The mechanisms of evolutionary selection

Sex differences in brain, behavior, and cognition are inherently interesting to the scientist and the lay person alike. In fact, some level of interest in sex differences would be expected for nearly all individuals of any sexually reproducing species, given that one of the most fundamental goals of life--to reproduce--necessarily involves negotiating some type of relationship with at least one member of the opposite sex. Not surprisingly, research on sex differences has occupied biological and social scientists for more than a century but, with a few notable exceptions (e.g., Daly & Wilson, 1983; Buss, 1994), the research programs in these two broad areas have largely developed independently of one another. In recent years, biologists have used Darwin’s (1871) principles of sexual selection (explained in Chapter 2) to provide a coherent theoretical framework for the study of sex differences across hundreds of studies and across scores of species (Andersson, 1994).

At the same time, social scientists have, for the most part, been studying sex differences from a completely different theoretical perspective, gender roles (e.g., Eagly, 1987). The gist is that most nonphysical human sex differences are the result of the culturally-mediated social roles that are adopted by boys and men and girls and women. In many cases, the belief that human sex differences are the result of the adoption of such roles is accepted, it seems, without a critical evaluation of this perspective. The goal of this book is not to provide such a critical evaluation--although associated discussion can be found in Chapter 6 and Chapter 7--but rather to approach the issue of human sex differences from the same theoretical perspective that is used to study sex differences in all other species--sexual selection. In fact, it is the thesis of this book that human sex differences can never be fully understood without an understanding and an appreciation of sexual selection and an understanding of how the associated processes are manifested in other species. The basic structure of the book is overviewed in this chapter, following a brief introduction to the mechanisms of evolutionary selection (see Dennett, 1995, and Weiner, 1995, for extended and accessible discussion of the mechanisms of evolutionary selection).

The Mechanisms of Evolutionary Selection

Any process, event, or ecological condition that in any way influences life, death, and reproduction is a potential selection pressure. Any such pressure acts on individuals, but not in a random fashion; although random or chance events do occur and can influence evolutionary processes (Mayr, 1983). Rather, for nearly all features of physiology, body structure, or behavior individuals of the same species will differ to some degree. In many cases, these individuals differences are unrelated to life, death, and reproduction. In other cases, even slight differences can determine which individuals will live and reproduce and which individuals will die. It is in these cases that evolutionary selection is occurring (Darwin, 1859).

The result of such selection is that those individuals who happen to have a somewhat shorter beak or a somewhat larger body size--or whatever characteristic influences survival and reproduction--will survive in greater numbers than their peers. If these characteristics are inherited, then the survivors will produce offspring who also have a somewhat shorter beak or a somewhat larger body size than other members of the same species (i.e., conspecifics). If these characteristics continue to influence life, death, and reproduction in the offspring’s generation, then the process will repeat itself. Over generations and sometimes in a single generation there is a change in the selected characteristic, such that the average individual in the population now has a shorter beak or a larger body size than did the average individual several generations earlier.

It is this process--natural selection--that shapes species to their ecology. All that is required for natural selection to occur is that the trait dealing in life, death, and reproduction vary across individuals and that some portion of this variability have a genetic basis (Mayr, 1983). Under these conditions, selection will occur, whether the trait is physical, physiological, or behavioral.

If evolution of behavior proceeds like the evolution of structural or molecular characteristics, then, according to the Darwinian interpretation, it must have two characteristics. First, in order to be able to respond to selection pressures, such behavior must at least in part have a genetic basis, and secondly, the genetic basis must be somewhat variable, that is, it must be able to supply the material on which natural selection can act. Behavioral characteristics thus would share, whenever they evolve, the two most important aspects of evolving structural characteristics: variability and a genetic basis. (Mayr, 1974, pp. 653-654).

Thus, heritable individual differences provide the grist for evolutionary selection. Given that nearly all features of human anatomy, physiology, behavior, cognitions, and so on show individual variability that is partly heritable, they are all potentially subject to selection pressures (e.g., Bouchard, Lykken, McGue, Segal, & Tellegen, 1990; Farber, 1981; Finkel & McGue, 1997; Plomin & Petrill, 1997). The issue is complex, however.

Selection pressures can reduce or eliminate heritable variability and thus many traits that have undergone strong selection in the past no longer show heritable variability (e.g., all genetically normal human beings have two legs, an inherited but nonvariable characteristic). Some traits that show heritable variability have not been subject to selection pressures at all (Gould & Vrba, 1982; e.g., reading ability, discussed in Chapter 9) and other traits that show heritable variability are only subject to selection pressures under certain conditions. Selection pressures can vary from one generation to the next or from one geographical region to the next. At times--when food is abundant and predators and parasites are scarce--selection pressures are weak and thus most individuals survive and reproduce, that is, individual differences are not especially important under these conditions.

The process of evolutionary selection and change can be illustrated by the work of Peter and Rosemary Grant (e.g., Grant & Grant, 1989; Grant & Grant, 1993); this research is nicely captured in Weiner’s (1995) Pulitzer Prize winning narrative. For several decades the Grants have been studying the relation between ecological change on several of the Gal?font> pagos islands--Daphne major and Genovesa--and change in the survival rates and physical characteristics of several species of finch that reside on these islands, often called Darwin’s finches. One of these finches, the medium ground finch (Geospiza fortis), resides on Daphne major and ecological change on this island has been shown to result in changes in the average beak size of individuals of this species from one generation to the next (Grant & Grant, 1993). Figure 1.1 shows that individual medium ground finches naturally vary from each other in beak size, as well as for other physical characteristics. To the left is an illustration of an individual with a relatively small beak and to the right is an individual of the same age and sex with a relatively large beak. The distributions show that the beak size of most individuals will be in-between these two extremes.

For the medium ground finch, and in fact for all of Darwin’s finches, the size and shape of an individual’s beak determines which foods can be eaten and which foods cannot. When food sources (e.g., seeds, insects, etc.) are plentiful and varied there is little relation between beak size and survival and reproductive rates. Under these conditions, most of Darwin’s finches--within and across species--survive and reproduce. When foods are scarce, individual birds tend to specialize in one food source (e.g., seeds) or another (e.g., insects) depending on the size and shape of their beak. Under these conditions, some food sources are usually more plentiful than others. Individuals who are able to specialize--due to beak size and shape--in a relatively abundant food source survive and reproduce in greater numbers than do individuals whose beak size and shape forces them to specialize in a scarce food source.

To illustrate, there was very little rain on Daphne major in 1973. The result of this drought was an 84% decline in the quantity of foods available to Darwin’s finches and a sharp increase in finch mortality rates (Weiner, 1995). For Darwin’s finches, life or death depended greatly on beak size. One of the foods that was still relatively plentiful during this time was the seeds of the caltrop plant (Tribulus cistoides). These seeds are encased in mericarps--shown in the center of Figure 1.1--which are armored with spikes and relatively large, at least for a finch. Some medium ground finches or fortis were able to exploit this food source, whereas others were not.

fortis with bigger beaks can crack the mericarp and gouge out the seeds faster than those with smaller beaks. Tiny variations are everything. A fortis with a beak 11 millimeters long can crack caltrop; a fortis with a beak only 10.5 millimeters long will not even try. "The smallest grain in the balance" can decide who shall live and who shall die. Between a beak big enough to crack caltrop and a beak that can’t, the difference is only half a millimeter (Weiner, 1995, p. 64).

During this time medium ground finches with relatively large beaks survived in greater numbers than did conspecifics (recall, member of the same species) with relatively small beaks. To make matters worse, survivors with relatively small beaks were at a mating disadvantage. It appears that short-beaked males were weaker than their better fed large-beaked peers, which appeared to result in a difference in the vigor of the courtship displays of small- and large-beaked finches. Female medium ground finches choose mates based on the vigor of their courtship display and thus preferred large-beaked males. The combination of differential survival rates and female choice--a feature of sexual selection discussed in Chapter 2--resulted in a measurable shift in the next generation’s average beak size (beak size is heritable), as illustrated in Figure 1.1. The leftmost distribution represents the beak size characteristics of medium ground finches before the drought and the rightmost distribution represents these characteristics after the drought. Just after the drought, individual differences in beak size are still evident, but the average beak size has now increased and there are fewer individuals with extremely small beaks and more individuals with extremely large beaks.

For the medium ground finch having a beak that is larger than average is not inherently better than having a beak that is smaller than average, it is only beneficial during periods of drought. Several years after the drought, in 1982-83, an especially strong El Ni??ont> o event resulted in a 14 fold increase in rainfall on Daphne major (Grant & Grant, 1993). Following this heavy rainfall, the number of caltrop plants and their mericarps decreased significantly and the number of smaller seeds available on the island increased significantly. "Mechanical efficiency of handling small seeds appears to be a feature of finches with small beaks" (Grant & Grant, 1993, p. 114). The result was small-beaked individuals survived in greater numbers than did large-beaked individuals and small-beaked males were preferred as mating partners (presumably due to more vigorous courtship displays). The survival and reproductive advantages of small-beaked individuals was evident for at least 6 years following the El Ni??ont> o event. After several generations, the average beak size of medium ground finches was now smaller than it was just after the drought--the distribution had shifted back to the left!

An equally important finding was that these selection pressures only effected beak size and not other physical characteristics (e.g., leg length) (Grant & Grant, 1993). In other words, under difficult conditions--those resulting in strong selection pressures--evolutionary selection acts quickly (sometimes in one or a few generations) and selectively (effecting only those traits that directly influence survival and reproduction). The process of relatively fast evolutionary selection and change is not restricted to Darwin’s finches. It has also been demonstrated with a number of other species (e.g., Reznick, Shaw, Rodd, & Shaw, 1997; Seehausen, van Alphen, & Witte, 1997), including perhaps humans (Holliday, 1997). On the basis of change in relative bone size (e.g., femur, that is thigh bone, length) comparing fossils dating from 6,000 to 30,000 years ago to modern populations, Holliday concluded "that the current patterns of body form in Europe go back no farther than 20,000 years" (Holliday, 1997, p. 444).

Overview

To fully comprehend and appreciate human sex differences, an understanding of the evolutionary, hormonal, and ecological conditions that underlie sex differences in other species is essential, as noted earlier. In fact, a full understanding of human sex differences requires that we begin with a consideration of the evolution of sexual reproduction itself. This is so because the grist of evolutionary selection is heritable individual differences and the ultimate source of this variability--and the first topic addressed in Chapter 2--is sexual reproduction. In relation to asexual reproduction, sexual reproduction appears provide a number of benefits, including the elimination of harmful mutations (Crow, 1997), ecological adaptation (Williams, 1975), and the generation of a complex and varied immune system (Hamilton & Zuk, 1982). In all of these cases, the result is greater variability, or individual differences, within sexually reproducing species than within asexually reproducing species.

Once sexual reproduction evolved, an essential feature of the life history of all individuals of sexually reproducing species is to find a mate or mates. To further complicate this life-task, the individual variability that results from sexual reproduction will ensure that all potential mates are not equal, which, in turn, results in competition for the most suitable mate or for the most mates. The processes associated with choosing and competing for mates is sexual selection (Darwin, 1871), the fundamentals of which are the topic of the second section in chapter 2. Sexual selection is a dynamic process that is influenced by a host of factors, including sex differences in the relative costs and benefits of reproduction (Trivers, 1972) and the ecology of the species (Emlen & Oring, 1977), among others. These dynamics are most typically expressed in terms of female choice of mating partners and male-male competition over access to mates or for control of those resources that females need to rear their offspring (Andersson, 1994), the nuances of which are detailed in Chapter 2. Following the discussion of the dynamics of female choice and male-male competition, the focus shifts to discussion of the mechanisms that influence the expression of the associated sex differences in brain, behavior, and cognition, that is, sex hormones.

Chapter 3 brings us one step closer to human sex differences and focuses exclusively on sexual selection in nonhuman primates and the apparent pattern of sexual selection in our hominid ancestors. The research reviewed in this chapter reveals that nearly all of the sex differences found in humans are evident in many other primate species. As an example, one of the more thoroughly studied aspects of primate social behavior is male-male competition. For many species of primate, including humans in many contexts, males compete by means of physical attack and physical threat to establish social dominance over other males. Position within the resulting dominance hierarchy often times has rather dramatic reproductive consequences for individual males. In many contexts, only the most dominant, or alpha, male sires offspring (e.g., Altmann et al., 1996). The achievement of social dominance is complex, however. In some species, social dominance is achieved through one-on-one physical contests, in other species it is more dependent on the coalitional activities of groups of males, and in still other species it is influenced by the social support of females in the group (Dunbar, 1984; Goodall, 1986; Smuts, 1985). All of these different patterns, and many other features of male-male competition in primates, are described in Chapter 3.

With the exception of humans, female choice has not been as systematically studied in primates as male-male competition or female choice in other species (e.g., birds). The research that has been conducted clearly indicates that females in many, if not all, primate species prefer some males to others as mating partners (Smuts, 1985). The bases for female choice appears to vary with social and ecological conditions but is often influenced by infanticide risks and the social support that a male partner might provide (Hrdy, 1979). For instance, in the olive baboon (Papio anubis) females prefer as mating partners those males who provide social protection (e.g., from other males) and other forms of care to them and their offspring (Smuts & Gubernick, 1992).

Female-female competition is also evident in most, if not all, primate species. However, unlike male primates, female primates more typically compete for access to high-quality food and not access to mates (Silk, 1993). Access to high-quality food has important reproductive consequences for these females and their offspring, as females who have access to this food are larger, healthier and have more surviving offspring than their undernourished peers. Male choice is also evident in many species of primate and appears to be based on the nature of the relationship between the male and individual females and on implicit reproductive concerns. All other things being equal, male primates prefer to mate with females who are currently fertile (this is typically signaled through a swelling of the sexual organs) and have borne one or more offspring (Silk, 1987a).

One of the more consistent consequences of male-male competition in primates is larger and more aggressive males than females (Plavcan & van Schaik, 1997a). The more intense the male-male competition, the larger the sex difference in physical size, although these differences are somewhat less pronounced in species where male-male competition is coalition based as in our cousin, the chimpanzee (Pan troglodytes) (Goodall, 1986). The consistent relation between physical sex differences and the intensity of male-male competition allows inferences to be drawn about the likely nature of male-male competition in our ancestors. Beginning with our Australopithecine ancestors and continuing to modern humans, males are physical larger than females. When these patterns are combined with the patterns of male-male competition and female choice that are evident in extant primates inferences can be--and are in the final section of Chapter 3--drawn about the potential pattern of sexual selection during the course of human evolution (Foley & Lee, 1989).

Beginning in Chapter 4 and continuing throughout the remainder of the book, the focus is on sexual selection in modern human populations. Chapter 4 focuses specifically on paternal investment. In most mammalian species, males provide little if any direct investment in offspring (Clutton-Brock, 1989). As a result, the reproductive effort of males tends to be largely focused on mating effort and the associated male-male competition and the reproductive effort of females tends to be largely focused on parental effort and the associated female choice (e.g., to get the best genes for their offspring). The dynamics of sexual selection are much more complication for species--which includes humans--where males show some level of direct parental investment. When both the mother and the father invest in offspring and there are individual differences in the quality of care or genes that parents provide to these offspring, then female-female competition and male choice become important features of sexual selection, in addition to male-male competition and female choice (Parker & Simmons, 1996). Chapter 4 provides a contrast of maternal and paternal investment, documents the pattern of paternal investment across cultures and across species of primate, and finally, provides an overview of the relation between paternal investment and the physical and social well-being of children.

Chapter 5 provides a review of the dynamics of sexual selection in modern humans, that is, female choice, female-female competition, male-male competition and male choice. As with other primates, the dynamics of sexual selection in humans is complex and can vary from one culture or context (e.g., different historical periods within a culture) to the next. For instance, men throughout the world compete for cultural success (Irons, 1979), that is, they compete for control of culturally important resources and for the establishment of social status. Cultural success can be achieved in many different ways, ranging from obtaining the head of one’s competitor to securing a high-paying job. However it is achieved, successful men typically have more wives and children, or at least more mating opportunities, than their less successful peers (Chagnon, 1988; Irons, 1993; P?font> russe, 1993). In other words, in Chapter 5 there is not only discussion of sexual selection in humans, there are numerous illustrations of how these dynamics are expressed in different cultures, during different historical periods within cultures, and how they are modified by social ideologies.

Chapter 6 provides the foundation for later discussion of developmental sex differences (Chapter 7) and sex differences in brain and cognition (Chapter 8) and is one of the more unique features of this book. The goal of Chapter 6 was to develop a unified framework for understanding sex differences in the motivational, emotional, cognitive, neural, and developmental processes and systems that underlie the sex differences in reproductive strategies described in Chapter 4 and Chapter 5. The basic thesis is that the fundamental motivation of human beings, and all other complex organisms, is to achieve some level of control over the social (e.g., other people), biological (e.g., food), and physical (e.g., territory) resources that support life and allow one to reproduce (Geary, 1998; Heckhausen & Schulz, 1995). Or stated otherwise, the human mind--and the associated motivational, emotional, behavioral and brain systems--has been shaped by evolutionary selection to organize and guide attempts to control the social, biological, and physical resources that support survival and reproduction. Childhood is the portion of the lifespan during which these systems become adapted--for example through play--to local ecologies.

In this view, sex differences that are evident during development should be a reflection of later sex differences in reproductive strategies. The evidence for this thesis is provided in Chapter 7. More specifically, the chapter covers sex differences in physical development, during infancy, play patterns, social development, and parenting influences, all from the perspective of sexual selection. As an example, for primate species characterized by relatively intense male-male competition, males are not only larger than females they also show a different pattern of physical development (Leigh, 1996). The most general pattern is for males to mature later than females and to show a longer growth spurt during puberty (this contributes to their larger size). For species in which there is relatively little male-male competition and a monogamous mating system, males are the same size as females and males and females show nearly identical growth patterns (Leigh, 1995). Sex differences in human physical development follow the pattern found in species with relatively intense male-male competition (Tanner, 1990) and clearly support the position that male-male competition has been an important social dynamic during the course of human evolution.

In chapter 8, sex differences in brain and cognition are approached using a proposed system of evolved cognitive modules developed in Chapter 6, a system of modules corresponding to the motivation to control social, biological, and physical resources. Social modules, for instance, are divided into individual level cognitions--such as language, facial processing, and theory of mind (i.e., the ability to make inferences about the intentions, emotional states, and so on of other people)--and group-level cognitions--such as the formation of in-groups and out-groups. The use of this theoretical framework provides a unique organization to the research on human sex differences in brain and cognition and reveals patterns that are consistent with the view that many of these sex differences have been shaped by sexual selection. As an example, while girls and boys and women and men readily classify other human beings in terms of favored in-groups and disfavored out-groups (Stephan, 1985), there appear to be sex differences in the dynamics of in-group and out-group formation. In comparison to girls and women, boys and men appear to place more social pressures on in-group members to conform to group mores and appear to more easily develop agonistic attitudes and behaviors towards members of an out-group, especially during periods of competition or conflict. The sex difference in the dynamics of in-group and out-group formation can be readily understood in terms of coalition-based male-male competition.

The final chapter provides a discussion of how sex differences that appear to have been shaped by sexual selection might be indirectly related to sex differences that are important in modern society (Geary, 1996), including sex differences in academic competencies (e.g., reading achievement), violence, accidental death and injury rates, the experience of anxiety- and depression-related symptoms (e.g., sad affect) and disorders, eating disorders, and occupational interests and occupational achievement. To illustrate, girls and women obtain higher average scores than boys and men on reading achievement tests in elementary school, junior high school, high school, and in the general population of adults (Hedges & Nowell, 1995). Reading is almost certainly not an evolved cognitive competency and thus the advantage of girls and women in this area is not directly related to evolutionary selection (Geary, 1995; Rozin, 1976).

Nonetheless, the advantage of girls and women in reading achievement might be indirectly related to more primary, that is, evolved, cognitive sex differences. For instance, girls and presumably women appear to have a more elaborated theory of mind than do same-age boys and men (Banerjee, 1997) (Chapter 8). Girls and women appear to be more skilled, on average, than boys and men in making inferences about the emotional state, intentions, and so on of other people, which, in turn, appears to contribute to their advantage on tests of reading comprehension. The sex difference, favoring girls and women, on tests of reading comprehension is largest for social themes and smallest for themes that do not involve people (Willingham & Cole, 1997). In other words, theory of mind might facilitate reading comprehension through skill at mentally representing the plots and subplots that unfold in the narrative and girls and women appear to have an advantage over boys and men in generating these mental representations.

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