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)

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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explicitly acknowledged (including citation of published and unpublished sources).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...............................................................................................................33

DISCUSSION.............................................................................................................33

5.1: Introduction.....................................................................................................33

5.2: Discussion........................................................................................................33

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...............................................................................................................49

CONCLUSIONS........................................................................................................49

6.1: Conclusions.....................................................................................................49

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...........................................................................................53

REFERENCES...........................................................................................................55

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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.

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Phenotypes once thought to be the result of sexual selection have begun to be re-

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

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natural and sexual selection (Bond and Maze 1999; Ashman 2003; Delph et. al.

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.

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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

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

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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

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.

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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

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

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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

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.

12

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

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.

13

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

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

14

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.

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

15

…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

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 post-

cranial 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,

16

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.

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 cross-

referenced 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.

Family

Mean Male

Brain Mass

Mean Female

Brain Mass

Brain Mass

P-value

Mean Male Body Mass

Mean Female

Body Mass

Body Mass

P-value

Mean Male

EQ

Mean Femal

e EQEQ

P-valueLemuriformes 18.82 18.63 0.2889 1758 1825 0.0661 2.26 2.24 0.2710Loridae 10.97 10.16 0.0054 634 607 0.1596 1.82 1.71 0.0042*Galagonidae 7.36 6.91 0.0224 456 432 0.0103 1.34 1.29 0.0753Tarsidae 3.70 3.49 0.0666 456 116 0.0103 0.95 0.92 0.1035Pitheciidae 20.22 19.81 0.1074 1078 1003 0.1795 2.86 2.87 0.4788Cebidae 31.74 30.40 0.0011 1364 1079 0.0001 3.93 4.03 0.0007*Atelidae 87.68 84.36 0.0177 8012 6722 0.0011 7.07 7.08 0.4717Cercopithec. 73.81 64.52 0.0000 5874 3716 0.0000 6.53 6.48 0.1524Papionini 111.70 101.07 0.0000 12452 7377 0.0000 8.08 8.35 0.0248*Colobinae 76.35 69.22 0.0000 8150 6944 0.0003 6.18 5.82 0.0000*Hominoidea 269.48 237.99 0.0002 45884 27651 0.0020 13.77 13.60 0.2681*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 P-

values 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.

0 20 40 60 80 100 120 140 160

-100

-50

0

50

100

150

200

250

300

350Residuals - Encephalization and sex - Controlled for Phylogeny

Female residuals

Linear (Female residuals)

Male residuals

Linear (Male residuals)

Model generated slope - based on phylogenetically generalized least squares (PGLS)

Res

idu

als

for

each

sp

ecie

s

29

0 5 10 15 20 25 30 35

-100

-50

0

50

100

150

200

250

300

350Figure 3. Male and Female Residuals by Sex and Family

Male Cercopithecines

Female Cercopithecines

Male Lemuriformes

Female Lemuriformes

Male Atelidae

Female Atelidae

Male Cebidae

Female Cebidae

Male Loridae

Female Loridae

Male Hominoidea

Female Hominoidea

Male Pitheciidea

Female Pitheciidea

Male Papionini

Female Papionini

Male Colobinae

Female Colobinae

Male Galagonidae & Tarsiidae

Female 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

Body Size

Mean Male Body Mass

Mean Female

Body Mass

Mean Male EQ

Mean Female EQ P-value

0-500g 264 261 1.32 1.34 0.1698501-1000g 758 690 2.56 2.55 0.38541001-2500g 1839 1697 3.60 3.59 0.43462501-5000g 4323 3180 6.46 6.45 0.38525001-7500g 6700 5709 6.79 6.56 0.0002*7501-10000g 9760 7408 7.16 7.15 0.4205>10000g 50630 28999 13.37 13.48 0.3602

*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 Mean EQ Males Mean EQ Females P-value

Fruit 7.38 7.41 0.3681Fruit plus 2.11 2.12 0.4093Gum 1.34 1.34 0.4849Insects 1.10 1.08 0.3021Leaves 5.34 5.36 0.4487Leaves & Fruit 6.12 5.98 0.1432Omnivorous 5.98 6.02 0.3035Seeds 6.26 6.43 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 Mean EQ Males Mean EQ Females P-value

Polygynous 5.62 5.60 0.3571Polyandrous 3.32 3.39 0.0902Monogamous 4.28 4.24 0.1385Polygynandrous 8.29 8.35 0.2477Varied 2.86 2.85 0.4105Unknown 4.12 4.13 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.

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

32

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 pair-

wise 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

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