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M.Sc. in Human Evolution and Behaviour Dissertation Neurological sexual dimorphism and competing selection pressures Monica Nelson Dissertation submitted in partial fulfilment of the requirements for the degree M.Sc. in Human Evolution and Behaviour (UCL) of the University of London in 2011 Word Count: 18,543 UNIVERSITY COLLEGE LONDON DEPARTMENT OF ANTHROPOLOGY Note: This dissertation is an unrevised examination copy for consultation only and it should not be quoted or cited without the permission of the Chairman of the Board of Examiners M.Sc. in Human Evolution and Behaviour (UCL) i Declaration of originality This is to certify that the work is entirely my own and not of any other person, unless explicitly acknowledged (including citation of published and unpublished sources). The work has not previously been submitted in any form to the University College of London or to any other institution for assessment for any other purpose. Signed _________________________________________________ Date ___________________________________________________ ii 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. iii 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 iv 4.2.3: Dietary Composition…………………………………………………30 4.2.4: Reproductive Strategy……………………………………………….31 4.3: Discussion of results…………………………………………………………31 CHAPTER 5 .............................................................................................................. 34 DISCUSSION ............................................................................................................ 34 5.1: Introduction ..................................................................................................... 34 5.2: Discussion ....................................................................................................... 34 5.2.1: Results by Family……………………………………………………33 5.2.2: Results and Body Size……………………………………………….36 5.2.3: Results and Diet……………………………………………………...37 5.2.4: Results and Reproductive Strategy…………………………………..40 5.2.5: Synthesis……………………………………………………………..42 5.2.6: Consideration of Results in light of a few major hypotheses………..46 CHAPTER 6 .............................................................................................................. 51 CONCLUSIONS ........................................................................................................ 51 6.1: Conclusions ..................................................................................................... 51 6.1.1: Is one sex more encephalized than the other?......................................49 6.1.2: Is encephalization a primitive or derived trait?...................................50 6.1.3: Is there a relationship between body size, encephalization and sex?..51 6.1.4: Correlation between encephalization and other variables analyzed?..52 6.2: Recommendations ........................................................................................... 56 REFERENCES........................................................................................................... 58 v 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 vi 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 1 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 2 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. 3 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. 4 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. 5 2.2: Natural Selection and Sexual Selection Though the same overarching principles that govern natural selection apply in equal measure to sexual selection, the two processes often seem to act in opposition to one another (Gould 1974; King 1989; Nevo & Belles 1989; Estrada & Jiggins 2008). Variation, heritability, overpopulation, and differential fitness are factors in both types of selection, but while sexual selection may reasonably thought of a subclass in the class of all pressures that drive natural selection, it is often the case that sexual selection appears to either cancel out or override to be more general interspecies natural selection pressures such as those resulting from ecological or physiological constraints. This one aspect of natural selection is of such key importance that Darwin followed up his own seminal work (1859) with a second tome, The descent of man, and selection in relation to sex (1871), which was entirely devoted to trying to explain the mechanisms involved in it. In this section the relationship between interspecies competition, or natural selection broadly speaking, and sexual selection is explored. Ultimately, the key difference between natural selection and sexual selection lies between the species, or the population, and the individual. Natural selection and sexual selection are not two distinct processes, but rather the same process working at different taxon levels. Natural selection works at the interspecies level to create new species, whereas sexual selection involves intraspecies selection. Competition at the intraspecies level involves members of the same sex who compete to secure reproductive opportunities (Reynolds, J. D. and Harvey, P.H. 1994; Strier 2011). This type of competition often gives rise to phenotypically dimorphic traits between males and females. Darwin attributed the widespread occurrence of traits that seem to serve no purpose with regard to survival, such as bawdy colouring or heavy ornamentation, to this type of selection (1871). Robert Trivers (1972) later refined the hypothesis, by explicitly outlining the roles of male-male competition and female mate choice. Since that time a number of other models of selection have been suggested and the clarity of these earlier hypotheses has become slightly muddled. Phenotypes once thought to be the result of sexual selection have begun to be re- 6 examined and considered in light of less obvious benefits that they may confer at a much broader level. Traits that have historically been classified as having been evolved as a result of sexual selection, such as canine tooth length and body mass dimorphism, are not necessarily secondary sexual characteristics at all. A number of researchers (Clutton-Brock et al., 1977; Leutenegger and Kelly, 1977; Harvey et al., 1978; Martin et al., 1994; Plavcan and van Schaik, 1994) have looked at the possibility that these features are actually the byproduct of natural selection, resulting from the heavier ecological demands on one sex or the other. Even more interestingly, certain traits that may evolve as the result of sexual selection can be lost as a result of natural selection pressures, and traits that may have originally evolved under one or the other type of pressure may be reinforced or exaggerated as a result of a different pressure. Kingslover and Diamond (2010) discuss in some detail the various mechanisms that may limit the strength of directional selection. The points they raise, however, may be applicable to any given type of selection. They identified five different ways in which the selection strength may be compromised. Among the mechanisms they discuss are 1) a limited genetic variation, 2) trade offs between different selection pressures such as those discussed in the previous paragraph, 3) direct selection on one trait which results in correlated, indirect selection on a trait in the opposite direction, 4) changes in selection pressure over time and 5) the possibility that stabilizing selection is stronger and more common than was previously thought. At least the first three points mentioned above should be borne in mind when evaluating sexually dimorphic traits, as it often the case that environmental constraints cap what would otherwise be runaway sexual selection, and it is always the case with sexually reproducing organisms that genetic variation is linked with primary sex differences. The results from studies involving a variety of plants, insects, and animals have shown that the points considered by Kingslover and Diamond are empirically supported. Even in plants there exists a constant push-pull relationship between natural and sexual selection (Bond and Maze 1999; Ashman 2003; Delph et. al. 7 2004), with ecological features limiting or enhancing the extent of dimorphism in flowering plants. Likewise, with insects (Estrada and Jiggins 2008), fish (Hamon 2005), reptiles (King 1989), birds (Karubian and Swaddle 2001) and mammals (Gould 1974). In mimetic insects, such as butterflies and moths, natural selection may work to enhance the effect of sexual selection, or perhaps vice versa, by enhancing the ability of males to detect mates and predators. The biochemical processes involved in mate recognition have simultaneously evolved to assist in predator avoidance (Estrada and Jiggins 2008). In fish, predators more easily identify showy males. Therefore, when the risk of predation is high the less sexy, duller-coloured phenotypes are more successful at both reproducing and staying alive (Hamon 2005). The longer tail length seen in many male snakes appears to be a byproduct of both natural and sexual selection in that longer tail length in males is the result of morphological constraints on the entire order, or natural selection, while shorter tail length in females enhances reproductive output, giving shorter-tailed females an advantage over other females of their own species (King 1989). Here sexual, selection is working on one sex while natural selection is driving the same phenomenon in the other. In birds, a very similar scenario appears to have played out with regard to wing length. The gap in wing size is the result of different selection pressures on males and females. Ecological constraints work to put a cap on female size while male-male competition has simultaneously favours broader wingspan in males. Mammalian examples also pervade the literature, with Gould’s famous Irish Elk example (1974) being one of the most famous. In this case, antler size is restricted by natural selection constraints while sexual selection drives has driven an increase size. Females prefer males with large antlers and males with large antlers fare better in contests with other males, but once a certain limit is reached the costs to the animal in terms of nutrition and its ability to successfully navigate the environment are too great to allow for any further increase. 2.3: Sexual Dimorphism without Sexual Selection Having surveyed the ways in which natural and sexual selection both work together and in opposition to one another, this section will be devoted to examining scenarios 8 in which sexual dimorphism may arise without sexual selection as the primary driving force. In a fairly comprehensive discussion of this topic Plavcan (2001) states, “Dimorphism in various traits is known to be correlated with body mass, diet, substrate, phylogeny, and even rainfall” and points out that “Each of these correlations may reflect a variety of different mechanisms affecting the expression and evolution of dimorphism” (p. 40). How some of these factors may influence the development of sexual dimorphism will now be explored. The correlation between body size and dimorphism found in many primates is not unique to the family and has been shown to exist in a number of species. Plavcan 2001 p. 41) noted that, “Sexual dimorphism in body mass and canine tooth size is correlated with overall body size (Clutton-Brock et al., 1977; Harvey et al., 1978; Leutenegger and Cheverud, 1982, 1985; Gautier-Hion and Gautier, 1985; Cheverud et al., 1985; Plavcan and van Schaik, 1992, 1994, 1997b; Pickford, 1986; Plavcan, 1999)”, explaining that with an increase in the overall size of the animals in particular species, there is an accompanying increase in the quantitative distance between male and female body size. Essentially, the bigger the animal in question is, the greater the degree of dimorphism will be. In smaller animals, the difference in size between males and females will be less than that found between males and females in larger species. So, in large animals a larger male may be much larger than his female counter part, simply by virtue of the fact that the animals are large, rather than as the result of sexual selection. The relationship between body mass and degree of dimorphism is not necessarily allometric, however. Males may far exceed or fall below the predicted mean size for the trait in question (such as height, weight, cranial volume, etc.) and, likewise, for females. A number of explanations for how this may come to pass have been suggested. Clutton-Brock et. al. (1977) have offered five ways in which dimorphism can arise that may undermine a strictly allometric model, which are also not the result of direct sexual selection. First, there may be a correlated response between sexes if larger body size is selected for in either. If ecological conditions favour an increase (or decrease) in size for 9 males, then females may become larger as well and vice versa. Second, among larger animals there are fewer species competing for the same resources. This may in turn translate into fewer constraints on body size, especially among males. Because competition is low at this level, males may grow unchecked regardless of whether there is intraspecies competition, and if either sex can grow unchecked, the gap in size between the two will widen even more than it would if both were kept in check in the same manner and to the same extent. In this case it wouldn’t be a case of larger size being selected for, but an absence of a selection pressure against it. Third, there may be less cost involved with an increase in size for males. This possibility will be taken up in further detail in the following sections, but essentially what this means is that the metabolic demands of building and sustaining the body of a female animal may be more costly in terms of resources than that for males, so female growth may be limited while male is less so. The fourth mechanism suggested is a possible reduction in feeding competition where the food quality is poor and the species in question feeds in clumps. A marked difference in size between the sexes may offset the natural competition for resources by reducing the caloric or nutritional needs of the smaller sex. Here, gorillas may provide a good example. The quality of their diet is generally quite low, they feed together, and females are significantly smaller. The females are roughly half the size of males and, as a result, require far few calories to meet their own metabolic demands. The fifth and final suggestion they outline is closely tied to the third. In this case, the idea is that there is pressure on females to remain smaller in order to reach maturity sooner. The body of any animal can only mature as quickly as resources in the environment can provide nourishment and facilitate growth, so a smaller adult body size is more quickly and easily reached than a larger one. Whether any one, or all of, the five mechanisms outlined above is empirically supported is still up for debate, but a number of studies conducted since the paper cited above was originally published have shown that they do seem to offer viable alternatives, or perhaps complementary adjuncts, to the sexual selection hypotheses (Kappeler, 1990, 1991; Godfrey et al., 1993; Mitani et al., 1996; Plavcan and van Schaik, 1997b; Plavcan, 1999). Group size, dietary composition and quality, and 10 ecological constraints do influence the extent to which dimorphism in body mass may manifest itself in a given species. Contrast analyses have shown there is correlation between shifts in expected values based on allometry and these elements, demonstrating that sexual selection alone should not be regarded as the sole contributing factor when evaluating size differences between males and females. Additionally, there are cases where both natural and sexual selection are working alternately to shape a particular trait, but sexual selection is not the primary force at work. For example, in any given species, the size of the individual animals will influence the type of social structure that evolves for the species. This in turn influences mating behaviour, making what may have been a trait that originally evolved as result of natural selection pressures shift in one direction or the other under sexual selection pressure. Plavcan provides an illustration, pointing out that “at larger body sizes, females tend to form large groups which makes it easier for males to try to exclude other males from access to females” (2001, p. 41). Here, the larger body size of females may have originally evolved as a result of a correlated response to an increase in male body size (which may have evolved as a result of any of the natural selection mechanisms discussed above). The increase in size results in a change in social behaviour which in turn makes it easier for males to monopolize females, making the large male offspring of large females more successful reproductively and perhaps more attractive as suitors of the large, clumped females. The large body size that originally evolved as a result of natural selection pressures is then perpetuated as a result of sexual selection. Of course these mechanisms may also be operating in a similar manner at the level of much more specific traits or phenotypes. Sexual dimorphism may be exhibited in something as unique as a single tooth or even a small section of the brain. In the next section some of the literature on neurological sexual dimorphism, as expressed via differences in the brain, will be surveyed. 2.4: Neurological Sexual Dimorphism Current research on the subject of neurological sexual dimorphism is predominantly aimed at discovering differences in certain structures or substructures within the 11 brain (Lindenfors et. al. 2007; Renius et. al. 2008), as well as microscopic and biochemical dissimilarities between male and female brains (Shah et. al. 2004; Cosgrove et. al. 2007). This has not, however, always been the case, and the larger issue of overall differences in brain size has remained a hot topic (Gittelman 1994; Nyborg, H. 2005). Because the main focus of this research project is brain size dimorphism, and relative brain size more specifically, the bulk of this section will be directed at an examination of the literature regarding overall brain size, first in terms of gross size difference and second in terms of relative difference. As mentioned previously, overall brain size has long been recognized as a significant feature in animals that exhibit cognitively complex behaviours. The idea that bigger equals better, or at least smarter, is one that goes back at least a century and a half (Darwin 1871; Northcutt 2001). Sheer volume of grey matter does seem to correlate with an ability to perform intellectually demanding tasks, at least in humans (Pilcher 2004; Haier et. al. 2004). We also have a great deal of evidence that large brains and intelligence often go hand in hand in other animals and, though the matter of what intelligence properly consists in is far from settled, other apes, cetaceans, and elephants have long been recognized as particularly intelligent animals (Roth and Dicke 2005; Marino 1998). All of these large-bodied mammals possess brains that are exceptionally large, particularly when measured against the brain sizes of animals with similar body sizes in other classes. For example birds, such as the ostrich and emu, have far smaller brains than apes though their body size is quite similar (Bennett and Harvey 1985). The same holds true for reptiles, amphibians, and fish. The general consensus at present is that it is complex social behaviour in conjunction with the demands of reproduction under precarious ecological conditions have driven the trend toward greater encephalization in mammals, relative to that of other animals of similar size in other classes (Shultz and Dunbar 2010; Barrickman et. al. 2008). The trend is especially pronounced in primates (Deaner et. al. 2006), but 12 differences in brain size are also found within families in other orders that are consistent with this position (Gittelman 1994). Interestingly, the differences in brain size between species in the same family are most marked between females. For instance, Taylor and van Schaik (2007) found that among pongids differences in diet quality, life history, and habitat translated into differences in brain size amongst females from species to species, but not males. In a similar vein, Gittelman observed that brain size differences corresponded to differences in ecology and life history in female terrestrial carnivora but males showed no such pattern. If ecological and evolutionary pressures are exerting greater force (in either direction) on overall brain growth in females than in males, one sex or the other will end up with larger brains. The general pattern in mammals is one in which it is typically males who have evolved to possess greater absolute brain size. Absolute brain size may not actually be a particularly significant issue, however. If the same pressures that have brought about a reduction in brain size have also driven an overall reduction in the size of the entire animal one would not expect the smaller animals to have brains the same size as that of the larger ones. Likewise, we would predict that two animals of the same species, of different sizes, would have different sized brains, just as we would expect them to exhibit differences in sizes of most of their organs. What would be unusual would be an overall reduction in size without a corresponding decrease in brain size. Simply measuring gross brain size without taking into consideration changes in the physiology of the entire organism may create a misleading picture of what is actually taking place as, in these cases, the dimorphism isn’t actually neurological but rooted in a difference in overall body mass. The difference in brain size may be strictly allometric and, therefore, not indicative of anything particularly interesting about brains or their specific evolution. This brings us to our second topic of consideration, relative brain size. Because females are generally smaller overall in most dimorphic species, it is expected that female animals will have smaller brains than their male counterparts. Having less overall body mass, it stands to reason that specific parts of their anatomy 13 will also be smaller. Bearing this in mind, neurological dimorphism must also be considered in terms of relative brain size. Unfortunately, because there is little agreement on how best understand and measure differences in relative brain size, the body of literature on this topic is far more limited than that involving research on overall brain size. For reasons explained in the earlier section on sexual dimorphism and sexual selection (Plavcan 2001), it is not entirely obvious what sort differences we should expect to see here. Moreover, what the appropriate mathematical model for determining EQ, or measurements from the expected relative brain size, has not been established (Williams 2001; Jerison 1979; Pilbeam and Gould 1974). That said, there is a relatively large corpus of raw data available (Isler et. al. 2008) for analysis that may be used with any of the models currently suggested. With this project, I hope to shed further light on the question of whether there exist legitimate differences in relative brain size, using this data. If the differences in size are simply allometric, this one line of inquiry may finally be put to rest. If not, fodder for further research will be made available. Before moving on, however, hypotheses involving explanations of how encephalization occurs in the first place will be considered. 2.5: Encephalization and Neotonization Amen-Ra’s 2007 paper introducing the neurotrophic neotonization theory is not the first essay to suggest a hypothesis of this sort. The idea that brain size and density increases with repeated exposure to famine conditions is one that has been present in the scientific literature for some time. One of the earliest, now widely cited, research projects asserting a correlation between brain size increases with a reduction in certain postcranial structures was conducted by Aiello and Wheeler (1995). The findings from their project were documented in paper that established what has come to be known as the expensive tissue hypothesis. Amen-Ra and a number of other researchers have been working since that time to explain, with greater and greater precision, how exactly this process may have occurred in physiological terms. In this section the research and literature on this phenomenon will be examined and discussed. 14 A great deal of work has been done investigating the metabolic requirements involved in developing and maintaining large brains and much has been discovered (Magistretti et. al. 1999). In humans, the brain makes up less than 2% of the total body weight but is responsible for 20-25% of an individual’s energy consumption (Magistretti et. al. 2000; Raichle and Gusnard 2002). In other primates the energetic demands of the brain varies from species to species but tends to be relatively high as well, though not as high as it is in humans (Magistretti et al. 2000). How we’ve evolved to meet the energetic demands of our large brains appears to have involved a forfeiture of other metabolically demanding tissues. In humans, the loss of gut tissue is one of the most obvious places where this trade-off has occurred (Aiello and Wheeler 1995), but the overall volume of post-cranial lean tissue is markedly less in primates than in a number of other animals outside of the order with similar brain sizes (Roth and Dicke 2005). In order to understand the shift toward greater encephalization seen not just in humans, but across the entire primate order as well, it is necessary to look at both proximate and ultimate causes. The physiological processes that occur within the animals are what bring about actual changes in morphology, but they are driven by external events. Research focusing on the evolution of what has been termed the human quadripartite complex (Amen-Ra 2006) has been key in helping expand our understanding of how extreme encephalization occurs. Investigations involving the connection between long lifespan, low reproductive potential, lengthy development and high brain/bodyweight ratio in hominid populations have resulted in discoveries relating to both the proximate and ultimate causes of encephalization. The N3 hypothesis, which lays out the metabolic processes, or proximate causes, that have resulted in the extreme encephalization we see in modern human beings is explained as follows …humans exhibit an altered pattern of neurotrophin expression resulting from positive selection for heightened intelligence amidst environmental deterioration and consequent dietary deficiency. The altered pattern of neurotrophin expression exhibited by humans, it is deduced, results in a 15 protracted phase of developmental neurogenesis and a resultant retention of neurons that would otherwise be extirpated due to programmed cell death. Importantly, during neonatal neurogenesis mammals produce an excess number of neurons whose eventual destruction is dictated by neurotrophic factors (Amen-Ra 2007, p. 1147). In layman’s terms what this says is that, under famine conditions, brain tissue is not only preserved but new growth is triggered as well. Moreover, the normal loss of brain tissue that would occur under non-famine conditions is inhibited. This process is crucial to understanding how something like Aiello and Wheeler’s expensive tissue hypothesis may work. In that case, the gut tissue would be reduced over time just as all lean tissue would be, but the brain is preserved and grows. Over several generations, incremental growth of the brain without immediate concomitant postcranial growth and further gut reduction results in the evolution of a relatively small ape with a large brain. This is not, however, a Lamarckian explanation. There is a genetic component, common to a number of mammals, driving the process described further below. Studies involving mammals both inside and outside the primate order have shown that the metabolic activities that brought about an increase in the relative brain size of hominids are not unique to humans (Burkhalter et. al. 2003). The biochemical processes that are set in motion when an organism is faced with a shortage of resources lead to the preservation or growth of new neural tissue in other animals as well (Wang et. al. 2006). As a mammalian body begins to waste, post-cranially, chemical signals triggering both brain preservation and growth are initiated by a series of interconnected metabolic actions. Studies contrasting the effects of famine on various animals showed that in rats an “increased expression of genes encoding orexigenic, hypothalamic peptides such as neuropeptide Y, agouti-related protein, and pro-opiomelanocortin” (p. 232) may be tied to changes that take place in the gut tissue of the animals during the final stages of starvation. If the rats survive this last phase and refeeding commences the changes resulting from the influence of the neuropeptides on the brain are not reversed, the normal breakdown simply resumes. 16 The increased encephalization is the result of epigenetic factors, but it is the expression of certain genes that determine gut reduction and neuropeptide increases. As such the increase in brain size, or at least the propensity for it, is to a certain degree heritable. If the mechanisms driving the propensity for brain growth are even partially driven by a genetic component, natural selection can operate on them. If natural selection is operating on a trait, we may expect to see differences in the degree to which that trait is expressed in different populations. In this case, if famine is bringing about an increase in the growth of neurological tissue in conjunction with the loss of postcranial tissue, we might predict that populations that more susceptible to the effects of famine, in terms of mortality and reproductive success, may show a greater degree of encephalization. 17 CHAPTER 3 DATA AND METHODS 3.1: Introduction To test the hypothesis that greater relative brain size has been selected for in one sex, or the other, a data set collected by Isler et. al. (2008) from an earlier study involving research on primate endocranial volume was used. The original set assembled by Isler and colleagues included measurements of endocranial volume and body mass for 276 primate species, and was sorted according to sex. The data for these animals had been obtained from a number of earlier published studies conducted on both wild and captive populations of primates from all over the world. For the purpose of testing the hypotheses laid out previously, the data for the animals included in this project were statistically analyzed along four dimensions. These categories included family, body size, diet, and reproductive strategy. Once each of these quantitative analyses was complete, phylogeny was controlled for and results were re-evaluated. 3.2: Data Used The data that was used for this research paper involved only 213 of the original 276 animals included in the original data set from the 2008 study by Isler et. al.. The 63 animals that were not included were rejected on the basis of incomplete information. With these animals values for body size, endocranial volume or sex were missing from the data set. Additionally, for certain analyses, such as diet and reproductive strategy, subspecies were omitted from the analysis in order to avoid skewing the results on the basis of redundancy (for example only data for only one subspecies of P. troglodytes was used, rather than all four of the subspecies of common chimpanzee, in the omnivore group). 18 3.2.1: Spatial and temporal characteristics The original data, which comprise the data set used in this study, was collected and compiled by researchers from all over the world over a period of several decades. The studies included began in the middle of the 20th century and culminated with the with the Isler et. al. study in 2008. The numbers reported all represent mean values of measurements taken for each species, or subspecies, of each sex. Endocranial volumes were contributed by researchers working on the 2008 study with additional data provided by Harvey and Clutton-Brock (1985), Verheyen (1962), Hopf and Claussen (1970), Bronson (1981), Ikeda and Watanabe (1966), Hershkovitz (1970), and Elton et. al. (2001). In some cases actual brain mass volumes were collected but these numbers were not provided. All cranial data was listed in terms of endocranial volume. Information on body mass was also collected by the research group working on the Isler et. al. study, with additional contributions from Smith and Jungers (1997), Gordon (2006), Araujo et. al. (2000), Schulke et. al. (2004), Thalmann and Geissmann (2000)and Kappeler (1991). Information on data quality and the number of animals included measured for each species was also collected and included with the data set. 3.3: Methods and techniques Because the data did not include either actual brain volumes or encephalization quotients, both measurements needed to be estimated. In the case of the former, the model recommended by Rightmire (2004) was followed. Brain mass was estimated by taking the endocranial volume, multiplying it by 0.976, and then multiplying that figure by 1.147. Once brain mass volumes for all the animals were obtained, the encephalization quotient was determined by dividing brain mass volume by body mass volume and multiplying that figure by a slope measurement of 0.28 for each animal. The decision to use William’s (2002) recommended slope of 0.28, rather than 0.67 or 0.75 (Jerison 1979), was motivated by two factors. First, William’s formula is the only one specifically geared toward measuring the encephalization of primates. Previous suggested slopes were aimed at assessing encephalization of either all terrestrial animals, including birds and reptiles, or all mammals. William’s 19 formula is the only one of the three that specifically takes into account phylogeny. Additionally, 0.28 is the most conservative of the three slopes suggested in the literature (Jerison 1979; Pilbeam and Gould 1974) and, therefore, the least likely to exaggerate differences. This ultimately made it easier to assess whether genuine differences existed between the sexes. This second factor was not essential to the study, as statistical analyses made clear where legitimate differences were to be found, but starting with a more conservative figure made it easier to see where the largest disparities existed during the initial evaluation of the data. After all of the necessary figures that could be estimated were obtained, data for the 213 animals with complete information were sorted into the various categories briefly described above and in more detail below. The data was then statistically analyzed, and then re-examined once phylogeny had been controlled for. 3.3.1: Data Analysis 3.3.1.1: Family Once values for brain mass and EQ were obtained the data points were sorted and separated according to taxonomic family. The divisions were made according to the taxonomic classes on the 10kTrees website (Arnold et. al. 2010). This was done in order to prepare the data for eventual phylogenetic analysis. The result of sorting the species in this way was the creation of eleven separate groups. These groups included the following families: lemuriformes, loridae, galgonidae, tarsidae, pitheciidae, cebidae, atelidae, cercopithecini, papionini, colobinae, and hominoidea. The New World monkeys were not sorted into the five categories typical usually employed in classification were collapsed into four, with the callitrichidae being included in the cebidae group on the basis of phylogeny. Once all of the animals were sorted according to family, the encephalization quotients obtained using the mean brain volume values of males and females were compared. The data was analyzed for statistically significant differences using a one-tailed Pearson’s t-test in Excel. A pair-wise comparison of EQ values for males 20 and females was done for each family. P-values of less than 0.05 were considered statistically significant. Because all of the animals in each family share in common a particular genetic heritage, and therefore do not represent independent data points, it was necessary to reanalyze the data, taking phylogeny into consideration. Doing this made it possible to establish whether the differences observed in the initial analyses were the result of a trend consistent with a primitive trait or had been selected for (Felsenstein 1985). Therefore, after the initial set of analyses, in which the animals were sorted into families and the EQ values obtained using the slope recommended by Williams (2001) were used to t-test each family for statistically significant differences, an additional set of analyses was done in which the difference were reassessed with phylogeny controlled for. To control for phylogeny, values from tree files generated by 10kTrees.com, utilizing information provided by GenBank, were generated. Those trees were then input into the R statistics program along with the mean values for brain and body mass for each species and a PGLS (Phylogenetic generalized least squares) analysis was done. Residuals from that analysis were then compared to evaluate whether the original differences remained once phylogeny had been controlled for. 3.3.1.2: Body Size Once all of the data had been analyzed by sex according to family, it was then evaluated in terms of the overall size of the animals. As discussed in the previous section, a correlation between body size and degree of dimorphism has been suggested (Plavcan 2001). Larger animals do appear to exhibit greater dimorphism than smaller ones. To test this theory the animals in this data set were divided up according size, independently of family, and then pair-wise comparisons were done in the same manner as had been done in the initial comparisons done according to taxonomic grouping. The data on body size was included in the original data set as specified above, so it was simply broken up into smaller sets according to size, from smallest to largest, 21 based on what appeared to be natural divisions in the data. Initially, the animals were sorted into a half dozen groups. The divisions were (1) >500g, (2) 501 – 1,000g, (3) 1,001 – 2,500g, (4) 2,501 – 5,000g, (5) 5,001 – 10,000g, and (6) <10,000g. Almost half of the entire set of data points ended up falling into the fifth category, so this group was further divided into two in order to get a clearer picture of where differences might lie should they exist. With this last division, there were a total of seven size classes that were tested. These included five of the original six (1,2,3,4, and 6) plus additional categories for animals weighing between 5,001 – 7,500g and 7,501 – 10,000g. As with the analyses done according to family and phylogeny, the mean EQ values of each sex were compared using Pearson’s one tail t-test. Values of less than .05 were considered significant. 3.3.1.3: Diet Theories regarding the influence of dietary composition have been a major component of both anthropological and archaeological studies for several decades. The degree to which diet has been a significant factor in shaping the neurological development of other primates is therefore an important line of enquiry to consider when looking at dimorphism reflected in brain size. Recognizing this, it was decided that the data should be analyzed along these lines. The data set was resorted once again, this time in terms of dietary composition of the animals. For this set of analyses the data was sorted into one of eight categories according to primary food source or sources. The groups included fruit, leaves, fruit plus, gum, insects, leaves, leaves and fruit, seeds, and omnivorous. The fruit plus group includes animals that get nearly equal parts of their nutrition from fruit and insects or fruit and gum. Animals in the leaves and fruit category have diets made that are equally frugivorous and folivorous. For all other animals, the group they’ve been assigned to makes up the majority of their diets. The omnivorous group includes animals whose diets are too varied to make any one other group designation appropriate. 22 Information on the dietary habits for each animal was researched and crossreferenced using several databases. The Primate Info Net Library and Research database at the University of Wisconsin (http://pin.primate.wisc.edu/) was the initial source consulted for diet information. Specific information was obtained from the individual fact sheets for each of the animals available on this website. In cases where information was missing, unclear, or there was no fact sheet available for a particular animal other databases were accessed. These included the Animal Diversity Web maintained by the University of Michigan Museum of Zoology (http://animaldiversity.ummz.umich.edu/site/index.html), and the IUCN Red List of Endangered Species (http://www.iucnredlist.org/). Information on these websites has been obtained from published research in a variety of reputable journals and compiled by experts in the field of primatology. The Animal Diversity Web page was the primary source of information for the dietary habits of the animals analyzed in this study. Mean EQ values of males and females were compared in the same manner as they had been when analyzing animals according to family and body size. P-values of less than .05 were considered significant. 3.3.1.4: Reproductive Strategy Because traits such as size and dietary preference have a strong influence on behaviour, and the connection between these three elements is not strictly unidirectional, one last set of analyses involving social behaviour was done. For this set of tests, animals were sorted into categories based on reproductive strategy. The categories broke down as follows: polygynous, polyandrous, monogamous, polygynandrous, varied, and unknown. With the exception of “varied” and “unknown”, all categories represent the species’ dominant mating strategy. The assigned category may not be the only tactic employed by the animals in question, nor is there absolute consensus in many cases that the animals do behave in a manner consistent with the category to which they’ve been assigned. 23 In cases where there were differences of opinion regarding the species’ typical behaviour, additional resources were consulted and the strategy that appeared most often in the literature was chosen. In cases where the research had not been done or the information was not available in any of the databases consulted, the species was assigned to the unknown category. Where there was no clearly dominant reproductive strategy employed, the species was assigned to the varied category. The information on reproductive strategy was obtained from the same databases utilized to obtain information on dietary composition. Once again, these included the University of Michigan Museum of Zoology’s Animal Diversity Web database, the University of Wisconsin’s Primate Info Net, and the IUCN Red list database. Once the statistical analyses were complete the results were compiled and put into table form. Those tables and a brief explication of what the results indicate are contained in the following section. A brief discussion of some of the key points, and potential areas where further investidation may be necessary to get a clearer picture of things, is also included. 24 CHAPTER 4 RESULTS 4.1: Introduction In the following sections results of pair-wise comparisons of male and female EQ values, according to the dimensions discussed in the previous section, are laid out in table form and briefly explored. Scatter plots showing the residual values for the models generated by the PGLS analysis are also included along with a phylogram that schematically represents the genetic relationship of the animals included in that analysis. Possible shortcomings of the analyses and an overview of the potential implications are presented at the end of this chapter. A more in depth discussion of both of these issues has been reserved for the following chapter. 4.2: Results of Pair-wise Comparisons of Male and Female EQ 4.2.1: Family Table 1. Pair-wise comparison of male and female primate brain mass, body mass, and EQ according to family. Mean Mean Mean Mean Male Female Brain Male Female Body Mean Mean Brain Brain Mass Body Body Mass Male Femal EQ Family Mass Mass P-value Mass Mass P-value EQ e EQ P-value 18.82 18.63 0.2889 1758 1825 0.0661 2.26 2.24 0.2710 Lemuriformes 10.97 10.16 0.0054 634 607 0.1596 1.82 1.71 0.0042* Loridae 7.36 6.91 0.0224 456 432 0.0103 1.34 1.29 0.0753 Galagonidae 3.70 3.49 0.0666 456 116 0.0103 0.95 0.92 0.1035 Tarsidae 20.22 19.81 0.1074 1078 1003 0.1795 2.86 2.87 0.4788 Pitheciidae 31.74 30.40 0.0011 1364 1079 0.0001 3.93 4.03 0.0007* Cebidae 87.68 84.36 0.0177 8012 6722 0.0011 7.07 7.08 0.4717 Atelidae 73.81 64.52 0.0000 5874 3716 0.0000 6.53 6.48 0.1524 Cercopithec. 111.70 101.07 0.0000 12452 7377 0.0000 8.08 8.35 0.0248* Papionini 76.35 69.22 0.0000 8150 6944 0.0003 6.18 5.82 0.0000* Colobinae 269.48 237.99 0.0002 45884 27651 0.0020 13.77 13.60 0.2681 Hominoidea *P-values of less than 0.05 were considered statistically significant. P-values obtained using a one-tailed t-test. 25 The first set of analyses involved the comparison of EQ values for male and female primates from eleven different families. For seven of the eleven, there were no significant differences observed between male and female animals with regard to divergence from the expected degree of encephalization, as indicated by the p-values that were generated by a one-tailed t-test comparing mean EQ values. There were, however, significant differences in the remaining four families. In the loridae and colobinae families males proved to have consistently higher EQ values than females when analyzed this way. The p-values for these two groups were ~0.0042 and ~0.000, respectively. In the case of the latter, the actual p-value (~0.000000008) was so small that it shows as zero when rounded to the fourth decimal place, as indicated in the table above. Comparisons of the cebidae and papionini families also demonstrated a significant difference in the EQ values of male and female animals in these species. In these cases the females proved to be the more encephalized animals, with respective Pvalues of 0.0007 and 0.0248. Because the animals sorted according to family represent closely related genetic clusters of animals, values for all males and females for whom phylogenetic information was available were statistically re-evaluated with phylogeny controlled for. The tree (Fig. 1) immediately below is a phylogram that was generated using the FigTree software in conjunction with the tree data provided by 10kTrees.com. It provides a schematic representation of the relationship of the 139 animal species that information was available for. This information was used in conjunction with the R statistics program to analyse the effect of phylogeny on shifts in encephalization. Using the PGLS command in R, plotting brain mass over body mass, the y-intercept of the model generated for males was 35.45 with an SE of 22.53 and a p-value of 0.1178. The body mass coefficient, or slope, was 0.0019 with an SE of 0.00017 and a p-value of less than 2-16. The y-intercept for the female model was 30.84 with an SE of 17.86 and a p-value of 0.0864. The slope for the female model was 0.0032 with an SE of 0.00022 with the same p-value of the male model, less than 2-16. 26 The results of those analyses indicate that phylogeny has played a role in perpetuating difference where in many cases where it exists. It is not clear, however, that phylogeny is the only factor influencing the differences in relative brain size seen between males and females across the entire primate order. In at least a few species, the divergence from the expected values is greater than phylogeny alone should allow for (see Fig. 2 and Fig. 3). These elevated values may be indicative of a grade shift occurring in certain clades or families, such as that seen in the results for the Great Apes in the hominoidea family. 27 Figure 1. Phylogram representing the genetic relationship of 139 primate species. 28 Figure 2. Scatterplot of residuals comparing male and female encephalization, controlled for phylogeny. Residuals - Encephalization and sex - Controlled for Phylogeny 350 Residuals for each species 300 250 200 Female residuals 150 Male residuals 100 Linear (Female residuals) 50 Linear (Male residuals) 0 0 20 40 60 80 100 120 140 160 -50 -100 Model generated slope - based on phylogenetically generalized least squares (PGLS) 29 Figure 3. Male and Female Residuals by Sex and Family 350 Male Cercopithecines 300 Female Cercopithecines Male Lemuriformes 250 Female Lemuriformes Male Atelidae 200 Female Atelidae Male Cebidae Female Cebidae 150 Male Loridae Female Loridae 100 Male Hominoidea Female Hominoidea 50 Male Pitheciidea Female Pitheciidea 0 0 -50 5 10 15 20 25 Male Papionini Female Papionini Male Colobinae Female Colobinae -100 Male Galagonidae & Tarsiidae Residuals generated by PGLS. Zero indicates no divergence from model predictioed values. Postive values indicate larger than expected relative brain size. Negative values indicate smaller than expected relative brain size. 30 4.2.2 Body Size Table 2. Pair-wise comparison of male and female EQ according to body size Mean Mean Male Female Mean Mean Body Size P-value Body Body Male EQ Female EQ Mass Mass 264 261 1.32 1.34 0.1698 0-500g 758 690 2.56 2.55 0.3854 501-1000g 1839 1697 3.60 3.59 0.4346 1001-2500g 4323 3180 6.46 6.45 0.3852 2501-5000g 6700 5709 6.79 6.56 0.0002* 5001-7500g 9760 7408 7.16 7.15 0.4205 7501-10000g 50630 28999 13.37 13.48 0.3602 >10000g *P-values of less than 0.05 were considered statistically significant. P-values were obtained using a one-tailed t-test. Consistent with Plavcan’s (2001) suggestion, overall dimorphism does increase with a general increase size. Neurological dimorphism as a stand-alone trait, on the other hand, does not appear to. When animals were divided according to size, only one category showed a significant difference in EQ values when male and female mean values were compared. Only in the 5001 to 7500g body weight class was a statistically significant difference observed, with a p-value of 0.0002. Here, males proved to be the more encephalized sex. 4.2.3 Dietary Composition Table 3. Pair-wise comparison of male and female EQ according to dietary composition Diet Fruit Fruit plus Gum Insects Leaves Leaves & Fruit Omnivorous Seeds Mean EQ Males Mean EQ Females 7.38 2.11 1.34 1.10 5.34 6.12 5.98 6.26 7.41 2.12 1.34 1.08 5.36 5.98 6.02 6.43 P-value 0.3681 0.4093 0.4849 0.3021 0.4487 0.1432 0.3035 0.1541 31 An analysis of encephalization against diet yielded results indicating no correlation between primary diet type and the degree of encephalization in the species analyzed. In no case were the p-values generated by one-tailed t-tests indicative of a correlation between brain size and primary food choice. The lowest p-values were found among species whose primary diet consists of equal parts leaves and fruit (0.1432), and those for whom the bulk of the diet is comprised of seeds (0.1541). In neither case are the values strongly indicative of a correlation between food choice and EQ, however. 4.2.4 Reproductive Strategy Table 4. P-values for pair-wise comparison of male and female EQ according to reproductive strategy Reproductive Strategy Polygynous Polyandrous Monogamous Polygynandrous Varied Unknown Mean EQ Males Mean EQ Females P-value 5.62 3.32 4.28 8.29 2.86 4.12 5.60 3.39 4.24 8.35 2.85 4.13 0.3571 0.0902 0.1385 0.2477 0.4105 0.4304 As with diet, the p-values generated by t-tests analyzing whether there might be a correlation between reproductive strategy and EQ, yielded nothing of any obvious significance. Here, however, one group did have a markedly lower p-value than the others. Species assigned to the polyandrous category appear to have a much higher proportion of females with higher EQs than males, though the p-value (0.0902) is not quite as low as is typically used to say anything definitive. The p-value for monogamous species was likewise worthy of further consideration at 0.1385, with males exhibiting greater encephalization in that case. 32 4.3: Discussion of results Before providing a more thorough treatment of the results in the next section, there are a couple of matters that warrant mentioning with regard to the data. The first thing that ought be borne in mind with regard to the results for the pair-wise comparisons in which diet and reproductive strategies were the dimensions along which relative brain size was assessed is the lack of clear, accurate information available for many of the species included in this data set. Many of the animals have only been studied in laboratories and zoos, where handlers proscribe diets, and reproductive strategies may depart radically from what is typical in the wild. Additionally, even in cases where the animals were studied in their native habitats, the amount of information obtained regarding these behaviours is often quite limited and does not always reflect the animal’s usual diet preferences or give the researchers a clear picture of precisely what sort of reproductive strategy is common to the species under observation. A second issue that bears consideration is the role of phylogeny. The results here tell us that once we take taxon-level influences are taken into consideration the picture that emerges is somewhat different, with females falling below males in the degree to which they’ve become encephalized. This may appear to conflict with the result of the initial pair-wise comparisons. It does not. What these results may indicate is that in species where one sex is more encephalized, the trend is the result of canalization rather than selection pressures. The trend toward encephalization may have occurred at some earlier evolutionary break. It does not mean that not that the animals in question do have larger relative brains sizes. 33 CHAPTER 5 DISCUSSION 5.1: Introduction In this section, some of the potential implications of the results described above will be explored, and a more thorough treatment of some of the more interesting findings will be provided. In addition to the models described in the literature review section of this paper, the results will also be examined in light and the models articulated by Wrangham (1986) and van Schaik (1989). The following sections are divided according to the individual variables analyzed. An additional section discussing the influence of the different variables on one another is also included toward the end of this chapter. The final paragraphs of this section examine the way the results of this study support, or refute, three of the major hypotheses explaining how encephalization in primates has occurred. These are the Social Brain hypothesis (Dunbar 1998), the maternal energy hypothesis (Martin 1996), and a third hypothesis that explains differences in encephalization as having resulted from differences in basal metabolic rates (McNab 1986a, McNab 1986b, Martin 1996). 5.2: Discussion 5.2.1 Results by Family With regard to the first and most general inquiry of this study, the question of whether one sex or the other has evolved greater relative brain size, the results were quite mixed. When pair-wise comparisons of the mean values for males and females of individual species were done using the raw data and the EQ slope recommended by Williams (2001), the results indicated that in one of the New World monkey families, the atelidae, females had a higher EQ values. The pair-wise comparisons also indicate that, when looking at the entire family, EQ values for female papionini were significantly higher than those for males of that family. In direct contrast to 34 this, prosimian males of the loridae family possess larger relative brain sizes and so do Old World monkey males in the colobinae family. Once phylogeny was controlled for and the species were reanalysed, a different picture emerged. The number of species included in the second set of analyses was far smaller at 139 than the original group of 212, but still large enough to get a reasonably clear picture of what may be happening across the order. The scatterplot of the residuals included above (Fig. 2) shows that the values for males appear to diverge more radically from the mean predicted values than those of the females. In almost every species, males show a wider range of values than females once phylogeny is controlled for. In species that fall above the slope, and are more encephalized than would be predicted, the males are nearly always more encephalized than them females. When the values fall below the mean, females are more encephalized and the negative values for males of the same species are larger. In all cases, female residual values tend to align much more closely with what would be expected for the species in question, based on its genetic distance from other species in the order. The values for individual species also tend to cluster very tightly according to family regard less of sex. Very few species exhibit values that sit a significant distance away from those of their closest relatives. When one species in a family sits close to the line so do the majority of the other species in that family. When there is greater divergence than expected for an individual species, closely related species of the same family tend to show the same trend. For example, the cebidae values all appear to cluster fairly tightly around the slope, regardless of the size of the individual species, while all the papionini tend to sit well above it. The clear exception is found in the hominoidea. In the hominoids, the great apes (Pan, Gorilla, and Pongo) show a massive departure from the expect values, with values falling well above what would be seen within one standard deviation, while the values for the gibbons (Hylobates) sit almost immediately on the line, falling precisely where they are predicted to. 35 Looking at the aims of this study, the differences in the values before and after phylogeny was controlled for seem to indicate that there may be different pressures operating on each sex in a number of species. The EQ values for females, once phylogeny is controlled for, cluster very tightly around the predicted mean values, indicating that, whatever the trend within any given species with regard to encephalization, the trait is less plastic in females. More importantly, in families where females are more encephalized, this trait doesn’t appear to have been selected for during the period in which the primate order has evolved. In other words, greater encephalization in females appears to be a canalized trait, which evolved prior to the evolutionary break where the primate order began, in the families where it is present. Individual species may exhibit a departure from this trend, but in nearly all cases where this is so, it is because the species as a whole has rather than just females. Even when females are more encephalized than would be expected (as in the case of the Great Apes), males are as well, indicating that the trait is probably evolving as a result of more general natural selection pressures acting on the entire species, rather than on females, or that females have become more encephalized because males have (Clutton-Brock et. al. 1977; Leutenegger and Cheverud 1982; Kappeler 1999). Male values, by contrast, do not exhibit any clear or obvious trend with regard to the degree of encephalization seen from one family to the next. In certain species there is a great deal of divergence, while in others the residual values are quite consistent with what would be expected. Looking at the second scatter plot (Fig. 3), however, it does appear that there are a number of tightly associated clusters of values in closely related species, many of which share similarly complex social structures with fairly heavy burdens on males in terms of sexual competition. Several species in the hominoidea, papionini, and atelidae families which are known to have complex social structures (Smuts 1985; Mittermeier and van Roosmalen 1981; van Roosmalen 1985), as well as high levels of sexual competition among males, also show high levels of encephalization among males, with residuals falling well above the predicted values. In species where competition is lower among males and social structures are more fluid, such as the callitrichidae (Porter and Christen 36 2002), the male EQ values are much lower with many species falling well below what would be expected based on the slope generated by the phylogenetic general least squares analysis. These results are consistent with findings of Schillaci (2006, p. e62) in which “an analysis of variance (ANOVA) derived from multiple regression models with mass dimorphism and male body mass as independent variables, and brain size and testis size as dependent variables, indicated that the level of male competition for mates had a significant association with brain size but not with testis size.” They also lend support to the social brain hypothesis (Dunbar 1998), which is discussed further in the section dealing with reproductive strategy below. 5.2.2 Results and Body Size When tested using a Pearson’s correlation one-tailed t-test, body size and EQ showed no evidence of being linked in any size class but one. Males and females of species in the 5001-7500g bodyweight classes do appear to manifest EQ values that differ significantly. In this group, the average EQ for males was 6.79 and 6.56 for females, with a p-value of 0.0002. Interestingly, there are a very high number of smaller hominoidea in this size class (see original Isler et. al. 2008 data set for individual species mean values, at doi:10.1016/j.jhevol.2008.08.004.) . Compared with the group of animals in which phylogeny was controlled for, the results of the analyses in the initial comparison done using only values provided by the raw data and Williams’ recommended slope seem far less interesting or indicative of anything. Once phylogeny is controlled for, the results indicate that body size does in fact correlate with the degree to which a species diverges from the expected level of encephalization. The largest animals exhibit the highest levels of encephalization and the values are well above what is predicted by the model for animals with their respective mean body mass values. In other words, the big animals possess brains even bigger than what would be expected for a big animal. Brain volume has not evolved in an isometric fashion in the larger primates. The presence of the hominoidea as extreme outliers, well outside the first SD, on the scatter plot above offer the clearest evidence of this trend. It tells us that the ratio of brain mass to body mass in the hominoidea is far higher than would be seen if these 37 structures had evolved in an isometric fashion. Of additional interest is the fact that once again we see evidence of higher levels of divergence from expected values for males than we do for females. Once again, female values are clustered much more tightly around the slope for their sex than males are for theirs. When the EQ values for an entire species are higher than expected, male values are almost always higher than those of females, and the largest gaps are seen among the largest animals, indicating that there is in fact a relationship between overall body size and EQ. The results of the analyses involving body size comport quite nicely with Plavcan’s (2001) assertions regarding this matter, as discussed in the literature review section of this paper. Dimorphism in body size does indeed seem to lead to greater dimorphism overall. Particular structures, in this case brain, do increase in size in an exponential, rather than linear, fashion and the amount that a structure may change as the species in question becomes larger may differ between the sexes. The mechanism or mechanisms that may account for the difference are not obvious when simply looking at the differences themselves but it seems reasonable to assume that reproductive demands and resource availability may play a role and, therefore, this issue will be revisited in the discussion of the results of both the analyses involving diet and reproductive strategy. 5.2.3 Results and Diet Among the least interesting results of this study were those generated by the pairwise comparisons of the raw data for males and females looking at a possible correlation between sex, EQ, and primary food source. The problem with this set of analyses was not, however, the lack of potentially interesting things that might be said about the relationship between EQ, diet and sex, but the difficulty of obtaining clear, accurate information about actual diet preferences from species to species. With several of the species in this study, the necessary information was not available, extremely limited, or the reports from one study to the next on the same species were conflicting. As such, a “best guess”, which involved choosing the position with the greatest consensus in the available literature, was often the category to which a species was ultimately assigned. These “best guesses” resulted in the creation of 38 categories that are, admittedly, too broad to be particularly useful in careful analysis of the relationship between diet and brain development. They also may be incorrect. Nevertheless, the influence of nutrition and resource availability are matters important enough to warrant some discussion, and therefore the balance of this section will be devoted an exploration of these issues in light of the other variables analyzed. Assuming Amen-Ra’s (2007) neurotrophic neotonization theory is correct, it is likely that this particular dimension, diet, has been pivotal in shaping neurologically dimorphic traits. Looking at the results above, however, it does not appear that composition plays as big a role as fluctuations in the availability of food do. The results of the analyses looking at composition don’t tell us nearly as much as what the scatterplots (Fig. 2 and Fig. 3) of the residual values of the models for male and female EQ do. Looking at the scatter plot we can see that the species with the greatest levels of positive divergence are found in the Old World monkeys (papionini) and the Great Apes (hominoidea). We know from research done involving our own evolution (Amen-Ra 2006) that resource availability on the African continent, where these species have evolved, has greatly fluctuated over the past several million years with famine conditions arising several times. On the other hand, the species that have evolved under less precarious conditions show much lower levels of encephalization with female EQ values sometimes surpassing those found in males and several species falling well below the slope generated by the models for both sexes. The diets of the animals on both continents vary greatly, but consistent availability of food has been much more erratic for the Old World species (Amen-Ra 2007) than it has been for New World monkeys. As noted in both of the earlier discussions of family and body size, EQ values for female primates tend to align much more closely with what the models based on phylogeny predict than those of males, indicating that selection pressures may be different for males and females. One way of interpreting that difference is in terms of the consequences that resource distribution has on each sex. Females, as stated in the introduction have more at stake when resource availability is compromised. A 39 female mammal must be able to meet her own nutritional demands as well as those of her offspring. The female animal, simply by virtue of these demands, has fewer resources available for use in the development of her own body. Males, in nearly all primate species, have far more leeway in terms of the extent to which they can diverge from the expected mean body or brain size and still survive because the cost in the development of these traits is always, relatively, lower. A female whose size exceeds what the resources in the environment can support will not only starve herself, but her offspring as well. A male faced with the same conditions will still be able to successfully reproduce, often many times over, before he starves to death. The potential for female body and brain growth is much more narrowly restricted by resource availability than it is for males. Hypotheses offered by van Schaik (1989) and Wrangham (1986) explain the dispersion of females in any given environment as mapping on to the resources, or food, available in that environment. The differences in the residual values seen above are consistent with these hypotheses, offering further support to the suggestion that females are more vulnerable to the effects of fluctuations in resource availability than to fluctuations in the availability of mating partners. We would expect a narrower range of values for both brain and body size in females, with females being both smaller and, by extension, less encephalized than males in regions where resource availability is more limited. The results of this study are consistent with this position. The fact that males are not only absolutely more encephalized, but relatively as well, is slightly more puzzling. It seems that if famine conditions are what drive increasing encephalization, then the sex more susceptible to the effects of famine would end up developing a relatively larger brain. We can see from the residuals that this has not been the case. Females are nearly always less relatively encephalized when species values fall above what is predicted by the model. Only in species that fall below or immediately along the model’s predicted values do females end up being more encephalized than males and, here again, this seems to have more to do with female values being more closely aligned with the predictions, rather than females actually 40 having evolved a larger brain. Here then it seems we may have a result that goes against what we would expect according to the N3 hypothesis. On the other hand, if there is an added selection pressure driving male encephalization that females do not have to contend with, the neurotrophic neotonization theory may still give us an accurate account of how certain primates, throughout the entire order, have evolved such extreme relative brain sizes. This possibility will be discussed further in the following section. 5.2.4 Results by Reproductive Strategy A review of the results of the pair-wise analyses examining the relationship between reproductive strategy, EQ, and sex indicates that the greater relative encephalization seen in so many of the Old World primate species, and males in particular, may be the result of sexual selection among males. Famine conditions may have set the trend in motion, but it appears that sexual selection has taken over from there. Males in all the hominoid species as well as a number of those in the Old World monkey families are more encephalized than the females. In nearly all of the species in question high levels of competition exist among males. The EQ values for Old World primates contrast quite starkly with what we see in the New World monkeys. While there certainly are a number of New World species that do sit above the slope generated by the model, many more fall below, with males generally falling below females when they do. The pair-wise comparisons of males and females according to reproductive strategy are in line with what the scatterplots (Fig. 2 and Fig. 3) illustrate. The most statistically significant difference seen between males and females, when sorted according to reproductive strategy, was in group containing polyandrous species (the cebidae) where the results indicated that females were relatively more encephalized. Though the p-value wasn’t quite low enough to say anything definitive, at 0.0902 it is unlikely that the difference in this group was solely due to chance. Females in polyandrous species are often relatively more encephalized than their male counterparts. The burden on males in these species, in terms of intraspecies competition, is also known to be quite low. 41 It appears then that the level of intraspecies competition, or sexual selection, largely influences the extent to which males become more encephalized. In females, encephalization is primarily determined by interspecies competition, or natural selection more broadly. Any given species will evolve according to what environmental constraints exist within its respective niche, but within primates, it is in the sex that is less susceptible to fluctuations in resource availability that we see more variability in the degree to which it becomes encephalized (Barton 1999; Barton 2006). In this case, it is the males. Once again, looking at the scatterplots (Fig. 2 and Fig. 3), this trend is quite apparent in both directions. Males in the polyandrous and many polygynandrous species, where male-male competition is either extremely low or non-existent, have the lowest EQ values of all the species analyzed. Social structures among species engaging in these types of reproductive strategies put far less of a burden on males than those in which mate securing is an issue. That Schillaci (2006) found a high degree of encephalization in monogamous species unexpected and somewhat puzzling, but his findings are not inconsistent with the results of this study. Even in monogamous species the social demands on males are generally greater than they are for their female counterparts, as males are generally the chosen, rather than the choosing, sex. If Dunbar’s (1998) social brain hypothesis is correct we should expect monogamous males, as well as polygynous, to have higher EQ values than males of species with more flexible reproductive strategies, as males in species with both of these reproductive strategies face a far heavier burden in securing a mate, or mates, than their polyandrous or polygynandrous cousins. The burden for males in monogamous species is certainly less than that of polygynous, but the business of procuring a partner is, nevertheless, far more taxing for males than it is for females in species where females are less particular about their mate choices. Whether there exists a genuine correlation between reproductive strategy and the degree to which a species is encephalized is something that has not been made entirely clear with this study, but it does appear that these two traits are in some way linked. The relationship between them may be only correlative, rather than causal, 42 with some an additional element linking the two. One reasonable candidate is, as mentioned previously, a certain kind of precariousness in the environmental conditions. Based on the research on encephalization discussed above, it would appear that certain environmental conditions would need to be present in order for the trend toward greater encephalization to even begin. A shortfall in available resources initiates the biochemical processes that lead to greater encephalization (Wang et. al. 2006). Those animals that do not possess the physiological means to endure famine conditions end up dying, leaving behind a generation of more encephalized, or at least more encephalizable, animals. Whatever genetic component it is that has allowed the survivors to survive is then passed on to the next generation and the process of species-wide encephalization is set in motion. If this trait confers some benefit on that species in question it will persist or evolve further over time as a result of natural selection. Once a trait appears in a population, the original selection pressures that originally drove its development need not be the ones that perpetuate further development of that trait. In this case, it appears that environmental fluctuations manifesting as repeated bouts of famine over several million years, triggered the process of encephalization in primates. Once the order was on that trajectory, complex social systems became possible and this trait was further influenced by sexual selection. Both the negative and the positive results in this study support this position. 5.2.5 Synthesis Because several variables were explored in this study, this section of the discussion will be devoted to pulling them all together in order to look at how the interplay of each of these elements may have affected the results. A clearly articulated conclusion has been reserved for the sixth and final chapter. Arguably, the most tightly connected variables in this study are those of diet and reproductive strategy. Both van Schaik (1989) and Wrangham (1986) have explored the connection between these two variables and the general consensus is that diet 43 plays a key role in determining reproductive strategy, which in turn shapes social structure. Here, again, it is argued that the most influential aspect of diet is the way the food is distributed in the environment, rather than nutrient content. Actual dietary composition is not wholly irrelevant though, despite what the results of this study appear to indicate, as the food type and food distribution patterns go hand in hand. Fruit, for example, is a seasonal, geographically limited resource that may monopolized be far more easily by a single dominant female than say something like leaves or insects. Fruit is also a great deal more difficult to procure on a regular basis. This means that frugivorous species are more susceptible to environmental fluctuations and are also more geographically limited as a result of their diet. Assuming the models offered up by Wrangham and van Schaik are correct and males do map onto females and females map on to food sources, the opportunity for males to monopolize females is more likely to arise in species that are predominantly frugivorous. Once it becomes possible for males to monopolize females, high levels of competition between males will arise, and social behaviours will become increasingly more complex. Considering this line of thought with regard to this particular study, we see that a number of the more encephalized animals are known to be both polygynous and frugivorous (such as the large hominoidea, and a number of species in the atelidae and papionini families) at while the group of animals with the lowest EQs includes the polyandrous omnivores (found among the cebidae). The pair-wise comparisons analyzing the data in terms of dietary composition do not provide this information, but a careful examination of the original data in conjunction with the scatterplot of residuals does. Looking at diet in conjunction with reproductive strategy gives us far more insight into the relationship between EQ and sex, than analyses of either variable on its own can. Two other variables that appear to be strongly connected are those of body size and reproductive strategy. The largest males in this study turned out to be the animals with the highest EQs. High levels of relative encephalization were also associated with high levels of body dimorphism, though the most dimorphic species were not those with the highest EQs. We have already seen how dimorphism can arise 44 without sexual selection (Clutton-Brock et. al. 1977), simply as a result of downward pressure on one sex, but the extreme dimorphism seen in the animals with the largest gaps in size between males and females appears to be tied to sexual selection. In both the papionini and hominoidea, families in which the highest levels of body dimorphism are found, a large number of the species are polygynous and males are far more encephalized than females. These are also the largest primates in the order, of both sexes, and there are no known polyandrous species in either family. Even Pan paniscus, with its apparently matriarchal social structure, does not employ a polyandrous reproductive strategy (White 1988; White 1996). The dominant strategies among the large-bodied primates analyzed in this study are polygyny and polygynandry, with half of the great ape species employing the former strategy and half employing the latter. Though polygynandry is a common reproductive strategy in the smaller monkeys in both New and Old world species, the strategy employed among the Great Apes is not the sort of free for all mating that is found in the smaller monkeys, but a far more competitive an combative affair wherein males are competing against one another almost as fiercely as they are in polygynous populations (Smuts 1985: Nishida et al. 2003; White 1988; White 1996). There are numerous species outside of the papionini and hominoidea that may also be characterized as polygynous or complexly polygynandrous, but there are no truly large-bodied polyandrous species. Additionally, even in the smaller polygynous animals, males are far larger and more encephalized. Body size, reproductive strategy, and encephalization appear to be closely linked, if not co-evolving in the strictest sense. The sections immediately above have discussed the relationship between pairs of variables that appear to be especially strongly linked, but these dyads far from exhaust the list of ways that each dimension may influence, or be influenced by, the others. Body size, diet, and reproductive strategy all shape one another, and this in turns influences the way a species, and even a family, evolves over time. A large number of the smallest of the animals in this study have evolved in geographic regions where the resources are more abundant, or were in the past, on the South 45 American continent. In these species, female encephalization quotients are nearly identical to those seen in males, with a few actually being higher (again, however, this is only because the entire species falls below the predicted values). These are also the only known truly polyandrous species. This may seem somewhat counterintuitive as it would seem that more resources would result in larger animals, but a review of the basic tenets of natural selection reveals why larger, more encephalized animals would evolve in regions where resources are less readily available. First, there is the most fundamental kind of natural selection pressure, that of interspecies competition. As long as there are adequate resources, the larger animals may dominate. Even when resources are diminished, if there is enough food available to circumvent the problem of total starvation, smaller and weaker animals will lose out in the fight for survival. It should be noted here that being weaker isn’t necessarily a matter of being less physically strong or robust, it may also be that one species lacks the cognitive capacity to deal with shifts in the environment with the same facility that its neighbours do. In environments, such as those where we find the small, polyandrous monkeys, this kind of pressure is greatly relaxed. Food is relatively plentiful and, though seasonal in many cases, consistent in its availability. If enough food is available for everyone, competition is low. No one species gains an advantage by being significantly larger, stronger, or “smarter” in environments where resources are adequate to support the entire population. Second, in resource deprived environments there is also the added burden of intraspecies competition creating an additional selection pressure. Intraspecies, or sexual, selection is markedly more pronounced in populations where food availability has fluctuated greatly over the period in which the species has evolved. Animals in these species are competing with other species for environmental resources as well as with other members of their own species for mating opportunities. The primary selection pressure, environmental conditions, determines the developmental trajectory for the entire species and the secondary pressure of 46 competition for mating opportunities results in the development of highly dimorphic traits within the species. Animals of both sexes need some sort of advantage to outcompete other animals in the environment, but the sex with the added burden of being the “chosen” one (rather than the more passive chooser) has to have an added edge relative to other members of his species. Looking at these considerations, we can now see how and why residuals values for male Hominoidea are so far above those for all of the other animals in this study. Diet, or more precisely, a lack of continuity in resource availability, seems to have driven the increase in overall species size. Those animals that were the largest and best able to navigate their environments were then able to outcompete other members of their own species in securing reproductive opportunities. Recognizing this, we can see that all four of the variables examined in this study have played a role in the development of these large-bodied, highly encephalized species. The same can be said of all the other animals studied. The degree to which any one dimension affects or is affected by the others may vary from species to species, but in every case every variable plays a role with regard to all of the others. It is never the case that any one dimension is the definitive variable when it comes to determining the extent to which a species becomes encephalized. The entire suite of variables must be taken into consideration when evaluating differences in encephalization from species to species, as well as between sexes. 5.2.6. Consideration of the results in light of a few major hypotheses Ultimately, what the results of this study seem to offer is further support for the social brain hypothesis (Dunbar 1998). According to this hypothesis, the large brains characteristic of primates in general have evolved as a result of the complex social systems found throughout the order. This is consistent with the results of this study. Ecological conditions may have been what initially sparked the trend toward greater encephalization, and why there exists such a huge range of EQ values from species to species, but the extent to which the trait has evolved from one species to the next 47 appears to be tied to the complexity of a species’ social structure. Reproductive strategy and diet have been the proxy for social structure in this study, as clear, detailed information on social structure is quite limited. When taken in conjunction with one another, information on diet and reproductive strategy do offer an adequate approximation of social complexity, as these two variables determine the kind of social structure that evolves. Animals faced with greatest burdens in terms of both resource availability and mating opportunities show the highest EQ values. These are also the species with the most complex and competitive social structures, and even more importantly, the species in which the social burdens are on males are highest. The more egalitarian species, and those in which males are not competing, turned out to be the least encephalized. This is consistent with what we would expect and as the social structures in polyandrous, omnivorous species are generally speaking the least socially complex, while frugivorous, polygynous ones are the most for reasons outlined by Wrangham (1986) and van Schaik (1989). That is not to say that the social structures of polyandrous species are altogether lacking in complexity. When it comes to primate behaviour, it is a matter of degree with one category of animals sitting at one end of the continuum and the other sitting at the opposite end. All species engage in socially complex behaviour to some extent, as primates are, on the whole, socially complex creatures. Sociality is a hallmark of the primate order (Shultz and Dunbar 2010). A final issue worth considering is the way in which the results of this study line up with a couple of other important hypotheses regarding encephalization. The first of these is what has been termed the maternal energy hypothesis (Martin 1996). The second isn’t a formal hypothesis, but a suggestion in the relevant literature that explains differences in encephalization in terms of differences in basal metabolic rates (McNab 1987a, McNab 1987b, Weisbecker and Goswami 2010). I will briefly consider each of these in turn, once again focusing on how the results here either support, or offer counterexamples to, each hypothesis. According to the maternal energy hypothesis the process of encephalization occurs 48 primarily as a result of the influence of maternal basal metabolic rate, along with maternal body size and gestation length (Martin 1996). The latter two variables, however, play ancillary roles, while maternal basal metabolic rate is the primary factor influencing brain growth. The idea here is that the mother’s energy turnover rate determines how encephalized her offspring becomes. More specifically, “the maternal energy hypothesis proposes that all mammals have the largest brains that are compatible with the metabolic resources available to their mothers during gestation and lactation” (Martin 1996 p. 155). Looking at the results of this study, it seems this hypothesis may hold up when considered in regard to species or families, but it’s not entirely clear that it does when we examine the differences in encephalization between males in females of the same species. If maternal basal metabolic rates determine her offspring’s potential encephalization, it’s not readily obvious to this author how males and females come to have such different EQs in so many species. Of course it may be that one of the two other variables, gestation length or body size, may have a greater impact than has been suggested by the hypothesis, and the differences may be accounted for in that way. It may also be the case that maternal basal rates vary according to the sex of the offspring she’s carrying. Without further information regarding either of these possibilities, however, it’s difficult to see how the maternal energy hypothesis can provide us with an explanation of how encephalization occurs in light of the results of this study. A second line of thought that warrants consideration also explains encephalization in terms of basal metabolic rates, but the focus is on the encephalized animal, rather than its mother. In this case, there doesn’t appear to be a firmly articulated hypothesis so much as a number of suggestions in the literature on this subject (McNab 1987a, McNab 1987b, Martin 1996, McNab and Eisenberg 1989, Weisbecker and Goswami 2010). The suggestion is that an animal’s own BMR, influences the extent of its encephalization. What the relationship between BMR and brain development is exactly, a positive or negative correlation with a rapid BMR, isn’t clear, but assuming that a higher BMR correlates with greater encephalization, we may have a potential explanation for the differences between males and females seen in this study. Here again, confounding variables such as body size and gestation 49 length, may need to be explored further before anything more is said on the matter, but unlike the previous hypothesis, there do not appear to be any obvious counterexamples to this suggestion in the results of this study. Having covered the results and some of possible implications that follow from them, the following chapter will be devoted to a more precise articulation of answers to the four questions introduced in the aims section of this paper. 50 CHAPTER 6 CONCLUSIONS 6.1: Conclusions In this section explicit answers to the questions presented in the aims section of this paper will be provided. Those questions were as follows: Across the primate order, does one or the other sex exhibit a trend toward greater encephalization? In families where one or the other sex is more encephalized, is this trait the result of canalization or is it derived? What is the relationship between overall body size, encephalization, and sex? Is there a correlation between relative brain size and diet, body size, or reproductive strategy? 6.1.1. Is one sex more encephalized than the other? On the whole, male primates turn out to be more encephalized than female primates, though the difference is only apparent once phylogeny is controlled for and species are taken on a case-by-case basis. When the raw data is evaluated, without controlling for phylogeny, and examined at the family taxon level rather than the species, the results are somewhat misleading. Looking at the data in this way, females appear to be more encephalized than males in two families, while males are more encephalized in two others, and the remaining families show no difference at all between the sexes. These results do not accurately reflect what the general trend in primates actually is. The results of the PGLS analysis provide a far more accurate picture. The models generated by this analysis show us that in species where females appeared to be more encephalized, the greater encephalization is simply the result of females diverging 51 less from the values the model predicts than males. In these cases, however, both sexes are still below the expected values for their sex and species. Even more importantly, in many families where there appeared to be no difference in EQ in the initial pair-wise analyses, several species were found to have males that were in fact significantly more encephalized than their female counterparts. This was especially evident in the hominoidea where the p-values generated by the initial t-test indicated that there was no difference between male and female EQs. Even a cursory glance of the scatterplot displaying the residuals shows a very high number of male hominoids to be significantly more encephalized than not only the females of their respective species, but all the other animals of both sexes as well. 6.1.2. Is encephalization the result of canalization or is it a derived trait? Looking at the results of the PGLS analysis, it appears that the extreme encephalization we see in primates is trait that is present in the order as result of canalization. With the exception of a few species, the majority of the animals analyzed in this study fall very close to the slope generated by the model. Very few diverge significantly from the predicted values. Only the hominoidea sit more than one standard deviation from values predicted by the model. What is particularly interesting about these results is that encephalization does not appear to have evolved, or be evolving, in the same way for both sexes. Looking at the scatterplots (Fig. 2 and Fig. 3), one thing that is apparent is that the values for females align much more closely with the predictions than the male values do. On the basis of this information it may be argued that encephalization in females is primarily the result of canalization. The results for males seem to tell a slightly different story. The males in at least two families, the hominoidea and papionini, appear to have become more encephalized as a result of selection pressures. There are a couple of exceptions where females are far more encephalized than the model predicts, but these females are all found in the hominoidea, where their male counterparts are even further above the predicted values, so it may be the case that females are simply becoming more encephalized because males are. The fact that males always diverge more than females in either direction would appear to indicate 52 that selection is working primarily on males, and only secondarily on females, if at all. Therefore, it seems that encephalization in males may be a derived trait that has resulted from sexual selection pressures, as discussed in earlier sections, while encephalization in females represents a species baseline that is largely the result of canalization. In short, competition with other males is driving an increase in brain size among males, while female brain size remains consistent with what would be expected if the trait were simply being passed on from one generation, or one species, to the next. 6.1.3. Is there a relationship between body size, encephalization and sex? When looking at differences between males and females, results of the pair-wise analyses done comparing EQ and body weight indicate that the relationship between body size and relative brain size is a loose one, at best. Only in the 5,001-7,500 g weight class was there a significant difference in the EQ values, with males being relatively more encephalized than females. This finding was somewhat unexpected, as it seems to contradict the position articulated by Plavcan regarding the relationship between the overall level of dimorphism in a species and its body size. It was anticipated that the larger animals (those in the 7,501 -10,00 g and <10,000 g categories) would exhibit a similar pattern, but they did not. Only males and females in that one category demonstrated a statistically significant difference. Looking at just body weight and EQ (again using Williams’ recommended slope), there were no significant differences among species in any other weight class. The more detailed information provided on the scatterplots (Fig. 2 and Fig. 3) further supports this finding. The largest and most dimorphic animals are not the species in which we see the highest levels of encephalization. The species with the highest rates of encephalization are indeed found in the family with the largest animals, the hominoidea, but it they are not the largest species in that family. According to the results, it is within the chimpanzee species (Pan troglodytes vellerosus, Pan troglodytes verus, and Pan troglodytes schweinfurthii) that we see the largest relative brain sizes. Males in the orangutan species (Pongo abelii and Pongo pygmaeus) follow closely behind these three along with the fourth chimpanzee subspecies (Pan 53 troglodytes troglodytes), while the males in the two gorilla species (Gorilla gorilla gorilla and Gorilla gorilla beringei) included in this study have EQ values that fall below not only all the other male Great Apes, but below the females in that clade as well. This is not what we should see in the results if high levels of overall dimorphism correlate with even higher levels of encephalization. The largest and most dimorphic male animals are not the most encephalized, despite the fact that they are the largest animals. Before discounting the idea that larger bodies result in even larger relative brain sizes altogether however, it should be noted that female EQ values do actually increase with increases in body size. It may be the case then that whatever the baseline for brain size is, within any given species, it is determined by the female values for that species and the differences we see in males are, once again, driven by sexual selection pressures. Body size and relative brain size would still be linked, with sexual selection accounting for the differences we see in just the values for males. This takes us back to one of the original considerations raised in the introduction of this paper, that of limitations on female growth. The possibility that reproductive demands constrain the development of larger female bodies was put forth as a reason for the apparent differences in male and female body and brain sizes. Looking again at the differences manifested in the residuals, and how tightly the female values cluster around the slope the model generated, it may be argued that this explanation should remain a viable hypothesis. It is clear that some pressure is constraining variation among females and a review of the results of the other analyses indicates that, whatever that constraint is, it is likely tied to reproduction in some fashion. 6.1.4. Correlation between encephalization and other variables analyzed As with the pair-wise comparisons involving just the raw data for body size and family, the results of the analyses exploring the relationship between EQ and diet and EQ and reproductive strategy did not appear to indicate any real differences between males and females. The only differences seen in either of these analyses were in the values for males and females in polyandrous and monogamous species. The p-values were a bit too high to be absolutely certain that the differences could not be due to 54 chance, but as discussed previously, they were low enough at 0.0902 and 0.1385 to warrant further investigation. An examination of the scatterplot showing the species sorted according to family (fig. 3) revealed that all of the animals in the polygynous group were found within the New World monkey clades, with no primarily frugivorous species among them. A fairly high proportion of the monogamous species were also found among the New World monkeys, with those that weren’t being found primarily among the prosimians (lemuriformes and galagonidae). Diet among the monogamous species is, however, more varied. What the net effect of this difference is is difficult to ascertain as the information on actual diet preferences is not known with the sort of precision that would be necessary to determine how much of an effect it may have on the other variables examined. Nevertheless, as has been discussed previously, there does appear to be a link between the availability of resources, whatever they may be, the reproductive strategy typically employed by a species, and the degree of encephalization of that species. It seems reasonably safe to assume that the amount, and consistent availability, of resources available to omnivorous animals would be greater than those for animals with more limited dietary breadth simply by virtue of the fact that the loss of one or two preferred foods will not have the same consequences for a less discriminating animal as it does for one that is highly selective. More options should translate into less competition, as the total exploitation of one resource does not result in the depletion of all possible food sources. An omnivorous animal will simply move on to the next available resource. If competition for resources in the environment is generally low, because food is readily available to all animals, intraspecies competition is likely to remain low as well. That is not to say that competition is entirely absent in resource rich environments, rather that it is likely to be much higher in resource deprived ones. As discussed previously, once interspecies competition increases, either because all available resources have been depleted or the resource a particular species relies on is no longer available, it is likely intraspecies competition will increase as well. Once this type of selection pressure is present in a population, it is unlikely to be reversed, 55 even if more resources become available. Once a hierarchical social structure has been established, it is likely to remain as the condition that facilitates it, differences in fitness between animals within the species, will also have been established. The conditions that allow certain animals within a population to thrive and reproduce, whether they are somatic or cognitive in nature, will continue to put those animals and their offspring in an advantageous position within their group and so will be perpetuated from one generation to the next. Bearing this in mind, it seems that the likelihood of a link between diet, reproductive strategy, and encephalization is quite strong. The precision of this study, however, was not adequate to ascertain the strength of the relationship between these variables. The fact that it was not is an issue that will be addressed in the following, and final, section of this paper. 6.2: Recommendations As indicated in the final lines of the previous section, the precision of this study was not at the level it needed to be to make any definite claims regarding the influence of the individual variables examined on one another. The significance of this matter was not readily apparent at the outset of this study, but an examination of the results of the pair-wise comparisons in conjunction with the phylogenetically controlled analysis has made it clear that the variables are, in fact, connected in various ways. On this basis, it is recommended that future research on this topic be undertaken with a proper weighting of the variables involved so the strength of the relationships between them be more clearly understood. Multivariate analyses would help to clarify the trends observed in this study and provide a better sense of how significant a role each variable plays in determining the extent of encephalization in a given species. A second, much broader and more general, recommendation would be a reconsideration the significance of encephalization. This study has shown that male primates are indeed more relatively encephalized than female primates, but what, if any, benefit that has conferred on them is still unclear. Encephalization quotients do 56 seem to be tied to all of the different variables looked at in this study, but without a more precise and detailed assessment of the composition of the brains themselves, rather than just their size, it seems unlikely that establishing a clear connection between the variables and the brain size will be possible. This sort of work has already been undertaken with humans and other apes, so a third, less general, recommendation would be to continue to expand these studies, looking at how brain architecture has evolved across the order. 57 REFERENCES Journals: Amen-Ra, N. (2006) Humans are evolutionarily adapted to caloric restriction resulting from ecologically dictated dietary deprivation imposed during the Plio– Pleistocene period. Medical Hypotheses, 66: 978-984. Amen-Ra, N. (2007) How dietary restriction catalyzed the evolution of the human brain: An exposition of the nutritional neurotrophic neoteny theory. Medical Hypotheses, 69: 1147-1153 Arnold, C., Matthews, L. J. & Nunn, C. L. (2010) The 10kTrees Website: A New Online Resource for Primate Phylogeny. Evolutionary Anthropology, 19: 114-118. Araujo, A., Arruda, M.F., Alencar, A.I., Albuquerque, F., Nascimento, M.C., and Yamamoto, M.E. (2000) Body weight of wild and captive common marmosets (Callithrix jacchus). International Journal of Primatology. 21: 317–324. Ashman, T.-L. (2003), Constraints on the evolution of males and sexual dimorphism: Field estimates of genetic architecture of reproductive traits in three populations of Gynodioecious fragaria virginiana. Evolution, 57 (9): 2012–2025. Barton, R. (2006) Primate brain evolution: Integrating comparative, neurophysiological, and ethological data. Evolutionary Anthropology 15: 224-236. Barrickman, N. L., Bastian, M.L., Isler, K. and van Schaik, C. P. (2008) Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. Journal of Human Evolution, 54:568-590. 58 Bennet, P. M. and Harvey, P.H. (1985) Brain size, development and metabolism in birds and mammals. Journal of Zoology, 207: 491-509. Bond, W. and Maze, K. (1999), Survival costs and reproductive benefits of floral display in a sexually dimorphic dioecious shrub, Leucadendron xanthoconus. Evolutionary Ecology, 13(1): 1-18. Bronson, R.T. (1981) Brain-weight body-weight relationships in twelve species of nonhuman primates. American Journal of Physical Anthropology 56: 77–81. Clutton-Brock, T.H., Harvey, P.H. and Rudder, B. (1977). Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature, 269:797-801. Cosgrove, K. P., Mazure, C. M., and Staley, J. K. (2007) Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62: 847-855. Deaner, R. O. and van Schaik, C. P. (2006) Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology 4: 149-196. Delph, L. F., Gehring, J. L., Frey, F. M., Arntz, A. M. and Levri, M. (2004) Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection. Evolution, 58 (9): 1936–1946. doi: 10.1111/j.0014-3820.2004.tb00481.x Dunbar, R. (1998) The Social Brain Hypothesis. Evolutionary Anthropology 6(5): 178-190. Elton, S., Bishop, L.C., and Wood, B. (2001)Comparative context of Plio-Pleistocene hominin brain evolution. Journal of Human Evolution 41: 1–27. Estrada, C. and Jiggins C. D. (2008) Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species? Journal of Evolutionary Biology, 21: 749–760. doi: 10.1111/j.1420-9101.2008.01517.x 59 Felsenstein, J. (1985) Phylogenies and the comparative method. The American Naturalist 125(1): 1-16. Gittelman, J. (1994) Female brain size and parental care in carnivores (mammal). Proceedings of the National Academy of Science 91: 5495-5497. Godfrey L., Lyon S., and Sutherland, M. (1993) Sexual dimorphism in large-bodied primates: The case of the subfossil lemurs. American Journal of Physical Anthropology 90: 315–334. Goldstein, J., Seidman, L., Horton, N., Makris, N., Kennedy , D., Caviness, V., Faraone, S. and Tsuang, M. (2001) Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex 11: 490-497. Gordon, A.D. (2006) Scaling of size and dimorphism in primates II: macroevolution. International Journal of Primatology 27: 63–105. Gould, S. J. (1974) Origin and function of 'bizarre' structures: Antler size and skull size in 'Irish Elk', Megaloceros giganteus. Evolution 28(2): 191-220. Hamon, T. R. (2005) Measurement of concurrent selection episodes. Evolution, 59(5): 1096–1103. doi: 10.1111/j.0014-3820.2005.tb01046.x Harvey, P.H. and Clutton-Brock, T.H. (1985) Life-history variation in primates. Evolution 39: 559–581. Harvey, P. H., Kavanagh, M. and Clutton-Brock T. H. (1978) Sexual dimorphism in primate teeth. Journal of Zoology London 186:474–485. Healy, S. and Hurly, T. (2004) Spatial learning and memory in birds. Brain Behavior and Evolution, 63:211-220. Helmuth, N. (2005) Sex-related differences in general intelligence g, brain size, and social status, Personality and Individual Differences 39(3): 497-509, ISSN 01918869, DOI: 10.1016/j.paid.2004.12.011. 60 Hereford, J., Hansen, T. F. and Houle, D. (2004) Comparing strengths of directional selection: How strong is strong?. Evolution, 58(10): 2133–2143. doi: 10.1111/j.00143820.2004.tb01592.x Hershkovitz, P. (1970) Cerebral fissure patterns in platyrrhine monkeys. Folia Primatologica. 13: 213–240. Ikeda, J., and Watanabe, T.,(1966) Morphological studies of Macaca fuscata. III. Craniometry. Primates 7, 271–288. Isler, K., Kirk, Joseph, E., Miller, M.A., Albrecht, G., Gelvin, B. and Martin, R. (2008) Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. Journal of Human Evolution 55: 967–978. Jerison, H. (1979) Paleoneurology and the evolution of the mind. Scientific American 234: 90-101. Jerison, H. (1979) Brain, Body and Encephalization in Early Primates. Journal of Human Evolution 8, 615-635. Kappeler P. (1990) The evolution of sexual size dimorphism in prosimian primates. American Journal of Primatology 21:201–214. Kappeler P. (1991) Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatologica (Basel) 57: 132–146 Kappeler P. (1999) Primate socioecology: new insights from males. Naturwissenschaften 85:18–29. Karubian, J. and Swaddle, J.P. (2001) Selection on females can lead to ‘larger males’. Proceedings of the Royal Society of London (B) 268:725-728. King, R. B. (1989) Sexual dimorphism in snake tail length: sexual selection, natural selection, or morphological constraint?. Biological Journal of the Linnean Society, 38: 133–154. doi: 10.1111/j.1095-8312.1989.tb01570.x 61 Kingslover, J. and Diamond, S. (2010), Phenotypic selection in natural populations: What limits directional selection? The American Naturalist 177(3): 346-357. Leutenegger, W. and Cheverud, J. (1982) Correlates of sexual dimorphism in primates: Ecological and size variables. International Journal of Primatology 3:387– 402. Lindenfors, P., Nunn, C. and Barton, R. (2007) Primate brain architecture and selection in relation to sex. BMC Biology 5:20. http://www.biomedcentral.com/17417007/5/20. Leutenegger, W. and Kelly, J.T. (1977). Relationship of sexual dimorphism in canine size and body size to social, behavioral and ecological correlates in anthropoid primates. Primates 18:117– 136. Marino, L. (1998) A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain Behavior and Evolution, 51: 230-238. Martin, R. (1996) Scaling of the mammalian brain: the Maternal Energy Hypothesis. Physiology 11 (4) 149-156. Martin L. (1991) Teeth, sex, and species. Nature 352:111–112. Mastretti, P. Pellerin, L., Rothman, D. L., and Shulman, R. (1999) Energy on demand. Science 22 (283): 496-497. [DOI:10.1126/science.283.5401.49 McNab, B.K. 1987a. Basal rate and phylogeny. Functional Ecology 1:159-160. McNab B. and Eisenberg, J. (1989) Brain size and its relation to the rate of metabolism in mammals. American Naturalist 133: 157–167. Mitani J., Gros-Louis J., and Richards A. (1996) Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. American Naturalist 147:966–980. 62 Mittermeier R. and van Roosmalen M. (1981) Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatologica 36: 1-39. Nevo, E. and Beiles, A. (1989) Sexual selection and natural selection in body size differentiation of subterranean mole rats. Journal of Zoological Systematics and Evolutionary Research 27: 263–269. doi: 10.1111/j.1439-0469.1989.tb00348.x Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., Hosaka, K., Hunt, K., Itoh, N., Kawanaka, K., and Matsumoto-Oda, A. (2003) Demography, female life history and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology 59(3): 99-121. Northcutt, R. G. (2001) Evolution of the nervous system: Changing views of brain evolution. Brain Research Bulletin 55(6): 663-674. Pilbeam, D., & Gould, S. (1974) Size and scaling in human evolution. Science 186: 892-901. Pilcher, H. (2004) Grey matter matters for intellect: Intelligence linked to size of key brain regions. Nature doi:10.1038/news040719-11. Plavcan, J.M. (2001) Sexual dimorphism in primate evolution. Yearbook of Physical Anthropology, 44: 25-53. Plavcan, J. M. and van Schaik C., P. (1994) Canine dimorphism. Evolutionary Anthropology 2:208–214. Plavcan J.M and van Schaik C.P. (1997b) Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology 103: 37–68. Porter, L. and Christen, A. (2002) Fungus and Callimico goeldii: new insights into Callimico Goeldii behavior and ecology. Evolutionary Anthropology 11(suppl 1):8790. 63 Raichle, M. and Gusnard, D. (2002) Appraising the brain’s energy budget. Proceedings of the National Academy of Science, 99 (16): 10237-10239. Reinius, B., Saetre, P., Leonard, J., Blekhman, R., Merino-Martinez, R., Gilad, Y. and Jazin, E. (2008) An evolutionarily conserved sexual signature in the primate brain. PLoS Genetics 4(6): 1-13. Roth, G., & Dicke, U. (2005) Evolution of the brain and intelligence. TRENDS in Cognitive Sciences 9(5): 250-257. Shah, N., Pisapia, D. J., Maniatis, S., Mendelsohn, M. M., Nemes, A., and Axel, R. (2004) Visualizing sexual dimorphism in the brain. Neuron 43: 313-319. Schillaci, M.A. (2006) Sexual Selection and the Evolution of Brain Size in Primates. PLoS ONE 1(1): e62. doi:10.1371/journal.pone.0000062. Schulke, O., Kappeler, P.M., and Zischler, H. (2004) Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behavioural Ecology Sociobiology 55: 293–301. Shultz, S. and Dunbar, R. (2010) Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proceedings of the National Academy of Science, 107(50): 21582-21586. Smith, R.J. and Jungers, W.L. (1997) Body mass in comparative primatology. Journal of Human Evolution 32: 523–559. Taylor, A. B., and van Schaik, C. P. (2006) Variation in brain size and ecology in Pongo. Journal of Human Evolution 52: 59-71. Thalmann, U. and Geissmann, T. (2000) Distribution and geographic variation in the western woolly lemur (Avahi occidentalis) with description of a new species (A.unicolor). International Journal of Primatology 21: 915–941. 64 van Roosmalen, M. (1985) Habitat preferences, diet, feeding strategy and social organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Surinam. Acta Amazonica 15(3/4, suppl): 1-238. van Schaik, C. (1989) The ecology of social relationships amongst female primates. In: Standen, V., & Foley, R. (eds.) Comparative socioecology: The behavioural ecology of humans and other mammals. Oxford: Blackwell Scientific Publications. 195-219. Verheyen, W.N., (1962) Contribution a` la craniologie compare ́e des primates: lesgenres Colobus Illiger 1811 et Cercopithecus Linne ́ 1758. Annual Museum Royal African Centre 105: 1–255. Wang, T., Hung, C.2 and Randall, D. (2006) The comparative physiology of food deprivation: From feast to famine. Annual Review of Physiology 68: 223–51. Weisbecker, V. and Goswami, A. (2010) Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proceedings of the National Academy of Sciences 107: 16216-16221. White F. (1988) Party composition and dynamics in Pan paniscus. International Journal of Primatology 9(3): 179-93. Williams, M. (2002) Primate encephalization and intelligence. Medical Hypotheses 58(4): 284-290. Wrangham, R. (1986) Ecology and social relationships in two species of chimpanzees. In: Rubenstein, D. I., & Wrangham, R. W. (eds), Ecological aspects of social evolution: Birds and mammals. Princeton, N.J: Princeton University Press. 352-378 Books: Barton R. (1999) The evolutionary ecology of the primate brain. In: Lee PC, editor. 65 Comparative primate socioecology. Cambridge: Cambridge University Press 167– 203. Darwin, C. R. (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray. [1st edition] Darwin, C. R. (1871) The descent of man, and selection in relation to sex. London: John Murray. Volume 1. 1st edition. Hopf, A. and Claussen, C. P. (1970) Comparative studies on the fresh weights of the brains and spinal cords of Theropithecus gelada, Papio hamadryas, and Cercopithecus aethiops. In: Kummer, H. (Ed.), Proceedings of the 3rd International Congress Primatology, Zurich, vol. 1. Karger, Basel, pp. 115–121. McNab, B.K. (1987b) The evolution of mammalian energetics. In: P. Calow, ed., Evolutionary Physiological Ecology. Cambridge University Press. pp 219-236. Okasha, S. (2009) Natural selection in the abstract. Evolution and the Levels of Selection. USA: Oxford University Press, pp. 10-34. Plavcan, J. (1999) Mating systems, intrasexual competition and sexual dimorphism in primates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. pp 241–269. Pickford, M. (1986). On the origins of body size dimorphism in primates. In: Pickford M, Chiarelli B, editors. Sexual dimorphism in living and fossil primates. Florence: Il Sedicesimo. p 77–91. Reynolds, J.D. & Harvey, P.H. (1994) Sexual selection and the evolution of sex differences. In Short R. & Balaban, eds. The Differences Between the Sexes. Cambridge: Cambridge University Press. pp 53-70. Smuts BB. (1985) Sex and friendship in baboons. New York: Aldine de Gruyter. pp 303. 66 White F. (1996) Comparative socioecology of Pan paniscus. In: McGrew W., Marchant L., and Nishida T., editors. Great ape societies. Cambridge, England: Cambridge University Press; p 29-41. Internet pages: Wilson, E. O. (2011) Where does good come from? Boston.com http://www.boston.com/bostonglobe/ideas/articles/2011/04/17/where_does_good_co me_from/?page=full Accessed May 2011. Coyne, J. (2011) The Boston Globe on kin selection. Why Evolution is True. http://whyevolutionistrue.wordpress.com/2011/04/17/the-boston-globe-on-kinselection/ Accessed May 2011. Mastretti, P., Pellerin, L. and Martin, J. Brain energy metabolism. American College of Neuropsychopharmacology. http://www.acnp.org/g4/GN401000064/CH064.HTML Accessed July 2011. Primate Info Net Library and Informatin Service. National Primate Research Center, Univeristy of Wisconsin – Madison. Primate Fact Sheets. http://pin.primate.wisc.edu/ Accessed May through September 2011. Animal Diversity Web – University of Michigan Museum of Zoology. http://animaldiversity.ummz.umich.edu/site/index.html Accessed May through September 2001. IUCN (International Union for Conservation of Nature) Red list – The IUCN Red List of Threatened Species. http://www.iucnredlist.org/ Accessed May through September 2001. 67