INTRODUCTION

Relations among living great apes and humans have been worked out in recent years to the satisfaction of most researchers, from both the molecular and the morphological/fossil approaches (Begun 1999; Begun, Ward & Rose 1997; Page & Goodman 2001; Satta, Klein & Takahata 2000; Shoshani et al. 1996). It is now widely recognized that humans and Pan (chimpanzees and bonobos) are members of a clade (evolutionary lineage) to the exclusion of other living primates, and that among living apes gorillas are next most closely related, orangutans after that, and hylobatids (gibbons and siamangs) after that. The living great apes, humans, and their ancestral lineages then form a natural evolutionary group, the hominids (Table 2.1 and Figure 2.1). Where fossil hominids (Miocene to Pleistocene great apes and humans) fall within this framework is the subject of intense debate, but this question is not critical to the theme of this chapter.

Phylogenetic parsimony suggests that characteristics shared among all members of the hominid group probably evolved once in their common ancestor rather than repeatedly in the separate lineages of the Hominidae. In some cases the symplesiomorphic (shared primitive) nature of characters shared among living hominids is supported by fossil evidence, such as brain size, body mass and rate of maturation (Begun & Kordos, Chapter 14, Gebo, Chapter 17, Kelley, Chapter 15, this volume). Among the shared characteristics that cannot be directly confirmed in the fossil record is great apes' distinctive intelligence.

Cooperatively breeding birds span a huge range of social organization, defined in part by the number of individuals of each sex and their reproductive roles within the group (Brown 1987; Stacey and Koenig 1990a; Cockburn 1998). In some species or groups, individuals of one sex share reproduction roughly equally, while in others a single individual monopolizes reproduction by that sex. Reproductive skew theory attempts to understand this variation in the partitioning of reproduction among individuals of the same sex. Such variation can be quantified as “reproductive skew,” ranging from 0 (egalitarianism) to 1 (monopolization). A key assumption of many models of optimal reproductive skew is that dominant individuals control the reproduction of subordinates, but that in some circumstances allow subordinates to share reproduction as a way of enlisting their cooperation (Vehrencamp 1979, 1980, 1983a, 1983b; Emlen 1982b). Dominants therefore determine the partitioning of reproduction and the magnitude of skew through the size of the reproductive “concession” granted to subordinates. Reproductive skew models were originally designed to explain variation among species, but are also applicable to variation within species and even within single populations (Emlen 1995; Reeve et al. 1998).

Within the last decade there has been a resurgence of interest in reproductive skew, stimulated in part by the ability to use molecular methods to determine parentage and thereby quantify skew.

Joint nesting is a relatively rare form of cooperative breeding in which two or more breeding group members of the same sex contribute genes to a clutch of eggs and cooperate in the care of young (Brown 1987; Vehrencamp 2000). Traditionally, joint nesting referred to multiple-female clutches. However, with the development of DNA techniques for assigning paternity, a growing number of cooperative species with shared-paternity clutches have been discovered. Joint-female (or communally laying) systems and joint-male (or cooperatively polyandrous) systems exhibit many important differences. Nevertheless, several avian joint-female species are also characterized by the presence of two or more adult males who share paternity to some degree. Here we focus on the diversity of joint-female systems, referring the reader to Chapter 10 and other reviews for discussions of breeding systems with male cobreeding (Faaborg and Patterson 1981; Hartley and Davies 1994; Ligon 1999).

Most joint-female species are non-passerines. By contrast, helper-at-the-nest species, as well as cooperatively polyandrous species, are found among both the passerines and non-passerines. There may be a good explanation for this pattern. Communally laying species all share one important feature: males make a large contribution to incubation and care of the young. In some joint-female species males perform all of the incubation and subsequent care, whereas in others the males perform more than half of the incubation, including nocturnal incubation.

In a survey of the phylogenetic origins of communal-laying species, all were found to arise in taxa with a history of strong male incubation (Vehrencamp 2000).

Tool use is an important aspect of being human that has assumed a central place in accounts of the evolutionary origins of human intelligence. This has inevitably focused a spotlight on any signs of tool use or manufacture in great apes and other nonhuman animals, to the relative neglect of skills that do not involve tools. The aim of this chapter is to explore whether this emphasis is appropriate. Suppose we take a broader view, accepting evidence from all manifestations of manual skill, what can we learn of the mental capacities of the great apes and the origins of human intelligence? My own ultimate purpose is to use comparative evidence from living species to reconstruct the evolutionary history of the many cognitive traits that came together to make human psychology. The cognition of great apes is the obvious starting point, to trace the more primitive (i.e., ancient) cognitive aptitudes that are still important to us today. In this chapter, I focus on great ape cognition as it is expressed in manual skills, based on cognitive aspects of tool use and manufacture considered significant in the human evolutionary lineage.

WHY IS TOOL USE IMPORTANT IN THE STUDY OF HUMAN EVOLUTION?

Consider first what aspects of tool use have recommended it as “special” to physical anthropologists and archaeologists. Most obviously, tools are convenient things for investigators. As physical objects, they can be collected, measured, and compared with ease.

In the nearly 80 years since Skutch (1935) coined the term “helper-at-the-nest,” cooperative breeding has attracted considerable interest, to no small extent because helping to raise non-descendant young violates a primary tenet of Darwinian theory. This “paradox” of how cooperative breeding could have evolved and subsequently have been maintained was partially resolved first by Hamilton (1963), who introduced the concept of kin-selected benefits by individuals that assist in rearing related individuals other than their own offspring, and later by Brown (1978), Koenig and Pitelka (1981), and Emlen (1982a), who developed the hypothesis that cooperatively breeding species were constrained by specific habitat requirements that induced philopatry, thus setting the stage for helping behavior.

Here we focus on the contributions of field endocrinology to our proximate-level understanding of cooperative breeding. Given that hormones are involved in mediating virtually all aspects of an organism's life and affect functions as diverse as gut absorption, blood production, and reproductive and agonistic behaviors, we can expect that they will also play an important role in the various kinds of cooperative and competitive interactions characteristic of cooperative breeders.

BACKGROUND

Reproductive hormones

Two endocrine axes are of primary interest here: the hypothalamo-pituitary-gonadal (HPG) axis and the hypothalamo–pituitary–adrenal (HPA) axis. The HPG axis consists of a region of the forebrain known as the hypothalamus, the pituitary that lies immediately below, and the gonads (Fig. 8.1). In response to stimulatory environmental or endogenous cues, the hypothalamus secretes gonadotropin-releasing hormone (GnRH).

INTRODUCTION

Amidst the welter of competencies that could be labeled “intelligence,” the great apes repeatedly demonstrate numerous high–level abilities that distinguish them from other mammals and ally them with humans (Griffin 1982; Parker & Gibson 1990; Russon, Bard & Parker 1996; Suddendorf & Whiten 2001). Self-concept is argued to be among this set of distinctive abilities. It is often viewed as an integral aspect of advanced intelligence, one that some have argued allows great apes to have a theory of mind (Heyes 1998 and references therein). Among the abilities that co-occur with it in humans are symbolic play, simple altruism, reciprocal relationships, a concept of planning, and pleasure in completion of complex tasks (Povinelli & Cant 1995).

Until recently, the demands of locomotion and posture, together referred to as positional behavior (Prost 1965), were not explicitly considered to correlate with any aspect of primate intelligence or its evolution, self-concept included. Primate intelligence is most often hypothesized to have evolved either for negotiating complex social problems, or for mapping and resolving complicated foraging challenges (for an overview, see Russon, Chapter 1, this volume). Chevalier-Skolnikoff, Galdikas and Skolnikoff (1982: 650) suggested instead that, at least for orangutans, locomotor demands were “the single major function for which the advanced cognitive abilities … evolved.” Povinelli and Cant (1995) subsequently refined and expanded this hypothesis, asserting that self-concept in orangutans evolved to enable these large-bodied apes to negotiate thin, compliant (i.e., flexible) branches during suspensory locomotor bouts, particularly when crossing gaps in the canopy.

Cooperative breeding continues to engender considerable interest among behavioral ecologists. However, the players and issues have changed dramatically since the publication of the first Cooperative Breeding in Birds volume (Stacey and Koenig 1990a). Back then, a series of long-term demographic studies were coming to fruition, opening the door for a synthetic volume that would “search for common themes and patterns” while illustrating “the great diversity that exists among cooperatively breeding birds” (Stacey and Koenig 1990b). At the time it appeared that the “common themes and patterns” would outstrip the “great diversity” and that a general understanding of the main issues raised by the phenomenon of cooperative breeding was about to be achieved (Emlen 1997a).

Such optimism concerning a general answer to the paradox of helping behavior was quickly dismissed (Cockburn 1998), and it has continued to elude our grasp. Instead, new theoretical approaches and studies have emerged to reinvigorate the field. Three stand out in particular. First is DNA fingerprinting, which was just getting started in the late 1980s and was only minimally represented in the 1990 volume. Multilocus minisatellite fingerprinting and its descendant, microsatellite fingerprinting, provided the long-sought-after ability to determine parentage and estimate relatedness. Fingerprinting allowed those who were continuing long-term studies or who had been fortunate enough to collect and save blood samples either to confirm prior inferences regarding patterns of parentage (as in Florida scrub-jays and acorn woodpeckers: Quinn et al. 1999; Dickinson et al. 1995; Haydock et al. Haydock et al. 2001) or to turn all prior inference on its head (as in the splendid fairy-wren: Brooker et al. 1990).

INTRODUCTION

Ecological hypotheses for the evolution of great ape intelligence relate selective pressures for increased intelligence to biological and environmental parameters such as body size, metabolic rate, life history, diet, home range size, habitat stratification, and predation risk (Clutton-Brock & Harvey 1980; Dunbar 1992; Gibson 1986; Milton 1981, 1988; Sawaguchi 1989, 1992). Of these, diet is the ecological selective pressure most frequently invoked to explain the emergence of great ape cognitive abilities. A correlation between diet and relative brain size in primates has long been established; frugivorous primates tend to have relatively larger brains than closely related folivorous taxa (Clutton-Brock & Harvey 1980; Milton 1981, 1988; Sawaguchi 1992). This pattern was most often explained in terms of the differing nutritional properties of fruits and leaves. A high-energy, fruit-based diet, it was thought, released energetic and metabolic constraints, allowing accelerated neonatal brain growth and maintenance of relatively greater adult brain mass (Jolly 1988; Martin 1981). However, the expansion of energy-hungry brain tissue will occur only where it confers an immediate adaptive advantage (Dunbar 1992). In other words, adequate energy supply is a necessary precondition for, but not in itself a sufficient stimulus to, increased encephalization.

Researchers seeking such a stimulus have tended to focus upon the adaptive role of intelligence in solving the unique foraging problems posed by primate diets.

INTRODUCTION

Research increasingly shows great apes surpassing other nonhuman primates in their mentality, achieving abilities traditionally considered uniquely human. Importantly, the cognitive capacities that distinguish them include rudimentary symbolic processes, in the sense of processes that operate on the basis of mental images rather than direct sensory-motor phenomena. Although this view does not represent consensus among experts (e.g., Tomasello & Call 1997), many well-respected researchers now accept this interpretation of the empirical evidence (e.g., Byrne 1995; Langer & Killen 1998; Parker & McKinney 1999; Parker, Mitchell & Boccia 1994; Parker, Mitchell & Miles 1999; Russon, Bard & Parker 1996; Savage–Rumbaugh, Shanker & Taylor 1998; Whiten & Byrne 1991; Wrangham et al. 1994).

If great apes are capable of symbolic cognitive processes, views of symbolism as having evolved within the human lineage are incorrect. Implications for understanding cognitive evolution within the primates are complex and important. First, neither the landmark significance of symbolism to cognition nor its importance in understanding the evolution of higher primate cognition is diminished by this revision. What is altered is timing. Symbolic cognition shifts from an achievement of the human lineage to a foundation for it. Second, reconstructions of the conditions leading to the evolution of symbolic processes remain important, but existing reconstructions lose much of their weight because they focus on conditions linked with the divergence of the human lineage. If symbolic processes are the joint province of humans and great apes, ancestral large hominoids are their probable evolutionary source.

This book arose from three realizations. First, there is an important need for good models of great ape cognitive evolution. Studies of comparative primate cognition over the last two decades increasingly show that all great apes share a grade of cognition distinct from that of other nonhuman primates. Their cognition appears to be intermediate in complexity between that of other nonhuman primates and humans, so it offers the best available model of the cognitive platform from which human cognition evolved. Understanding the position of the great apes is then essential to understanding cognitive evolution within the primate order and ultimately, in humans. Second, existing reconstructions of the evolutionary origins of great ape cognition are all in need of revision because of advances in research on great ape cognition itself, on modern great ape adaptation, and on fossil hominoids. Third, developing an accurate picture of the evolutionary origins of great ape intelligence requires bringing together expertise from a highly diverse range of fields beyond modern great ape cognition. Essential are current understandings of the brain, life histories, social and ecological challenges, and the interactions among them in both living and ancestral hominids.

We therefore assembled a team of contributors with expertise spanning the topics currently recognized as relevant to cognitive evolution in the great ape lineage, with the aim of piecing together the most comprehensive picture possible today. We asked all our contributors to explore the implications of their realm of expertise for cognition and cognitive evolution.

Helping behavior is enigmatic as it appears to entail an individual sacrificing personal reproduction while assisting others in their breeding attempts. Over the past 40 years, the field of cooperative breeding has developed a rich body of theory to explain helping behavior, and enough cooperative species have been studied in detail to establish common ground and test theory. Indeed Emlen (1997a) stated that the original paradox of cooperative breeding had largely been resolved with the widespread confirmation that (1) helpers are often individuals that are constrained from breeding due to a shortage of quality breeding opportunities, (2) helpers unable to obtain breeding positions in the current year frequently improve their chances of becoming breeders in the future, and (3) helpers frequently obtain large indirect benefits by helping to rear collateral kin. With identification of these direct and indirect benefits to helpers, Emlen suggested that the original questions asked by researchers in this field would appear to be “largely answered.”

In contrast, Cockburn (1998) concluded that “we are still some way from understanding the adaptive significance of helping behavior although we are poised for a reinvigoration of the study of cooperation through a number of conceptual, empirical, and technical advances.” Clearly, conceptual breakthroughs have been made, but many important questions also remain unanswered. In particular, our understanding of the varying level of helper contributions within and between species and how these contributions benefit breeders and helpers remains poor.

DOES GREAT APE INTELLIGENCE DIFFER FROM THAT OF MONKEYS?

There is growing consensus that great apes' intellectual abilities are qualitatively distinct from those of other primate taxa, as seen in their mirror self-recognition (e.g., Gallup, 1970) causal understanding of tool-using tasks without trial and error (Visalberghi, Fragaszy & Savage-Rumbaugh 1995), and imitative ability (e.g., Custance, Whiten & Bard 1995), among other traits and abilities (see Russon, Bard & Parker 1996; other chapters this volume). This raises the important question: In what ecological and social environments did this distinct intellectual capacity evolve?

Potential answers have been much discussed in recent years. Using brain parameters (e.g., absolute or relative brain size, neocortex ratio) as proxies for the rather amorphous concept of “intelligence,” comparative studies (Dunbar 1992, 1995) have found that the size of the social network (represented by group size) better explains variation in the neocortex ratio among primate taxa than any of the ecological parameters considered thus far, such as degree of frugivory, range size, or presence/absence of “extractive foraging.” This suggests that the social complexity resulting from primate-style group living is more likely to be behind variations in primate intelligence, as the so-called “social intellect hypothesis” sets out (Chance & Mead 1953; Humphrey 1976), than the ecological complexity arising from foraging problems, as some others have suggested (Menzel 1997; Milton 1981; Parker & Gibson 1979).