a great deal of evidence that large brains and
intelligence often go hand in hand in other animals and, though the matter of what
intelligence properly consists in is far from settled, other apes, cetaceans, and
elephants have long been recognized as particularly intelligent animals (Roth and
Dicke 2005; Marino 1998). All of these large-bodied mammals possess brains that
are exceptionally large, particularly when measured against the brain sizes of animals
with similar body sizes in other classes. For example birds, such as the ostrich and
emu, have far smaller brains than apes though their body size is quite similar
(Bennett and Harvey 1985). The same holds true for reptiles, amphibians, and fish.
The general consensus at present is that it is complex social behaviour in conjunction
with the demands of reproduction under precarious ecological conditions have driven
the trend toward greater encephalization in mammals, relative to that of other
animals of similar size in other classes (Shultz and Dunbar 2010; Barrickman et. al.
2008). The trend is especially pronounced in primates (Deaner et. al. 2006), but
12
differences in brain size are also found within families in other orders that are
consistent with this position (Gittelman 1994). Interestingly, the differences in brain
size between species in the same family are most marked between females. For
instance, Taylor and van Schaik (2007) found that among pongids differences in diet
quality, life history, and habitat translated into differences in brain size amongst
females from species to species, but not males. In a similar vein, Gittelman observed
that brain size differences corresponded to differences in ecology and life history in
female terrestrial carnivora but males showed no such pattern. If ecological and
evolutionary pressures are exerting greater force (in either direction) on overall brain
growth in females than in males, one sex or the other will end up with larger brains.
The general pattern in mammals is one in which it is typically males who have
evolved to possess greater absolute brain size.
Absolute brain size may not actually be a particularly significant issue, however. If
the same pressures that have brought about a reduction in brain size have also driven
an overall reduction in the size of the entire animal one would not expect the smaller
animals to have brains the same size as that of the larger ones. Likewise, we would
predict that two animals of the same species, of different sizes, would have different
sized brains, just as we would expect them to exhibit differences in sizes of most of
their organs. What would be unusual would be an overall reduction in size without a
corresponding decrease in brain size.
Simply measuring gross brain size without
taking into consideration changes in the physiology of the entire organism may
create a misleading picture of what is actually taking place as, in these cases, the
dimorphism isn’t actually neurological but rooted in a difference in overall body
mass. The difference in brain size may be strictly allometric and, therefore, not
indicative of anything particularly interesting about brains or their specific evolution.
This brings us to our second topic of consideration, relative brain size.
Because females are generally smaller overall in most dimorphic species, it is
expected that female animals will have smaller brains than their male counterparts.
Having less overall body mass, it stands to reason that specific parts of their anatomy
13
will also be smaller. Bearing this in mind, neurological dimorphism must also be
considered in terms of relative brain size. Unfortunately, because there is little
agreement on how best understand and measure differences in relative brain size, the
body of literature on this topic is far more limited than that involving research on
overall brain size. For reasons explained in the earlier section on sexual dimorphism
and sexual selection (Plavcan 2001), it is not entirely obvious what sort differences
we should expect to see here. Moreover, what the appropriate mathematical model
for determining EQ, or measurements from the expected relative brain size, has not
been established (Williams 2001; Jerison 1979; Pilbeam and Gould 1974). That said,
there is a relatively large corpus of raw data available (Isler et. al. 2008) for analysis
that may be used with any of the models currently suggested. With this project, I
hope to shed further light on the question of whether there exist legitimate
differences in relative brain size, using this data. If the differences in size are simply
allometric, this one line of inquiry may finally be put to rest. If not, fodder for
further research will be made available.
Before moving on, however, hypotheses
involving explanations of how encephalization occurs in the first place will be
considered.
2.5: Encephalization and Neotonization
Amen-Ra’s 2007 paper introducing the neurotrophic neotonization theory is not the
first essay to suggest a hypothesis of this sort. The idea that brain size and density
increases with repeated exposure to famine conditions is one that has been present in
the scientific literature for some time. One of the earliest, now widely cited, research
projects asserting a correlation between brain size increases with a reduction in
certain postcranial structures was conducted by Aiello and Wheeler (1995). The
findings from their project were documented in paper that established what has come
to be known as the expensive tissue hypothesis. Amen-Ra and a number of other
researchers have been working since that time to explain, with greater and greater
precision, how exactly this process may have occurred in physiological terms. In this
section the research and literature on this phenomenon will be examined and
discussed.
14
A great deal of work has been done investigating the metabolic requirements
involved in developing and maintaining large brains and much has been discovered
(Magistretti et. al. 1999). In humans, the brain makes up less than 2% of the total
body weight but is responsible for 20-25% of an individual’s energy consumption
(Magistretti et. al. 2000; Raichle and Gusnard 2002). In other primates the energetic
demands of the brain varies from species to species but tends to be relatively high as
well, though not as high as it is in humans (Magistretti et al. 2000).
How we’ve
evolved to meet the energetic demands of our large brains appears to have involved a
forfeiture of other metabolically demanding tissues. In humans, the loss of gut tissue
is one of the most obvious places where this trade-off has occurred (Aiello and
Wheeler 1995), but the overall volume of post-cranial lean tissue is markedly less in
primates than in a number of other animals outside of the order with similar brain
sizes (Roth and Dicke 2005).
In order to understand the shift toward greater encephalization seen not just in
humans, but across the entire primate order as well, it is necessary to look at both
proximate and ultimate causes. The physiological processes that occur within the
animals are what bring about actual changes in morphology, but they are driven by
external events. Research focusing on the evolution of what has been termed the
human quadripartite complex (Amen-Ra 2006) has been key in helping expand our
understanding of how extreme encephalization occurs. Investigations involving the
connection between long lifespan, low reproductive potential, lengthy development
and high brain/bodyweight ratio in hominid populations have resulted in discoveries
relating to both the proximate and ultimate causes of encephalization.
The N3 hypothesis, which lays out the metabolic processes, or proximate causes, that
have resulted in the extreme encephalization we see in modern human beings is
explained as follows
…humans exhibit an altered pattern of neurotrophin expression resulting
from positive selection for heightened intelligence amidst environmental
deterioration and consequent dietary deficiency. The altered pattern of
neurotrophin expression exhibited by humans, it is deduced, results in a
15
protracted phase of developmental neurogenesis and a resultant retention of
neurons that would otherwise be extirpated due to programmed cell death.
Importantly, during neonatal neurogenesis mammals produce an excess
number of neurons whose eventual destruction is dictated by neurotrophic
factors (Amen-Ra 2007, p. 1147).
In layman’s terms what this says is that, under famine conditions, brain tissue is not
only preserved but new growth is triggered as well. Moreover, the normal loss of
brain tissue that would occur under non-famine conditions is inhibited. This process
is crucial to understanding how something like Aiello and Wheeler’s expensive
tissue hypothesis may work. In that case, the gut tissue would be reduced over time
just as all lean tissue would be, but the brain is preserved and grows. Over several
generations, incremental growth of the brain without immediate concomitant postcranial growth and further gut reduction results in the evolution of a relatively small
ape with a large brain. This is not, however, a Lamarckian explanation. There is a
genetic component, common to a number of mammals, driving the process described
further below.
Studies involving mammals both inside and outside the primate order have shown
that the metabolic activities that brought about an increase in the relative brain size
of hominids are not unique to humans (Burkhalter et. al. 2003). The biochemical
processes that are set in motion when an organism is faced with a shortage of
resources lead to the preservation or growth of new neural tissue in other animals as
well (Wang et. al. 2006).
As a mammalian body begins to waste, post-cranially,
chemical signals triggering both brain preservation and growth are initiated by a
series of interconnected metabolic actions. Studies contrasting the effects of famine
on various animals showed that in rats an “increased expression of genes encoding
orexigenic, hypothalamic peptides such as neuropeptide Y, agouti-related protein,
and pro-opiomelanocortin” (p. 232) may be tied to changes that take place in the gut
tissue of the animals during the final stages of starvation. If the rats survive this last
phase and refeeding commences the changes resulting from the influence of the
neuropeptides on the brain are not reversed, the normal breakdown simply resumes.
16
The increased encephalization is the result of epigenetic factors, but it is the
expression of certain genes that determine gut reduction and neuropeptide increases.
As such the increase in brain size, or at least the propensity for it, is to a certain
degree heritable. If the mechanisms driving the propensity for brain growth are even
partially driven by a genetic component, natural selection can operate on them. If
natural selection is operating on a trait, we may expect to see differences in the
degree to which that trait is expressed in different populations. In this case, if famine
is bringing about an increase in the growth of neurological tissue in conjunction with
the loss of postcranial tissue, we might predict that populations that more susceptible
to the effects of famine, in terms of mortality and reproductive success, may show a
greater degree of encephalization.
17
CHAPTER 3
DATA AND METHODS
3.1: Introduction
To test the hypothesis that greater relative brain size has been selected for in one sex,
or the other, a data set collected by Isler et. al. (2008) from an earlier study involving
research on primate endocranial volume was used. The original set assembled by
Isler and colleagues included measurements of endocranial volume and body mass
for 276 primate species, and was sorted according to sex. The data for these animals
had been obtained from a number of earlier published studies conducted on both wild
and captive populations of primates from all over the world. For the purpose of
testing the hypotheses laid out previously, the data for the animals included in this
project were statistically analyzed along four dimensions. These categories included
family, body size, diet, and reproductive strategy. Once each of these quantitative
analyses was complete, phylogeny was controlled for and results were re-evaluated.
3.2: Data Used
The data that was used for this research paper involved only 213 of the original 276
animals included in the original data set from the 2008 study by Isler et. al.. The 63
animals that were not included were rejected on the basis of incomplete information.
With these animals values for body size, endocranial volume or sex were missing
from the data set. Additionally, for certain analyses, such as diet and reproductive
strategy, subspecies were omitted from the analysis in order to avoid skewing the
results on the basis of redundancy (for example only data for only one subspecies of
P. troglodytes was used, rather than all four of the subspecies of common
chimpanzee, in the omnivore group).
18
3.2.1: Spatial and temporal characteristics
The original data, which comprise the data set used in this study, was collected and
compiled by researchers from all over the world over a period of several decades.
The studies included began in the middle of the 20th century and culminated with the
with the Isler et. al. study in 2008. The numbers reported all represent mean values
of measurements taken for each species, or subspecies, of each sex. Endocranial
volumes were contributed by researchers working on the 2008 study with additional
data provided by Harvey and Clutton-Brock (1985), Verheyen (1962), Hopf and
Claussen (1970), Bronson (1981), Ikeda and Watanabe (1966), Hershkovitz (1970),
and Elton et. al. (2001). In some cases actual brain mass volumes were collected but
these numbers were not provided. All cranial data was listed in terms of endocranial
volume.
Information on body mass was also collected by the research group
working on the Isler et. al. study, with additional contributions from Smith and
Jungers (1997), Gordon (2006), Araujo et. al. (2000), Schulke
et. al. (2004),
Thalmann and Geissmann (2000)and Kappeler (1991). Information on data quality
and the number of animals included measured for each species was also collected
and included with the data set.
3.3: Methods and techniques
Because the data did not include either actual brain volumes or encephalization
quotients, both measurements needed to be estimated. In the case of the former, the
model recommended by Rightmire (2004) was followed. Brain mass was estimated
by taking the endocranial volume, multiplying it by 0.976, and then multiplying that
figure by 1.147. Once brain mass volumes for all the animals were obtained, the
encephalization quotient was determined by dividing brain mass volume by body
mass volume and multiplying that figure by a slope measurement of 0.28 for each
animal. The decision to use William’s (2002) recommended slope of 0.28, rather
than 0.67 or 0.75 (Jerison 1979), was motivated by two factors. First, William’s
formula is the only one specifically geared toward measuring the encephalization of
primates. Previous suggested slopes were aimed at assessing encephalization of
either all terrestrial animals, including birds and reptiles, or all mammals. William’s
19
formula is the only one of the three that specifically takes into account phylogeny.
Additionally, 0.28 is the most conservative of the three slopes suggested in the
literature (Jerison 1979; Pilbeam and Gould 1974) and, therefore, the least likely to
exaggerate differences. This ultimately made it easier to assess whether genuine
differences existed between the sexes.
This second factor was not essential to the
study, as statistical analyses made clear where legitimate differences were to be
found, but starting with a more conservative figure made it easier to see where the
largest disparities existed during the initial evaluation of the data.
After all of the necessary figures that could be estimated were obtained, data for the
213 animals with complete information were sorted into the various categories
briefly described above and in more detail below. The data was then statistically
analyzed, and then re-examined once phylogeny had been controlled for.
3.3.1: Data Analysis
3.3.1.1: Family
Once values for brain mass and EQ were obtained the data points were sorted and
separated according to taxonomic family. The divisions were made according to the
taxonomic classes on the 10kTrees website (Arnold et. al. 2010). This was done in
order to prepare the data for eventual phylogenetic analysis. The result of sorting the
species in this way was the creation of eleven separate groups.
These groups
included the following families: lemuriformes, loridae, galgonidae, tarsidae,
pitheciidae, cebidae, atelidae, cercopithecini, papionini, colobinae, and hominoidea.
The New World monkeys were not sorted into the five categories typical usually
employed in classification were collapsed into four, with the callitrichidae being
included in the cebidae group on the basis of phylogeny.
Once all of the animals were sorted according to family, the encephalization
quotients obtained using the mean brain volume values of males and females were
compared. The data was analyzed for statistically significant differences using a
one-tailed Pearson’s t-test in Excel. A pair-wise comparison of EQ values for males
20
and females was done for each family. P-values of less than 0.05 were considered
statistically significant.
Because all of the animals in each family share in common a particular genetic
heritage, and therefore do not represent independent data points, it was necessary to
reanalyze the data, taking phylogeny into consideration. Doing this made it possible
to establish whether the differences observed in the initial analyses were the result of
a trend consistent with a primitive trait or had been selected for (Felsenstein 1985).
Therefore, after the initial set of analyses, in which the animals were sorted into
families and the EQ values obtained using the slope recommended by Williams
(2001) were used to t-test each family for statistically significant differences, an
additional set of analyses was done in which the difference were reassessed with
phylogeny controlled for. To control for phylogeny, values from tree files generated
by 10kTrees.com, utilizing information provided by GenBank, were generated.
Those trees were then input into the R statistics program along with the mean values
for brain and body mass for each species and a PGLS (Phylogenetic generalized least
squares) analysis was done. Residuals from that analysis were then compared to
evaluate whether the original differences remained once phylogeny had been
controlled for.
3.3.1.2: Body Size
Once all of the data had been analyzed by sex according to family, it was then
evaluated in terms of the overall size of the animals. As discussed in the previous
section, a correlation between body size and degree of dimorphism has been
suggested (Plavcan 2001). Larger animals do appear to exhibit greater dimorphism
than smaller ones. To test this theory the animals in this data set were divided up
according size, independently of family, and then pair-wise comparisons were done
in the same manner as had been done in the initial comparisons done according to
taxonomic grouping.
The data on body size was included in the original data set as specified above, so it
was simply broken up into smaller sets according to size, from smallest to largest,
21
based on what appeared to be natural divisions in the data. Initially, the animals were
sorted into a half dozen groups. The divisions were (1) >500g, (2) 501 – 1,000g, (3)
1,001 – 2,500g, (4) 2,501 – 5,000g, (5) 5,001 – 10,000g, and (6) <10,000g. Almost
half of the entire set of data points ended up falling into the fifth category, so this
group was further divided into two in order to get a clearer picture of where
differences might lie should they exist. With this last division, there were a total of
seven size classes that were tested. These included five of the original six (1,2,3,4,
and 6) plus additional categories for animals weighing between 5,001 – 7,500g and
7,501 – 10,000g.
As with the analyses done according to family and phylogeny, the mean EQ values
of each sex were compared using Pearson’s one tail t-test. Values of less than .05
were considered significant.
3.3.1.3: Diet
Theories regarding the influence of dietary composition have been a major
component of both anthropological and archaeological studies for several decades.
The degree to which diet has been a significant factor in shaping the neurological
development of other primates is therefore an important line of enquiry to consider
when looking at dimorphism reflected in brain size. Recognizing this, it was decided
that the data should be analyzed along these lines. The data set was resorted once
again, this time in terms of dietary composition of the animals.
For this set of analyses the data was sorted into one of eight categories according to
primary food source or sources. The groups included fruit, leaves, fruit plus, gum,
insects, leaves, leaves and fruit, seeds, and omnivorous.
The fruit plus group
includes animals that get nearly equal parts of their nutrition from fruit and insects or
fruit and gum. Animals in the leaves and fruit category have diets made that are
equally frugivorous and folivorous. For all other animals, the group they’ve been
assigned to makes up the majority of their diets. The omnivorous group includes
animals whose diets are too varied to make any one other group designation
appropriate.
22
Information on the dietary habits for each animal was researched and crossreferenced using several databases. The Primate Info Net Library and Research
database at the University of Wisconsin (http://pin.primate.wisc.edu/) was the initial
source consulted for diet information. Specific information was obtained from the
individual fact sheets for each of the animals available on this website. In cases
where information was missing, unclear, or there was no fact sheet available for a
particular animal other databases were accessed.
These included the Animal
Diversity Web maintained by the University of Michigan Museum of Zoology
(http://animaldiversity.ummz.umich.edu/site/index.html), and the IUCN Red List of
Endangered Species (http://www.iucnredlist.org/).
Information on these websites
has been obtained from published research in a variety of reputable journals and
compiled by experts in the field of primatology. The Animal Diversity Web page
was the primary source of information for the dietary habits of the animals analyzed
in this study.
Mean EQ values of males and females were compared in the same manner as they
had been when analyzing animals according to family and body size. P-values of
less than .05 were considered significant.
3.3.1.4: Reproductive Strategy
Because traits such as size and dietary preference have a strong influence on
behaviour, and the connection between these three elements is not strictly
unidirectional, one last set of analyses involving social behaviour was done. For this
set of tests, animals were sorted into categories based on reproductive strategy. The
categories broke down as follows: polygynous, polyandrous, monogamous,
polygynandrous, varied, and unknown.
With the exception of “varied” and
“unknown”, all categories represent the species’ dominant mating strategy. The
assigned category may not be the only tactic employed by the animals in question,
nor is there absolute consensus in many cases that the animals do behave in a manner
consistent with the category to which they’ve been assigned.
23
In cases where there were differences of opinion regarding the species’ typical
behaviour, additional resources were consulted and the strategy that appeared most
often in the literature was chosen. In cases where the research had not been done or
the information was not available in any of the databases consulted, the species was
assigned to the unknown category.
Where there was no clearly dominant
reproductive strategy employed, the species was assigned to the varied category.
The information on reproductive strategy was obtained from the same databases
utilized to obtain information on dietary composition. Once again, these included the
University of Michigan Museum of Zoology’s Animal Diversity Web database, the
University of Wisconsin’s Primate Info Net, and the IUCN Red list database.
Once the statistical analyses were complete the results were compiled and put into
table form. Those tables and a brief explication of what the results indicate are
contained in the following section. A brief discussion of some of the key points, and
potential areas where further investidation may be necessary to get a clearer picture
of things, is also included.
24
CHAPTER 4
RESULTS
4.1: Introduction
In the following sections results of pair-wise comparisons of male and female EQ
values, according to the dimensions discussed in the previous section, are laid out in
table form and briefly explored. Scatter plots showing the residual values for the
models generated by the PGLS analysis are also included along with a phylogram
that schematically represents the genetic relationship of the animals included in that
analysis. Possible shortcomings of the analyses and an overview of the potential
implications are presented at the end of this chapter. A more in depth discussion of
both of these issues has been reserved for the following chapter.
4.2: Results of Pair-wise Comparisons of Male and Female EQ
4.2.1: Family
Table 1. Pair-wise comparison of male and female primate brain mass, body mass, and EQ
according to family.
Mean
Mean
Mean
Mean
Male Female
Brain
Male Female
Body Mean Mean
Brain
Brain
Mass
Body
Body
Mass
Male Femal
EQ
Family
Mass
Mass P-value
Mass
Mass P-value
EQ
e EQ P-value
18.82
18.63
0.2889
1758
1825
0.0661
2.26
2.24
0.2710
Lemuriformes
10.97
10.16
0.0054
634
607
0.1596
1.82
1.71
0.0042*
Loridae
7.36
6.91
0.0224
456
432
0.0103
1.34
1.29
0.0753
Galagonidae
3.70
3.49
0.0666
456
116
0.0103
0.95
0.92
0.1035
Tarsidae
20.22
19.81
0.1074
1078
1003
0.1795
2.86
2.87
0.4788
Pitheciidae
31.74
30.40
0.0011
1364
1079
0.0001
3.93
4.03 0.0007*
Cebidae
87.68
84.36
0.0177
8012
6722
0.0011
7.07
7.08
0.4717
Atelidae
73.81
64.52
0.0000
5874
3716
0.0000
6.53
6.48
0.1524
Cercopithec.
111.70
101.07
0.0000 12452
7377
0.0000
8.08
8.35 0.0248*
Papionini
76.35
69.22
0.0000
8150
6944
0.0003
6.18
5.82 0.0000*
Colobinae
269.48
237.99
0.0002 45884
27651
0.0020
13.77
13.60
0.2681
Hominoidea
*P-values of less than 0.05 were considered statistically significant. P-values obtained using a one-tailed t-test.
25
The first set of analyses involved the comparison of EQ values for male and female
primates from eleven different families. For seven of the eleven, there were no
significant differences observed between male and female animals with regard to
divergence from the expected degree of encephalization, as indicated by the p-values
that were generated by a one-tailed t-test comparing mean EQ values. There were,
however, significant differences in the remaining four families.
In the loridae and colobinae families males proved to have consistently higher EQ
values than females when analyzed this way. The p-values for these two groups
were ~0.0042 and ~0.000, respectively. In the case of the latter, the actual p-value
(~0.000000008) was so small that it shows as zero when rounded to the fourth
decimal place, as indicated in the table above.
Comparisons of the cebidae and papionini families also demonstrated a significant
difference in the EQ values of male and female animals in these species. In these
cases the females proved to be the more encephalized animals, with respective Pvalues of 0.0007 and 0.0248.
Because the animals sorted according to family
represent closely related genetic clusters of animals, values for all males and females
for whom phylogenetic information was available were statistically re-evaluated with
phylogeny controlled for. The tree (Fig. 1) immediately below is a phylogram that
was generated using the FigTree software in conjunction with the tree data provided
by 10kTrees.com. It provides a schematic representation of the relationship of the
139 animal species that information was available for. This information was used in
conjunction with the R statistics program to analyse the effect of phylogeny on shifts
in encephalization.
Using the PGLS command in R, plotting brain mass over body mass, the y-intercept
of the model generated for males was 35.45 with an SE of 22.53 and a p-value of
0.1178. The body mass coefficient, or slope, was 0.0019 with an SE of 0.00017 and
a p-value of less than 2-16. The y-intercept for the female model was 30.84 with an
SE of 17.86 and a p-value of 0.0864. The slope for the female model was 0.0032
with an SE of 0.00022 with the same p-value of the male model, less than 2-16.
26
The results of those analyses indicate that phylogeny has played a role in
perpetuating difference where in many cases where it exists. It is not clear, however,
that phylogeny is the only factor influencing the differences in relative brain size
seen between males and females across the entire primate order. In at least a few
species, the divergence from the expected values is greater than phylogeny alone
should allow for (see Fig. 2 and Fig. 3). These elevated values may be indicative of
a grade shift occurring in certain clades or families, such as that seen in the results
for the Great Apes in the hominoidea family.
27
Figure 1. Phylogram representing the genetic relationship of 139 primate
species.
28
Figure 2. Scatterplot of residuals comparing male and female encephalization, controlled for phylogeny.
Residuals - Encephalization and sex - Controlled for Phylogeny
350
Residuals for each species
300
250
200
Female residuals
150
Male residuals
100
Linear (Female
residuals)
50
Linear (Male residuals)
0
0
20
40
60
80
100
120
140
160
-50
-100
Model generated slope - based on phylogenetically generalized least squares (PGLS)
29
Figure 3. Male and Female Residuals by Sex and Family
350
Male Cercopithecines
300
Female Cercopithecines
Male Lemuriformes
250
Female Lemuriformes
Male Atelidae
200
Female Atelidae
Male Cebidae
Female Cebidae
150
Male Loridae
Female Loridae
100
Male Hominoidea
Female Hominoidea
50
Male Pitheciidea
Female Pitheciidea
0
0
-50
5
10
15
20
25
Male Papionini
Female Papionini
Male Colobinae
Female Colobinae
-100
Male Galagonidae & Tarsiidae
Residuals generated by PGLS. Zero indicates no divergence from model predictioed values. Postive values indicate larger than
expected relative brain size. Negative values indicate smaller than expected relative brain size.
30
4.2.2 Body Size
Table 2. Pair-wise comparison of male and female EQ according to body size
Mean
Mean
Male
Female
Mean
Mean
Body Size
P-value
Body
Body
Male EQ Female EQ
Mass
Mass
264
261
1.32
1.34
0.1698
0-500g
758
690
2.56
2.55
0.3854
501-1000g
1839
1697
3.60
3.59
0.4346
1001-2500g
4323
3180
6.46
6.45
0.3852
2501-5000g
6700
5709
6.79
6.56
0.0002*
5001-7500g
9760
7408
7.16
7.15
0.4205
7501-10000g
50630
28999
13.37
13.48
0.3602
>10000g
*P-values of less than 0.05 were considered statistically significant. P-values were obtained
using a one-tailed t-test.
Consistent with Plavcan’s (2001) suggestion, overall dimorphism does increase with
a general increase size. Neurological dimorphism as a stand-alone trait, on the other
hand, does not appear to.
When animals were divided according to size, only one
category showed a significant difference in EQ values when male and female mean
values were compared.
Only in the 5001 to 7500g body weight class was a
statistically significant difference observed, with a p-value of 0.0002. Here, males
proved to be the more encephalized sex.
4.2.3 Dietary Composition
Table 3. Pair-wise comparison of male and female EQ according to dietary
composition
Diet
Fruit
Fruit plus
Gum
Insects
Leaves
Leaves & Fruit
Omnivorous
Seeds
Mean EQ Males Mean EQ Females
7.38
2.11
1.34
1.10
5.34
6.12
5.98
6.26
7.41
2.12
1.34
1.08
5.36
5.98
6.02
6.43
P-value
0.3681
0.4093
0.4849
0.3021
0.4487
0.1432
0.3035
0.1541
31
An analysis of encephalization against diet yielded results indicating no correlation
between primary diet type and the degree of encephalization in the species analyzed.
In no case were the p-values generated by one-tailed t-tests indicative of a correlation
between brain size and primary food choice. The lowest p-values were found among
species whose primary diet consists of equal parts leaves and fruit (0.1432), and
those for whom the bulk of the diet is comprised of seeds (0.1541). In neither case
are the values strongly indicative of a correlation between food choice and EQ,
however.
4.2.4 Reproductive Strategy
Table 4. P-values for pair-wise comparison of male and female EQ according to
reproductive strategy
Reproductive Strategy
Polygynous
Polyandrous
Monogamous
Polygynandrous
Varied
Unknown
Mean EQ Males
Mean EQ
Females
P-value
5.62
3.32
4.28
8.29
2.86
4.12
5.60
3.39
4.24
8.35
2.85
4.13
0.3571
0.0902
0.1385
0.2477
0.4105
0.4304
As with diet, the p-values generated by t-tests analyzing whether there might be a
correlation between reproductive strategy and EQ, yielded nothing of any obvious
significance. Here, however, one group did have a markedly lower p-value than the
others. Species assigned to the polyandrous category appear to have a much higher
proportion of females with higher EQs than males, though the p-value (0.0902) is not
quite as low as is typically used to say anything definitive.
The p-value for
monogamous species was likewise worthy of further consideration at 0.1385, with
males exhibiting greater encephalization in that case.
32
4.3: Discussion of results
Before providing a more thorough treatment of the results in the next section, there
are a couple of matters that warrant mentioning with regard to the data. The first
thing that ought be borne in mind with regard to the results for the pair-wise
comparisons in which diet and reproductive strategies were the dimensions along
which relative brain size was assessed is the lack of clear, accurate information
available for many of the species included in this data set. Many of the animals have
only been studied in laboratories and zoos, where handlers proscribe diets, and
reproductive strategies may depart radically from what is typical in the wild.
Additionally, even in cases where the animals were studied in their native habitats,
the amount of information obtained regarding these behaviours is often quite limited
and does not always reflect the animal’s usual diet preferences or give the
researchers a clear picture of precisely what sort of reproductive strategy is common
to the species under observation.
A second issue that bears consideration is the role of phylogeny. The results here tell
us that once we take taxon-level influences are taken into consideration the picture
that emerges is somewhat different, with females falling below males in the degree to
which they’ve become encephalized. This may appear to conflict with the result of
the initial pair-wise comparisons. It does not. What these results may indicate is that
in species where one sex is more encephalized, the trend is the result of canalization
rather than selection pressures. The trend toward encephalization may have occurred
at some earlier evolutionary break. It does not mean that not that the animals in
question do have larger relative brains sizes.
33
CHAPTER 5
DISCUSSION
5.1: Introduction
In this section, some of the potential implications of the results described above will
be explored, and a more thorough treatment of some of the more interesting findings
will be provided. In addition to the models described in the literature review section
of this paper, the results will also be examined in light and the models articulated by
Wrangham (1986) and van Schaik (1989). The following sections are divided
according to the individual variables analyzed. An additional section discussing the
influence of the different variables on one another is also included toward the end of
this chapter. The final paragraphs of this section examine the way the results of this
study support, or refute, three of the major hypotheses explaining how
encephalization in primates has occurred. These are the Social Brain hypothesis
(Dunbar 1998), the maternal energy hypothesis (Martin 1996), and a third hypothesis
that explains differences in encephalization as having resulted from differences in
basal metabolic rates (McNab 1986a, McNab 1986b, Martin 1996).
5.2: Discussion
5.2.1 Results by Family
With regard to the first and most general inquiry of this study, the question of
whether one sex or the other has evolved greater relative brain size, the results were
quite mixed. When pair-wise comparisons of the mean values for males and females
of individual species were done using the raw data and the EQ slope recommended
by Williams (2001), the results indicated that in one of the New World monkey
families, the atelidae, females had a higher EQ values. The pair-wise comparisons
also indicate that, when looking at the entire family, EQ values for female papionini
were significantly higher than those for males of that family. In direct contrast to
34
this, prosimian males of the loridae family possess larger relative brain sizes and so
do Old World monkey males in the colobinae family.
Once phylogeny was controlled for and the species were reanalysed, a different
picture emerged. The number of species included in the second set of analyses was
far smaller at 139 than the original group of 212, but still large enough to get a
reasonably clear picture of what may be happening across the order. The scatterplot
of the residuals included above (Fig. 2) shows that the values for males appear to
diverge more radically from the mean predicted values than those of the females. In
almost every species, males show a wider range of values than females once
phylogeny is controlled for. In species that fall above the slope, and are more
encephalized than would be predicted, the males are nearly always more
encephalized than them females. When the values fall below the mean, females are
more encephalized and the negative values for males of the same species are larger.
In all cases, female residual values tend to align much more closely with what would
be expected for the species in question, based on its genetic distance from other
species in the order.
The values for individual species also tend to cluster very tightly according to family
regard less of sex. Very few species exhibit values that sit a significant distance
away from those of their closest relatives. When one species in a family sits close to
the line so do the majority of the other species in that family. When there is greater
divergence than expected for an individual species, closely related species of the
same family tend to show the same trend. For example, the cebidae values all appear
to cluster fairly tightly around the slope, regardless of the size of the individual
species, while all the papionini tend to sit well above it. The clear exception is found
in the hominoidea. In the hominoids, the great apes (Pan, Gorilla, and Pongo) show
a massive departure from the expect values, with values falling well above what
would be seen within one standard deviation, while the values for the gibbons
(Hylobates) sit almost immediately on the line, falling precisely where they are
predicted to.
35
Looking at the aims of this study, the differences in the values before and after
phylogeny was controlled for seem to indicate that there may be different pressures
operating on each sex in a number of species. The EQ values for females, once
phylogeny is controlled for, cluster very tightly around the predicted mean values,
indicating that, whatever the trend within any given species with regard to
encephalization, the trait is less plastic in females. More importantly, in families
where females are more encephalized, this trait doesn’t appear to have been selected
for during the period in which the primate order has evolved. In other words, greater
encephalization in females appears to be a canalized trait, which evolved prior to the
evolutionary break where the primate order began, in the families where it is present.
Individual species may exhibit a departure from this trend, but in nearly all cases
where this is so, it is because the species as a whole has rather than just females.
Even when females are more encephalized than would be expected (as in the case of
the Great Apes), males are as well, indicating that the trait is probably evolving as a
result of more general natural selection pressures acting on the entire species, rather
than on females, or that females have become more encephalized because males have
(Clutton-Brock et. al. 1977; Leutenegger and Cheverud 1982; Kappeler 1999).
Male values, by contrast, do not exhibit any clear or obvious trend with regard to the
degree of encephalization seen from one family to the next. In certain species there
is a great deal of divergence, while in others the residual values are quite consistent
with what would be expected. Looking at the second scatter plot (Fig. 3), however, it
does appear that there are a number of tightly associated clusters of values in closely
related species, many of which share similarly complex social structures with fairly
heavy burdens on males in terms of sexual competition.
Several species in the hominoidea, papionini, and atelidae families which are known
to have complex social structures (Smuts 1985; Mittermeier and van Roosmalen
1981; van Roosmalen 1985), as well as high levels of sexual competition among
males, also show high levels of encephalization among males, with residuals falling
well above the predicted values. In species where competition is lower among males
and social structures are more fluid, such as the callitrichidae (Porter and Christen
36
2002), the male EQ values are much lower with many species falling well below
what would be expected based on the slope generated by the phylogenetic general
least squares analysis. These results are consistent with findings of Schillaci (2006,
p. e62) in which “an analysis of variance (ANOVA) derived from multiple regression
models with mass dimorphism and male body mass as independent variables, and
brain size and testis size as dependent variables, indicated that the level of male
competition for mates had a significant association with brain size but not with testis
size.” They also lend support to the social brain hypothesis (Dunbar 1998), which is
discussed further in the section dealing with reproductive strategy below.
5.2.2 Results and Body Size
When tested using a Pearson’s correlation one-tailed t-test, body size and EQ showed
no evidence of being linked in any size class but one. Males and females of species
in the 5001-7500g bodyweight classes do appear to manifest EQ values that differ
significantly. In this group, the average EQ for males was 6.79 and 6.56 for females,
with a p-value of 0.0002. Interestingly, there are a very high number of smaller
hominoidea in this size class (see original Isler et. al. 2008 data set for individual
species mean values, at doi:10.1016/j.jhevol.2008.08.004.) .
Compared with the group of animals in which phylogeny was controlled for, the
results of the analyses in the initial comparison done using only values provided by
the raw data and Williams’ recommended slope seem far less interesting or
indicative of anything. Once phylogeny is controlled for, the results indicate that
body size does in fact correlate with the degree to which a species diverges from the
expected level of encephalization. The largest animals exhibit the highest levels of
encephalization and the values are well above what is predicted by the model for
animals with their respective mean body mass values. In other words, the big
animals possess brains even bigger than what would be expected for a big animal.
Brain volume has not evolved in an isometric fashion in the larger primates. The
presence of the hominoidea as extreme outliers, well outside the first SD, on the
scatter plot above offer the clearest evidence of this trend. It tells us that the ratio of
brain mass to body mass in the hominoidea is far higher than would be seen if these
37
structures had evolved in an isometric fashion. Of additional interest is the fact that
once again we see evidence of higher levels of divergence from expected values for
males than we do for females. Once again, female values are clustered much more
tightly around the slope for their sex than males are for theirs. When the EQ values
for an entire species are higher than expected, male values are almost always higher
than those of females, and the largest gaps are seen among the largest animals,
indicating that there is in fact a relationship between overall body size and EQ.
The results of the analyses involving body size comport quite nicely with Plavcan’s
(2001) assertions regarding this matter, as discussed in the literature review section
of this paper. Dimorphism in body size does indeed seem to lead to greater
dimorphism overall. Particular structures, in this case brain, do increase in size in an
exponential, rather than linear, fashion and the amount that a structure may change as
the species in question becomes larger may differ between the sexes.
The
mechanism or mechanisms that may account for the difference are not obvious when
simply looking at the differences themselves but it seems reasonable to assume that
reproductive demands and resource availability may play a role and, therefore, this
issue will be revisited in the discussion of the results of both the analyses involving
diet and reproductive strategy.
5.2.3 Results and Diet
Among the least interesting results of this study were those generated by the pairwise comparisons of the raw data for males and females looking at a possible
correlation between sex, EQ, and primary food source. The problem with this set of
analyses was not, however, the lack of potentially interesting things that might be
said about the relationship between EQ, diet and sex, but the difficulty of obtaining
clear, accurate information about actual diet preferences from species to species.
With several of the species in this study, the necessary information was not available,
extremely limited, or the reports from one study to the next on the same species were
conflicting. As such, a “best guess”, which involved choosing the position with the
greatest consensus in the available literature, was often the category to which a
species was ultimately assigned. These “best guesses” resulted in the creation of
38
categories that are, admittedly, too broad to be particularly useful in careful analysis
of the relationship between diet and brain development. They also may be incorrect.
Nevertheless, the influence of nutrition and resource availability are matters
important enough to warrant some discussion, and therefore the balance of this
section will be devoted an exploration of these issues in light of the other variables
analyzed.
Assuming Amen-Ra’s (2007) neurotrophic neotonization theory is correct, it is likely
that this particular dimension, diet, has been pivotal in shaping neurologically
dimorphic traits. Looking at the results above, however, it does not appear that
composition plays as big a role as fluctuations in the availability of food do. The
results of the analyses looking at composition don’t tell us nearly as much as what
the scatterplots (Fig. 2 and Fig. 3) of the residual values of the models for male and
female EQ do. Looking at the scatter plot we can see that the species with the
greatest levels of positive divergence are found in the Old World monkeys
(papionini) and the Great Apes (hominoidea).
We know from research done
involving our own evolution (Amen-Ra 2006) that resource availability on the
African continent, where these species have evolved, has greatly fluctuated over the
past several million years with famine conditions arising several times. On the other
hand, the species that have evolved under less precarious conditions show much
lower levels of encephalization with female EQ values sometimes surpassing those
found in males and several species falling well below the slope generated by the
models for both sexes. The diets of the animals on both continents vary greatly, but
consistent availability of food has been much more erratic for the Old World species
(Amen-Ra 2007) than it has been for New World monkeys.
As noted in both of the earlier discussions of family and body size, EQ values for
female primates tend to align much more closely with what the models based on
phylogeny predict than those of males, indicating that selection pressures may be
different for males and females. One way of interpreting that difference is in terms
of the consequences that resource distribution has on each sex. Females, as stated in
the introduction have more at stake when resource availability is compromised. A
39
female mammal must be able to meet her own nutritional demands as well as those
of her offspring. The female animal, simply by virtue of these demands, has fewer
resources available for use in the development of her own body. Males, in nearly all
primate species, have far more leeway in terms of the extent to which they can
diverge from the expected mean body or brain size and still survive because the cost
in the development of these traits is always, relatively, lower. A female whose size
exceeds what the resources in the environment can support will not only starve
herself, but her offspring as well. A male faced with the same conditions will still be
able to successfully reproduce, often many times over, before he starves to death.
The potential for female body and brain growth is much more narrowly restricted by
resource availability than it is for males.
Hypotheses offered by van Schaik (1989) and Wrangham (1986) explain the
dispersion of females in any given environment as mapping on to the resources, or
food, available in that environment. The differences in the residual values seen
above are consistent with these hypotheses, offering further support to the suggestion
that females are more vulnerable to the effects of fluctuations in resource availability
than to fluctuations in the availability of mating partners.
We would expect a
narrower range of values for both brain and body size in females, with females being
both smaller and, by extension, less encephalized than males in regions where
resource availability is more limited. The results of this study are consistent with this
position.
The fact that males are not only absolutely more encephalized, but relatively as well,
is slightly more puzzling. It seems that if famine conditions are what drive increasing
encephalization, then the sex more susceptible to the effects of famine would end up
developing a relatively larger brain. We can see from the residuals that this has not
been the case. Females are nearly always less relatively encephalized when species
values fall above what is predicted by the model. Only in species that fall below or
immediately along the model’s predicted values do females end up being more
encephalized than males and, here again, this seems to have more to do with female
values being more closely aligned with the predictions, rather than females actually
40
having evolved a larger brain. Here then it seems we may have a result that goes
against what we would expect according to the N3 hypothesis. On the other hand, if
there is an added selection pressure driving male encephalization that females do not
have to contend with, the neurotrophic neotonization theory may still give us an
accurate account of how certain primates, throughout the entire order, have evolved
such extreme relative brain sizes.
This possibility will be discussed further in the
following section.
5.2.4 Results by Reproductive Strategy
A review of the results of the pair-wise analyses examining the relationship between
reproductive strategy, EQ, and sex indicates that the greater relative encephalization
seen in so many of the Old World primate species, and males in particular, may be
the result of sexual selection among males. Famine conditions may have set the
trend in motion, but it appears that sexual selection has taken over from there. Males
in all the hominoid species as well as a number of those in the Old World monkey
families are more encephalized than the females. In nearly all of the species in
question high levels of competition exist among males.
The EQ values for Old World primates contrast quite starkly with what we see in the
New World monkeys. While there certainly are a number of New World species that
do sit above the slope generated by the model, many more fall below, with males
generally falling below females when they do. The pair-wise comparisons of males
and females according to reproductive strategy are in line with what the scatterplots
(Fig. 2 and Fig. 3) illustrate. The most statistically significant difference seen
between males and females, when sorted according to reproductive strategy, was in
group containing polyandrous species (the cebidae) where the results indicated that
females were relatively more encephalized. Though the p-value wasn’t quite low
enough to say anything definitive, at 0.0902 it is unlikely that the difference in this
group was solely due to chance. Females in polyandrous species are often relatively
more encephalized than their male counterparts. The burden on males in these
species, in terms of intraspecies competition, is also known to be quite low.
41
It appears then that the level of intraspecies competition, or sexual selection, largely
influences the extent to which males become more encephalized. In females,
encephalization is primarily determined by interspecies competition, or natural
selection more broadly.
Any given species will evolve according to what
environmental constraints exist within its respective niche, but within primates, it is
in the sex that is less susceptible to fluctuations in resource availability that we see
more variability in the degree to which it becomes encephalized (Barton 1999;
Barton 2006). In this case, it is the males. Once again, looking at the scatterplots
(Fig. 2 and Fig. 3), this trend is quite apparent in both directions.
Males in the polyandrous and many polygynandrous species, where male-male
competition is either extremely low or non-existent, have the lowest EQ values of all
the species analyzed. Social structures among species engaging in these types of
reproductive strategies put far less of a burden on males than those in which mate
securing is an issue. That Schillaci (2006) found a high degree of encephalization in
monogamous species unexpected and somewhat puzzling, but his findings are not
inconsistent with the results of this study. Even in monogamous species the social
demands on males are generally greater than they are for their female counterparts,
as males are generally the chosen, rather than the choosing, sex. If Dunbar’s (1998)
social brain hypothesis is correct we should expect monogamous males, as well as
polygynous, to have higher EQ values than males of species with more flexible
reproductive strategies, as males in species with both of these reproductive strategies
face a far heavier burden in securing a mate, or mates, than their polyandrous or
polygynandrous cousins. The burden for males in monogamous species is certainly
less than that of polygynous, but the business of procuring a partner is, nevertheless,
far more taxing for males than it is for females in species where females are less
particular about their mate choices.
Whether there exists a genuine correlation between reproductive strategy and the
degree to which a species is encephalized is something that has not been made
entirely clear with this study, but it does appear that these two traits are in some way
linked. The relationship between them may be only correlative, rather than causal,
42
with some an additional element linking the two. One reasonable candidate is, as
mentioned previously, a certain kind of precariousness in the environmental
conditions.
Based on the research on encephalization discussed above, it would appear that
certain environmental conditions would need to be present in order for the trend
toward greater encephalization to even begin. A shortfall in available resources
initiates the biochemical processes that lead to greater encephalization (Wang et. al.
2006). Those animals that do not possess the physiological means to endure famine
conditions end up dying, leaving behind a generation of more encephalized, or at
least more encephalizable, animals.
Whatever genetic component it is that has
allowed the survivors to survive is then passed on to the next generation and the
process of species-wide encephalization is set in motion. If this trait confers some
benefit on that species in question it will persist or evolve further over time as a
result of natural selection. Once a trait appears in a population, the original selection
pressures that originally drove its development need not be the ones that perpetuate
further development of that trait. In this case, it appears that environmental
fluctuations manifesting as repeated bouts of famine over several million years,
triggered the process of encephalization in primates. Once the order was on that
trajectory, complex social systems became possible and this trait was further
influenced by sexual selection. Both the negative and the positive results in this study
support this position.
5.2.5 Synthesis
Because several variables were explored in this study, this section of the discussion
will be devoted to pulling them all together in order to look at how the interplay of
each of these elements may have affected the results.
A clearly articulated
conclusion has been reserved for the sixth and final chapter.
Arguably, the most tightly connected variables in this study are those of diet and
reproductive strategy. Both van Schaik (1989) and Wrangham (1986) have explored
the connection between these two variables and the general consensus is that diet
43
plays a key role in determining reproductive strategy, which in turn shapes social
structure. Here, again, it is argued that the most influential aspect of diet is the way
the food is distributed in the environment, rather than nutrient content. Actual
dietary composition is not wholly irrelevant though, despite what the results of this
study appear to indicate, as the food type and food distribution patterns go hand in
hand. Fruit, for example, is a seasonal, geographically limited resource that may
monopolized be far more easily by a single dominant female than say something like
leaves or insects. Fruit is also a great deal more difficult to procure on a regular
basis. This means that frugivorous species are more susceptible to environmental
fluctuations and are also more geographically limited as a result of their diet.
Assuming the models offered up by Wrangham and van Schaik are correct and males
do map onto females and females map on to food sources, the opportunity for males
to monopolize females is more likely to arise in species that are predominantly
frugivorous. Once it becomes possible for males to monopolize females, high levels
of competition between males will arise, and social behaviours will become
increasingly more complex. Considering this line of thought with regard to this
particular study, we see that a number of the more encephalized animals are known
to be both polygynous and frugivorous (such as the large hominoidea, and a number
of species in the atelidae and papionini families) at while the group of animals with
the lowest EQs includes the polyandrous omnivores (found among the cebidae).
The pair-wise comparisons analyzing the data in terms of dietary composition do not
provide this information, but a careful examination of the original data in conjunction
with the scatterplot of residuals does.
Looking at diet in conjunction with
reproductive strategy gives us far more insight into the relationship between EQ and
sex, than analyses of either variable on its own can.
Two other variables that appear to be strongly connected are those of body size and
reproductive strategy. The largest males in this study turned out to be the animals
with the highest EQs. High levels of relative encephalization were also associated
with high levels of body dimorphism, though the most dimorphic species were not
those with the highest EQs. We have already seen how dimorphism can arise
44
without sexual selection (Clutton-Brock et. al. 1977), simply as a result of downward
pressure on one sex, but the extreme dimorphism seen in the animals with the largest
gaps in size between males and females appears to be tied to sexual selection. In both
the papionini and hominoidea, families in which the highest levels of body
dimorphism are found, a large number of the species are polygynous and males are
far more encephalized than females. These are also the largest primates in the order,
of both sexes, and there are no known polyandrous species in either family. Even
Pan paniscus, with its apparently matriarchal social structure, does not employ a
polyandrous reproductive strategy (White 1988; White 1996).
The dominant strategies among the large-bodied primates analyzed in this study are
polygyny and polygynandry, with half of the great ape species employing the former
strategy and half employing the latter.
Though polygynandry is a common
reproductive strategy in the smaller monkeys in both New and Old world species, the
strategy employed among the Great Apes is not the sort of free for all mating that is
found in the smaller monkeys, but a far more competitive an combative affair
wherein males are competing against one another almost as fiercely as they are in
polygynous populations (Smuts 1985: Nishida et al. 2003; White 1988; White 1996).
There are numerous species outside of the papionini and hominoidea that may also
be characterized as polygynous or complexly polygynandrous, but there are no truly
large-bodied polyandrous species. Additionally, even in the smaller polygynous
animals, males are far larger and more encephalized.
Body size, reproductive
strategy, and encephalization appear to be closely linked, if not co-evolving in the
strictest sense.
The sections immediately above have discussed the relationship between pairs of
variables that appear to be especially strongly linked, but these dyads far from
exhaust the list of ways that each dimension may influence, or be influenced by, the
others. Body size, diet, and reproductive strategy all shape one another, and this in
turns influences the way a species, and even a family, evolves over time. A large
number of the smallest of the animals in this study have evolved in geographic
regions where the resources are more abundant, or were in the past, on the South
45
American continent. In these species, female encephalization quotients are nearly
identical to those seen in males, with a few actually being higher (again, however,
this is only because the entire species falls below the predicted values). These are
also the only known truly polyandrous species.
This may seem somewhat
counterintuitive as it would seem that more resources would result in larger animals,
but a review of the basic tenets of natural selection reveals why larger, more
encephalized animals would evolve in regions where resources are less readily
available.
First, there is the most fundamental kind of natural selection pressure, that of
interspecies competition. As long as there are adequate resources, the larger animals
may dominate. Even when resources are diminished, if there is enough food
available to circumvent the problem of total starvation, smaller and weaker animals
will lose out in the fight for survival. It should be noted here that being weaker isn’t
necessarily a matter of being less physically strong or robust, it may also be that one
species lacks the cognitive capacity to deal with shifts in the environment with the
same facility that its neighbours do. In environments, such as those where we find
the small, polyandrous monkeys, this kind of pressure is greatly relaxed. Food is
relatively plentiful and, though seasonal in many cases, consistent in its availability.
If enough food is available for everyone, competition is low. No one species gains
an advantage by being significantly larger, stronger, or “smarter” in environments
where resources are adequate to support the entire population.
Second, in resource deprived environments there is also the added burden of
intraspecies competition creating an additional selection pressure. Intraspecies, or
sexual, selection is markedly more pronounced in populations where food
availability has fluctuated greatly over the period in which the species has evolved.
Animals in these species are competing with other species for environmental
resources as well as with other members of their own species for mating
opportunities. The primary selection pressure, environmental conditions, determines
the developmental trajectory for the entire species and the secondary pressure of
46
competition for mating opportunities results in the development of highly dimorphic
traits within the species.
Animals of both sexes need some sort of advantage to outcompete other animals in
the environment, but the sex with the added burden of being the “chosen” one (rather
than the more passive chooser) has to have an added edge relative to other members
of his species. Looking at these considerations, we can now see how and why
residuals values for male Hominoidea are so far above those for all of the other
animals in this study. Diet, or more precisely, a lack of continuity in resource
availability, seems to have driven the increase in overall species size. Those animals
that were the largest and best able to navigate their environments were then able to
outcompete other members of their own species in securing reproductive
opportunities.
Recognizing this, we can see that all four of the variables examined in this study
have played a role in the development of these large-bodied, highly encephalized
species. The same can be said of all the other animals studied. The degree to which
any one dimension affects or is affected by the others may vary from species to
species, but in every case every variable plays a role with regard to all of the others.
It is never the case that any one dimension is the definitive variable when it comes to
determining the extent to which a species becomes encephalized. The entire suite of
variables must be taken into consideration when evaluating differences in
encephalization from species to species, as well as between sexes.
5.2.6. Consideration of the results in light of a few major hypotheses
Ultimately, what the results of this study seem to offer is further support for the
social brain hypothesis (Dunbar 1998). According to this hypothesis, the large brains
characteristic of primates in general have evolved as a result of the complex social
systems found throughout the order. This is consistent with the results of this study.
Ecological conditions may have been what initially sparked the trend toward greater
encephalization, and why there exists such a huge range of EQ values from species to
species, but the extent to which the trait has evolved from one species to the next
47
appears to be tied to the complexity of a species’ social structure. Reproductive
strategy and diet have been the proxy for social structure in this study, as clear,
detailed information on social structure is quite limited. When taken in conjunction
with one another, information on diet and reproductive strategy do offer an adequate
approximation of social complexity, as these two variables determine the kind of
social structure that evolves.
Animals faced with greatest burdens in terms of both resource availability and
mating opportunities show the highest EQ values. These are also the species with the
most complex and competitive social structures, and even more importantly, the
species in which the social burdens are on males are highest. The more egalitarian
species, and those in which males are not competing, turned out to be the least
encephalized. This is consistent with what we would expect and as the social
structures in polyandrous, omnivorous species are generally speaking the least
socially complex, while frugivorous, polygynous ones are the most for reasons
outlined by Wrangham (1986) and van Schaik (1989). That is not to say that the
social structures of polyandrous species are altogether lacking in complexity. When
it comes to primate behaviour, it is a matter of degree with one category of animals
sitting at one end of the continuum and the other sitting at the opposite end. All
species engage in socially complex behaviour to some extent, as primates are, on the
whole, socially complex creatures. Sociality is a hallmark of the primate order
(Shultz and Dunbar 2010).
A final issue worth considering is the way in which the results of this study line up
with a couple of other important hypotheses regarding encephalization. The first of
these is what has been termed the maternal energy hypothesis (Martin 1996). The
second isn’t a formal hypothesis, but a suggestion in the relevant literature that
explains differences in encephalization in terms of differences in basal metabolic
rates (McNab 1987a, McNab 1987b, Weisbecker and Goswami 2010). I will briefly
consider each of these in turn, once again focusing on how the results here either
support, or offer counterexamples to, each hypothesis.
According to the maternal energy hypothesis the process of encephalization occurs
48
primarily as a result of the influence of maternal basal metabolic rate, along with
maternal body size and gestation length (Martin 1996). The latter two variables,
however, play ancillary roles, while maternal basal metabolic rate is the primary
factor influencing brain growth. The idea here is that the mother’s energy turnover
rate determines how encephalized her offspring becomes. More specifically, “the
maternal energy hypothesis proposes that all mammals have the largest brains that
are compatible with the metabolic resources available to their mothers during
gestation and lactation” (Martin 1996 p. 155). Looking at the results of this study, it
seems this hypothesis may hold up when considered in regard to species or families,
but it’s not entirely clear that it does when we examine the differences in
encephalization between males in females of the same species. If maternal basal
metabolic rates determine her offspring’s potential encephalization, it’s not readily
obvious to this author how males and females come to have such different EQs in so
many species. Of course it may be that one of the two other variables, gestation
length or body size, may have a greater impact than has been suggested by the
hypothesis, and the differences may be accounted for in that way. It may also be the
case that maternal basal rates vary according to the sex of the offspring she’s
carrying. Without further information regarding either of these possibilities,
however, it’s difficult to see how the maternal energy hypothesis can provide us with
an explanation of how encephalization occurs in light of the results of this study.
A second line of thought that warrants consideration also explains encephalization in
terms of basal metabolic rates, but the focus is on the encephalized animal, rather
than its mother.
In this case, there doesn’t appear to be a firmly articulated
hypothesis so much as a number of suggestions in the literature on this subject
(McNab 1987a, McNab 1987b, Martin 1996, McNab and Eisenberg 1989,
Weisbecker and Goswami 2010). The suggestion is that an animal’s own BMR,
influences the extent of its encephalization. What the relationship between BMR and
brain development is exactly, a positive or negative correlation with a rapid BMR,
isn’t clear, but assuming that a higher BMR correlates with greater encephalization,
we may have a potential explanation for the differences between males and females
seen in this study. Here again, confounding variables such as body size and gestation
49
length, may need to be explored further before anything more is said on the matter,
but unlike the previous hypothesis, there do not appear to be any obvious
counterexamples to this suggestion in the results of this study.
Having covered the results and some of possible implications that follow from them,
the following chapter will be devoted to a more precise articulation of answers to the
four questions introduced in the aims section of this paper.
50
CHAPTER 6
CONCLUSIONS
6.1: Conclusions
In this section explicit answers to the questions presented in the aims section of this
paper will be provided. Those questions were as follows:

Across the primate order, does one or the other sex exhibit a trend toward
greater encephalization?

In families where one or the other sex is more encephalized, is this trait the
result of canalization or is it derived?

What is the relationship between overall body size, encephalization, and sex?

Is there a correlation between relative brain size and diet, body size, or
reproductive strategy?
6.1.1. Is one sex more encephalized than the other?
On the whole, male primates turn out to be more encephalized than female primates,
though the difference is only apparent once phylogeny is controlled for and species
are taken on a case-by-case basis.
When the raw data is evaluated, without
controlling for phylogeny, and examined at the family taxon level rather than the
species, the results are somewhat misleading. Looking at the data in this way,
females appear to be more encephalized than males in two families, while males are
more encephalized in two others, and the remaining families show no difference at
all between the sexes. These results do not accurately reflect what the general trend
in primates actually is.
The results of the PGLS analysis provide a far more accurate picture. The models
generated by this analysis show us that in species where females appeared to be more
encephalized, the greater encephalization is simply the result of females diverging
51
less from the values the model predicts than males. In these cases, however, both
sexes are still below the expected values for their sex and species. Even more
importantly, in many families where there appeared to be no difference in EQ in the
initial pair-wise analyses, several species were found to have males that were in fact
significantly more encephalized than their female counterparts. This was especially
evident in the hominoidea where the p-values generated by the initial t-test indicated
that there was no difference between male and female EQs. Even a cursory glance of
the scatterplot displaying the residuals shows a very high number of male hominoids
to be significantly more encephalized than not only the females of their respective
species, but all the other animals of both sexes as well.
6.1.2. Is encephalization the result of canalization or is it a derived trait?
Looking at the results of the PGLS analysis, it appears that the extreme
encephalization we see in primates is trait that is present in the order as result of
canalization. With the exception of a few species, the majority of the animals
analyzed in this study fall very close to the slope generated by the model. Very few
diverge significantly from the predicted values. Only the hominoidea sit more than
one standard deviation from values predicted by the model.
What is particularly interesting about these results is that encephalization does not
appear to have evolved, or be evolving, in the same way for both sexes. Looking at
the scatterplots (Fig. 2 and Fig. 3), one thing that is apparent is that the values for
females align much more closely with the predictions than the male values do. On
the basis of this information it may be argued that encephalization in females is
primarily the result of canalization. The results for males seem to tell a slightly
different story. The males in at least two families, the hominoidea and papionini,
appear to have become more encephalized as a result of selection pressures. There
are a couple of exceptions where females are far more encephalized than the model
predicts, but these females are all found in the hominoidea, where their male
counterparts are even further above the predicted values, so it may be the case that
females are simply becoming more encephalized because males are.
The fact that
males always diverge more than females in either direction would appear to indicate
52
that selection is working primarily on males, and only secondarily on females, if at
all. Therefore, it seems that encephalization in males may be a derived trait that has
resulted from sexual selection pressures, as discussed in earlier sections, while
encephalization in females represents a species baseline that is largely the result of
canalization. In short, competition with other males is driving an increase in brain
size among males, while female brain size remains consistent with what would be
expected if the trait were simply being passed on from one generation, or one
species, to the next.
6.1.3. Is there a relationship between body size, encephalization and sex?
When looking at differences between males and females, results of the pair-wise
analyses done comparing EQ and body weight indicate that the relationship between
body size and relative brain size is a loose one, at best. Only in the 5,001-7,500 g
weight class was there a significant difference in the EQ values, with males being
relatively more encephalized than females. This finding was somewhat unexpected,
as it seems to contradict the position articulated by Plavcan regarding the relationship
between the overall level of dimorphism in a species and its body size. It was
anticipated that the larger animals (those in the 7,501 -10,00 g and <10,000 g
categories) would exhibit a similar pattern, but they did not. Only males and females
in that one category demonstrated a statistically significant difference. Looking at
just body weight and EQ (again using Williams’ recommended slope), there were no
significant differences among species in any other weight class.
The more detailed information provided on the scatterplots (Fig. 2 and Fig. 3) further
supports this finding. The largest and most dimorphic animals are not the species in
which we see the highest levels of encephalization. The species with the highest
rates of encephalization are indeed found in the family with the largest animals, the
hominoidea, but it they are not the largest species in that family. According to the
results, it is within the chimpanzee species (Pan troglodytes vellerosus, Pan
troglodytes verus, and Pan troglodytes schweinfurthii) that we see the largest relative
brain sizes. Males in the orangutan species (Pongo abelii and Pongo pygmaeus)
follow closely behind these three along with the fourth chimpanzee subspecies (Pan
53
troglodytes troglodytes), while the males in the two gorilla species (Gorilla gorilla
gorilla and Gorilla gorilla beringei) included in this study have EQ values that fall
below not only all the other male Great Apes, but below the females in that clade as
well.
This is not what we should see in the results if high levels of overall
dimorphism correlate with even higher levels of encephalization. The largest and
most dimorphic male animals are not the most encephalized, despite the fact that
they are the largest animals.
Before discounting the idea that larger bodies result in even larger relative brain sizes
altogether however, it should be noted that female EQ values do actually increase
with increases in body size. It may be the case then that whatever the baseline for
brain size is, within any given species, it is determined by the female values for that
species and the differences we see in males are, once again, driven by sexual
selection pressures. Body size and relative brain size would still be linked, with
sexual selection accounting for the differences we see in just the values for males.
This takes us back to one of the original considerations raised in the introduction of
this paper, that of limitations on female growth. The possibility that reproductive
demands constrain the development of larger female bodies was put forth as a reason
for the apparent differences in male and female body and brain sizes. Looking again
at the differences manifested in the residuals, and how tightly the female values
cluster around the slope the model generated, it may be argued that this explanation
should remain a viable hypothesis. It is clear that some pressure is constraining
variation among females and a review of the results of the other analyses indicates
that, whatever that constraint is, it is likely tied to reproduction in some fashion.
6.1.4. Correlation between encephalization and other variables analyzed
As with the pair-wise comparisons involving just the raw data for body size and
family, the results of the analyses exploring the relationship between EQ and diet and
EQ and reproductive strategy did not appear to indicate any real differences between
males and females. The only differences seen in either of these analyses were in the
values for males and females in polyandrous and monogamous species. The p-values
were a bit too high to be absolutely certain that the differences could not be due to
54
chance, but as discussed previously, they were low enough at 0.0902 and 0.1385 to
warrant further investigation. An examination of the scatterplot showing the species
sorted according to family (fig. 3) revealed that all of the animals in the polygynous
group were found within the New World monkey clades, with no primarily
frugivorous species among them. A fairly high proportion of the monogamous
species were also found among the New World monkeys, with those that weren’t
being found primarily among the prosimians (lemuriformes and galagonidae). Diet
among the monogamous species is, however, more varied. What the net effect of
this difference is is difficult to ascertain as the information on actual diet preferences
is not known with the sort of precision that would be necessary to determine how
much of an effect it may have on the other variables examined.
Nevertheless, as has been discussed previously, there does appear to be a link
between the availability of resources, whatever they may be, the reproductive
strategy typically employed by a species, and the degree of encephalization of that
species.
It seems reasonably safe to assume that the amount, and consistent
availability, of resources available to omnivorous animals would be greater than
those for animals with more limited dietary breadth simply by virtue of the fact that
the loss of one or two preferred foods will not have the same consequences for a less
discriminating animal as it does for one that is highly selective. More options should
translate into less competition, as the total exploitation of one resource does not
result in the depletion of all possible food sources. An omnivorous animal will
simply move on to the next available resource. If competition for resources in the
environment is generally low, because food is readily available to all animals,
intraspecies competition is likely to remain low as well. That is not to say that
competition is entirely absent in resource rich environments, rather that it is likely to
be much higher in resource deprived ones.
As discussed previously, once interspecies competition increases, either because all
available resources have been depleted or the resource a particular species relies on is
no longer available, it is likely intraspecies competition will increase as well. Once
this type of selection pressure is present in a population, it is unlikely to be reversed,
55
even if more resources become available. Once a hierarchical social structure has
been established, it is likely to remain as the condition that facilitates it, differences
in fitness between animals within the species, will also have been established. The
conditions that allow certain animals within a population to thrive and reproduce,
whether they are somatic or cognitive in nature, will continue to put those animals
and their offspring in an advantageous position within their group and so will be
perpetuated from one generation to the next. Bearing this in mind, it seems that the
likelihood of a link between diet, reproductive strategy, and encephalization is quite
strong. The precision of this study, however, was not adequate to ascertain the
strength of the relationship between these variables. The fact that it was not is an
issue that will be addressed in the following, and final, section of this paper.
6.2: Recommendations
As indicated in the final lines of the previous section, the precision of this study was
not at the level it needed to be to make any definite claims regarding the influence of
the individual variables examined on one another. The significance of this matter
was not readily apparent at the outset of this study, but an examination of the results
of the pair-wise comparisons in conjunction with the phylogenetically controlled
analysis has made it clear that the variables are, in fact, connected in various ways.
On this basis, it is recommended that future research on this topic be undertaken with
a proper weighting of the variables involved so the strength of the relationships
between them be more clearly understood. Multivariate analyses would help to
clarify the trends observed in this study and provide a better sense of how significant
a role each variable plays in determining the extent of encephalization in a given
species.
A second, much broader and more general, recommendation would be a
reconsideration the significance of encephalization. This study has shown that male
primates are indeed more relatively encephalized than female primates, but what, if
any, benefit that has conferred on them is still unclear. Encephalization quotients do
56
seem to be tied to all of the different variables looked at in this study, but without a
more precise and detailed assessment of the composition of the brains themselves,
rather than just their size, it seems unlikely that establishing a clear connection
between the variables and the brain size will be possible. This sort of work has
already been undertaken with humans and other apes, so a third, less general,
recommendation would be to continue to expand these studies, looking at how brain
architecture has evolved across the order.
57
REFERENCES
Journals:
Amen-Ra, N. (2006) Humans are evolutionarily adapted to caloric restriction
resulting from ecologically dictated dietary deprivation imposed during the Plio–
Pleistocene period. Medical Hypotheses, 66: 978-984.
Amen-Ra, N. (2007) How dietary restriction catalyzed the evolution of the human
brain: An exposition of the nutritional neurotrophic neoteny theory. Medical
Hypotheses, 69: 1147-1153
Arnold, C., Matthews, L. J. & Nunn, C. L. (2010) The 10kTrees Website: A New
Online Resource for Primate Phylogeny. Evolutionary Anthropology, 19: 114-118.
Araujo, A., Arruda, M.F., Alencar, A.I., Albuquerque, F., Nascimento, M.C., and
Yamamoto, M.E. (2000) Body weight of wild and captive common marmosets
(Callithrix jacchus). International Journal of Primatology. 21: 317–324.
Ashman, T.-L. (2003), Constraints on the evolution of males and sexual dimorphism:
Field estimates of genetic architecture of reproductive traits in three populations of
Gynodioecious fragaria virginiana. Evolution, 57 (9): 2012–2025.
Barton, R. (2006) Primate brain evolution: Integrating comparative,
neurophysiological, and ethological data. Evolutionary Anthropology 15: 224-236.
Barrickman, N. L., Bastian, M.L., Isler, K. and van Schaik, C. P. (2008) Life history
costs and benefits of encephalization: a comparative test using data from long-term
studies of primates in the wild. Journal of Human Evolution, 54:568-590.
58
Bennet, P. M. and Harvey, P.H. (1985) Brain size, development and metabolism in
birds and mammals. Journal of Zoology, 207: 491-509.
Bond, W. and Maze, K. (1999), Survival costs and reproductive benefits of floral
display in a sexually dimorphic dioecious shrub, Leucadendron xanthoconus.
Evolutionary Ecology, 13(1): 1-18.
Bronson, R.T. (1981) Brain-weight body-weight relationships in twelve species of
nonhuman primates. American Journal of Physical Anthropology 56: 77–81.
Clutton-Brock, T.H., Harvey, P.H. and Rudder, B. (1977). Sexual dimorphism,
socionomic sex ratio and body weight in primates. Nature, 269:797-801.
Cosgrove, K. P., Mazure, C. M., and Staley, J. K. (2007) Evolving knowledge of sex
differences in brain structure, function, and chemistry. Biological Psychiatry, 62:
847-855.
Deaner, R. O. and van Schaik, C. P. (2006) Do some taxa have better domain-general
cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary
Psychology 4: 149-196.
Delph, L. F., Gehring, J. L., Frey, F. M., Arntz, A. M. and Levri, M. (2004) Genetic
constraints on floral evolution in a sexually dimorphic plant revealed by artificial
selection. Evolution, 58 (9): 1936–1946. doi: 10.1111/j.0014-3820.2004.tb00481.x
Dunbar, R. (1998) The Social Brain Hypothesis. Evolutionary Anthropology 6(5):
178-190.
Elton, S., Bishop, L.C., and Wood, B. (2001)Comparative context of Plio-Pleistocene
hominin brain evolution. Journal of Human Evolution 41: 1–27.
Estrada, C. and Jiggins C. D. (2008) Interspecific sexual attraction because of
convergence in warning colouration: is there a conflict between natural and sexual
selection in mimetic species? Journal of Evolutionary Biology, 21: 749–760.
doi: 10.1111/j.1420-9101.2008.01517.x
59
Felsenstein, J. (1985) Phylogenies and the comparative method. The American
Naturalist 125(1): 1-16.
Gittelman, J. (1994) Female brain size and parental care in carnivores (mammal).
Proceedings of the National Academy of Science 91: 5495-5497.
Godfrey L., Lyon S., and Sutherland, M. (1993) Sexual dimorphism in large-bodied
primates: The case of the subfossil lemurs. American Journal of Physical
Anthropology 90: 315–334.
Goldstein, J., Seidman, L., Horton, N., Makris, N., Kennedy , D., Caviness, V.,
Faraone, S. and Tsuang, M. (2001) Normal sexual dimorphism of the adult human
brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex 11: 490-497.
Gordon, A.D. (2006) Scaling of size and dimorphism in primates II: macroevolution.
International Journal of Primatology 27: 63–105.
Gould, S. J. (1974) Origin and function of 'bizarre' structures: Antler size and skull
size in 'Irish Elk', Megaloceros giganteus. Evolution 28(2): 191-220.
Hamon, T. R. (2005) Measurement of concurrent selection episodes. Evolution,
59(5): 1096–1103. doi: 10.1111/j.0014-3820.2005.tb01046.x
Harvey, P.H. and Clutton-Brock, T.H. (1985) Life-history variation in primates.
Evolution 39: 559–581.
Harvey, P. H., Kavanagh, M. and Clutton-Brock T. H. (1978) Sexual dimorphism in
primate teeth. Journal of Zoology London 186:474–485.
Healy, S. and Hurly, T. (2004) Spatial learning and memory in birds. Brain Behavior
and Evolution, 63:211-220.
Helmuth, N. (2005) Sex-related differences in general intelligence g, brain size, and
social status, Personality and Individual Differences 39(3): 497-509, ISSN 01918869, DOI: 10.1016/j.paid.2004.12.011.
60
Hereford, J., Hansen, T. F. and Houle, D. (2004) Comparing strengths of directional
selection: How strong is strong?. Evolution, 58(10): 2133–2143. doi: 10.1111/j.00143820.2004.tb01592.x
Hershkovitz, P. (1970) Cerebral fissure patterns in platyrrhine monkeys. Folia
Primatologica. 13: 213–240.
Ikeda, J., and Watanabe, T.,(1966) Morphological studies of Macaca fuscata. III.
Craniometry. Primates 7, 271–288.
Isler, K., Kirk, Joseph, E., Miller, M.A., Albrecht, G., Gelvin, B. and Martin, R.
(2008) Endocranial volumes of primate species: scaling analyses using a
comprehensive and reliable data set. Journal of Human Evolution 55: 967–978.
Jerison, H. (1979) Paleoneurology and the evolution of the mind. Scientific
American 234: 90-101.
Jerison, H. (1979) Brain, Body and Encephalization in Early Primates. Journal of
Human Evolution 8, 615-635.
Kappeler P. (1990) The evolution of sexual size dimorphism in prosimian primates.
American Journal of Primatology 21:201–214.
Kappeler P. (1991) Patterns of sexual dimorphism in body weight among prosimian
primates. Folia Primatologica (Basel) 57: 132–146
Kappeler P. (1999) Primate socioecology: new insights from males.
Naturwissenschaften 85:18–29.
Karubian, J. and Swaddle, J.P. (2001) Selection on females can lead to ‘larger
males’. Proceedings of the Royal Society of London (B) 268:725-728.
King, R. B. (1989) Sexual dimorphism in snake tail length: sexual selection, natural
selection, or morphological constraint?. Biological Journal of the Linnean Society,
38: 133–154. doi: 10.1111/j.1095-8312.1989.tb01570.x
61
Kingslover, J. and Diamond, S. (2010), Phenotypic selection in natural populations:
What limits directional selection? The American Naturalist 177(3): 346-357.
Leutenegger, W. and Cheverud, J. (1982) Correlates of sexual dimorphism in
primates: Ecological and size variables. International Journal of Primatology 3:387–
402.
Lindenfors, P., Nunn, C. and Barton, R. (2007) Primate brain architecture and
selection in relation to sex. BMC Biology 5:20. http://www.biomedcentral.com/17417007/5/20.
Leutenegger, W. and Kelly, J.T. (1977). Relationship of sexual dimorphism in canine
size and body size to social, behavioral and ecological correlates in anthropoid
primates. Primates 18:117– 136.
Marino, L. (1998) A comparison of encephalization between odontocete cetaceans
and anthropoid primates. Brain Behavior and Evolution, 51: 230-238.
Martin, R. (1996) Scaling of the mammalian brain: the Maternal Energy Hypothesis.
Physiology 11 (4) 149-156.
Martin L. (1991) Teeth, sex, and species. Nature 352:111–112.
Mastretti, P. Pellerin, L., Rothman, D. L., and Shulman, R. (1999) Energy on
demand. Science 22 (283): 496-497. [DOI:10.1126/science.283.5401.49
McNab, B.K. 1987a. Basal rate and phylogeny. Functional Ecology 1:159-160.
McNab B. and Eisenberg, J. (1989) Brain size and its relation to the rate of
metabolism in mammals. American Naturalist 133: 157–167.
Mitani J., Gros-Louis J., and Richards A. (1996) Sexual dimorphism, the operational
sex ratio, and the intensity of male competition in polygynous primates. American
Naturalist 147:966–980.
62
Mittermeier R. and van Roosmalen M. (1981) Preliminary observations on habitat
utilization and diet in eight Surinam monkeys. Folia Primatologica 36: 1-39.
Nevo, E. and Beiles, A. (1989) Sexual selection and natural selection in body size
differentiation of subterranean mole rats. Journal of Zoological Systematics and
Evolutionary Research 27: 263–269. doi: 10.1111/j.1439-0469.1989.tb00348.x
Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., Hosaka, K.,
Hunt, K., Itoh, N., Kawanaka, K., and Matsumoto-Oda, A. (2003) Demography,
female life history and reproductive profiles among the chimpanzees of Mahale.
American Journal of Primatology 59(3): 99-121.
Northcutt, R. G. (2001) Evolution of the nervous system: Changing views of brain
evolution. Brain Research Bulletin 55(6): 663-674.
Pilbeam, D., & Gould, S. (1974) Size and scaling in human evolution. Science 186:
892-901.
Pilcher, H. (2004) Grey matter matters for intellect: Intelligence linked to size of key
brain regions. Nature doi:10.1038/news040719-11.
Plavcan, J.M. (2001) Sexual dimorphism in primate evolution. Yearbook of Physical
Anthropology, 44: 25-53.
Plavcan, J. M. and van Schaik C., P. (1994) Canine dimorphism. Evolutionary
Anthropology 2:208–214.
Plavcan J.M and van Schaik C.P. (1997b) Intrasexual competition and body weight
dimorphism in anthropoid primates. American Journal of Physical Anthropology
103: 37–68.
Porter, L. and Christen, A. (2002) Fungus and Callimico goeldii: new insights into
Callimico Goeldii behavior and ecology. Evolutionary Anthropology 11(suppl 1):8790.
63
Raichle, M. and Gusnard, D. (2002) Appraising the brain’s energy budget.
Proceedings of the National Academy of Science, 99 (16): 10237-10239.
Reinius, B., Saetre, P., Leonard, J., Blekhman, R., Merino-Martinez, R., Gilad, Y.
and Jazin, E. (2008) An evolutionarily conserved sexual signature in the primate
brain. PLoS Genetics 4(6): 1-13.
Roth, G., & Dicke, U. (2005) Evolution of the brain and intelligence. TRENDS in
Cognitive Sciences 9(5): 250-257.
Shah, N., Pisapia, D. J., Maniatis, S., Mendelsohn, M. M., Nemes, A., and Axel, R.
(2004) Visualizing sexual dimorphism in the brain. Neuron 43: 313-319.
Schillaci, M.A. (2006) Sexual Selection and the Evolution of Brain Size in Primates.
PLoS ONE 1(1): e62. doi:10.1371/journal.pone.0000062.
Schulke, O., Kappeler, P.M., and Zischler, H. (2004) Small testes size despite high
extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behavioural
Ecology Sociobiology 55: 293–301.
Shultz, S. and Dunbar, R. (2010) Encephalization is not a universal
macroevolutionary phenomenon in mammals but is associated with sociality.
Proceedings of the National Academy of Science, 107(50): 21582-21586.
Smith, R.J. and Jungers, W.L. (1997) Body mass in comparative primatology.
Journal of Human Evolution 32: 523–559.
Taylor, A. B., and van Schaik, C. P. (2006) Variation in brain size and ecology in
Pongo. Journal of Human Evolution 52: 59-71.
Thalmann, U. and Geissmann, T. (2000) Distribution and geographic variation in the
western woolly lemur (Avahi occidentalis) with description of a new species
(A.unicolor). International Journal of Primatology 21: 915–941.
64
van Roosmalen, M. (1985) Habitat preferences, diet, feeding strategy and social
organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in
Surinam. Acta Amazonica 15(3/4, suppl): 1-238.
van Schaik, C. (1989) The ecology of social relationships amongst female primates.
In: Standen, V., & Foley, R. (eds.) Comparative socioecology: The behavioural
ecology of humans and other mammals. Oxford: Blackwell Scientific Publications.
195-219.
Verheyen, W.N., (1962) Contribution a` la craniologie compare ́e des primates:
lesgenres Colobus Illiger 1811 et Cercopithecus Linne ́ 1758. Annual Museum Royal
African Centre 105: 1–255.
Wang, T., Hung, C.2 and Randall, D. (2006) The comparative physiology of food
deprivation: From feast to famine. Annual Review of Physiology 68: 223–51.
Weisbecker, V. and Goswami, A. (2010) Brain size, life history, and metabolism at
the marsupial/placental dichotomy. Proceedings of the National Academy of
Sciences 107: 16216-16221.
White F. (1988) Party composition and dynamics in Pan paniscus. International
Journal of Primatology 9(3): 179-93.
Williams, M. (2002) Primate encephalization and intelligence. Medical Hypotheses
58(4): 284-290.
Wrangham, R. (1986) Ecology and social relationships in two species of
chimpanzees. In: Rubenstein, D. I., & Wrangham, R. W. (eds), Ecological aspects of
social evolution: Birds and mammals. Princeton, N.J: Princeton University Press.
352-378
Books:
Barton R. (1999) The evolutionary ecology of the primate brain. In: Lee PC, editor.
65
Comparative primate socioecology. Cambridge: Cambridge University Press 167–
203.
Darwin, C. R. (1859) On the origin of species by means of natural selection, or the
preservation of favoured races in the struggle for life. London: John Murray. [1st
edition]
Darwin, C. R. (1871) The descent of man, and selection in relation to sex. London:
John Murray. Volume 1. 1st edition.
Hopf, A. and Claussen, C. P. (1970) Comparative studies on the fresh weights of the
brains and spinal cords of Theropithecus gelada, Papio hamadryas, and Cercopithecus aethiops. In: Kummer, H. (Ed.), Proceedings of the 3rd International Congress
Primatology, Zurich, vol. 1. Karger, Basel, pp. 115–121.
McNab, B.K. (1987b) The evolution of mammalian energetics. In: P. Calow, ed.,
Evolutionary Physiological Ecology. Cambridge University Press. pp 219-236.
Okasha, S. (2009) Natural selection in the abstract. Evolution and the Levels of
Selection. USA: Oxford University Press, pp. 10-34.
Plavcan, J. (1999) Mating systems, intrasexual competition and sexual dimorphism
in primates. In: Lee PC, editor. Comparative primate socioecology. Cambridge:
Cambridge University Press. pp 241–269.
Pickford, M. (1986). On the origins of body size dimorphism in primates. In:
Pickford M, Chiarelli B, editors. Sexual dimorphism in living and fossil primates.
Florence: Il Sedicesimo. p 77–91.
Reynolds, J.D. & Harvey, P.H. (1994) Sexual selection and the evolution of sex
differences. In Short R. & Balaban, eds. The Differences Between the Sexes.
Cambridge: Cambridge University Press. pp 53-70.
Smuts BB. (1985) Sex and friendship in baboons. New York: Aldine de Gruyter. pp
303.
66
White F. (1996) Comparative socioecology of Pan paniscus. In: McGrew W.,
Marchant L., and Nishida T., editors. Great ape societies. Cambridge, England:
Cambridge University Press; p 29-41.
Internet pages:
Wilson, E. O. (2011) Where does good come from? Boston.com
http://www.boston.com/bostonglobe/ideas/articles/2011/04/17/where_does_good_co
me_from/?page=full Accessed May 2011.
Coyne, J. (2011) The Boston Globe on kin selection. Why Evolution is True.
http://whyevolutionistrue.wordpress.com/2011/04/17/the-boston-globe-on-kinselection/ Accessed May 2011.
Mastretti, P., Pellerin, L. and Martin, J. Brain energy metabolism. American College
of Neuropsychopharmacology.
http://www.acnp.org/g4/GN401000064/CH064.HTML Accessed July 2011.
Primate Info Net Library and Informatin Service. National Primate Research Center,
Univeristy of Wisconsin – Madison. Primate Fact Sheets. http://pin.primate.wisc.edu/
Accessed May through September 2011.
Animal Diversity Web – University of Michigan Museum of Zoology.
http://animaldiversity.ummz.umich.edu/site/index.html Accessed May through
September 2001.
IUCN (International Union for Conservation of Nature) Red list – The IUCN Red
List of Threatened Species. http://www.iucnredlist.org/ Accessed May through
September 2001.
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