We know a great deal about roles the environment plays in shaping survival, reproductive success, and even social systems among primates. But how do primate life histories affect social systems and vice versa? Do baboons' patterns of growth, for example, help to structure their societies? Does fission-fusion sociality interact with predator pressure to influence the timing of maturation in chimpanzees?
Exploring these issues and many others, the contributors to Primate Life Histories and Socioecology provide the first systematic attempt to understand relationships among primate life histories, ecology, and social behavior conjointly. Topics covered include how primate life histories interact with rates of evolution, predator pressure, and diverse social structures; how the slow maturation of primates affects the behavior of both young and adult caregivers; and reciprocal relationships between large brains and increased social and behavioral complexity. The first collection of its kind, this book will interest a wide range of researchers, from anthropologists and evolutionary biologists to psychologists and ecologists.
Paul-Michael Agapow, Susan C. Alberts, Jeanne Altmann, Robert A. Barton, Nicholas G. Blurton Jones, Robert O. Deaner, Robin I. M. Dunbar, Jörg U. Ganzhorn, Laurie R. Godfrey, Kristen Hawkes, Nick J. B. Isaac, Charles H. Janson, Kate E. Jones, William L. Jungers, Peter M. Kappeler, Susanne Klaus, Phyllis C. Lee, Steven R. Leigh, Robert D. Martin, James F. O'Connell, Sylvia Ortmann, Michael E. Pereira, Andy Purvis, Caroline Ross, Karen E. Samonds, Jutta Schmid, Stephen C. Stearns, Michael R. Sutherland, Carel P. van Schaik, and Andrea J. Webster.
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About the Author
Peter M. Kappeler is the head of the Department of Behavior and Ecology at the German Primate Center in Göttingen. He is editor of Primate Males: Causes and Consequences of Variation in Group Composition and coeditor of Lemur Social Systems and Their Ecological Basis.
Michael E. Pereira is a research associate at the Lincoln Park Zoo and a science teacher at the Latin School of Chicago. He is coeditor of Juvenile Primates: Life History, Development, and Behavior, also published by the University of Chicago Press.
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Primate Life Histories and Socioecology
The University of Chicago Press
Copyright © 2003 The University of Chicago
All right reserved.
Primate Life Histories and Socioecology
Peter M. Kappeler, Michael E. Pereira, and Carel P. van Schaik
One major goal of socioecology is to explain the evolution of diversity among social systems, which are defined in relation to both grouping characteristics and the nature of social and mating relationships within groups. The socioecological model, a theoretical framework that has guided much research in this area (Crook 1964; Crook and Gartlan 1966; Crook 1968, 1970; Crook, Ellis, and Goss-Custard 1976; Emlen and Oring 1977; Terborgh and Janson 1986; Standen and Foley 1989), has traditionally emphasized the effects of major ecological factors, especially resource distribution and risk of predation (Jarman 1974; Wrangham 1980a; van Schaik 1983; van Schaik and van Hooff 1983; Rubenstein and Wrangham 1986; Wrangham 1987; van Schaik 1989; Janson and Goldsmith 1995; van Schaik 1996; Sterck, Watts, and van Schaik 1997; Janson 1998).
During the past decade, however, this perspective has been broadened by the elucidation of sex-typical reproductive strategies and influences of sexual conflict on social relationships (Clutton-Brock 1989; Davies 1991; Clutton-Brock and Parker 1992; Smuts and Smuts 1993; Brereton 1995; Clutton-Brock and Parker 1995; Dunbar 1995a; van Schaik 1996; van Schaik and Kappeler 1997; Treves 1998; Kappeler 1999; Linklater et al. 1999; van Schaik, van Noordwijk, and Nunn 1999; Widemo and Owens 1999; Davies 2000). Since individual and taxon-specific life histories may constrain sexual strategies and other behavioral adaptations, earlier assertions that life history limits on behavioral evolution "are not surprising enough to catalyse interest" (Stearns 1992, p. 210) merit reconsideration. Indeed, considerable work has demonstrated that nontrivial relationships among life history, ecology, and behavior are shaped by ecological conditions (Caswell 1983; Stearns and Koella 1986; Stearns 1989a; Reznick et al. 1990; Janson and van Schaik 1993; Via et al. 1995; Przybylo, Sheldon, and Merilä 2000), indicating avenues for further expansion of the socioecological model (see also Stearns 2000). The main goals of this chapter are, therefore, (1) to formally expand the socioecological model by describing these additional interrelationships, (2) to identify potential links of causality among them, and (3) to illustrate these links using work on primates as examples from a diverse taxon with well-described life histories, ecologies, and social systems.
Evidence for Interrelationships
To substantiate the value of expanding the socioecological model, we first present some recent nonprimate examples of interactions among life history, ecology, and behavior. The first case provides a fresh perspective on the evolution of cooperative breeding, which occurs in about 3% of extant bird species, by illustrating how a change in life history traits can have consequences for individual behavior and, therefore, for an entire social system.
Whereas current explanations for the absence of independent breeding in helper individuals focus largely on ecological constraints (e.g., Emlen 1994), a comparison of avian orders by Arnold and Owens (1999) suggests that the evolution of slow life histories has also played an important role. The high adult survival rate characteristic of slow life histories retards the rate of territory turnover, thereby limiting opportunities for dispersal and independent breeding by young adults. Shifts from fast to slow life histories, in other words, have apparently augmented the potential advantages of helping to raise one's parents' next clutches of young, promoting the expression of helping behavior under particular ecological conditions.
A second example suggests effects in the opposite direction; that is, a life history trait modified in response to changes in a behavioral variable. Specifically, some females of a semelparous spider (Stegodyphus lineatus) delay reproduction to reduce the risk of infanticide by males (Schneider 1999). Female Stegodyphus typically guard a single egg sac until their young hatch and begin eating their mother. Sometimes males succeed in destroying a female's egg sac, however, thereby stimulating her to produce a second clutch, which is typically much smaller. Whereas males generally mature early, with an expected adult life span of only two to three weeks, females vary by a factor of four in the time taken to reach sexual maturity. The number of males, and thus the risk of infanticide, consequently decreases as the reproductive season progresses. Intersexual conflict thus contributes to plasticity in female reproductive strategy in this species, with early-maturing females reducing the risk of infanticide by delaying oviposition.
A final example shows that life history and behavioral strategies are generally finely tuned to each other, potentially linked genetically (i.e., pleiotropic), and conjointly responsive to ecological conditions. This case features growth rate as a life history parameter influencing foraging decisions in relation to predation risk (Werner and Anholt 1993). Exposing both transgenic salmon (Salmo salar) with enhanced growth rates and unmanipulated control individuals to predators, Abrahams and Sutterlin (1999) showed that the transgenic animals continued to express higher rates of feeding. The genetic manipulation's simultaneous effects on life history, foraging, and antipredator behavior suggest that the evolution of all three traits has been constrained by the ecological variable of predation risk (see also Arenz and Leger 2000).
A review of the relevant literature provides many more examples of direct interactions among features of life history, ecology, and behavior. The conceptual integration of these interrelationships into the socioecological model, however, is still in its infancy. We advocate the expansion of this theoretical framework by reviewing the new aspects suggested by primate studies, just as primate studies have previously helped to elaborate and refine the model. Because life histories are the new component we wish to add, we begin with an overview of life history concepts and the general characteristics of primate life histories. In subsequent sections, we examine interactions between life histories and social systems. The limited available information on modulation of life histories in response to ecological variation is summarized in other chapters (Ganzhorn et al., chap. 6; Janson, chap. 5; Lee and Kappeler, chap. 3; Pereira and Leigh, chap. 7; all this volume).
The life history of an organism is defined by features of its life cycle pertaining to developmental and reproductive rates as well as reproductive effort (Roff 1992; Stearns 1992). In mammals, gestation length, size, number, and sex of offspring, interbirth interval, age and size at weaning, age and size at first breeding, and life span are the most important life history traits (Charnov 1991).
Actual life histories vary tremendously among individuals of the same species. An elephant, for instance, can die as a fetus or soon after birth, but she can also live to be 80 years old. Nevertheless, each life history trait shows characteristic central tendencies when averaged for all individuals of a species, and there appear to be invariant relations between life history traits assessed across higher taxonomic levels (Charnov 1993; Hawkes, O'Connell, and Blurton Jones, chap. 9, this volume; Purvis et al., chap. 2, this volume). The elephant will endure for a maximum of almost 100 years-not 10 or 1000 years-no matter how well she is protected from predators, pathogens, the elements, malnourishment, poisons, and free radicals. Gestation length will show virtually no variation, and she will always give birth to a single, precocial infant, rather than litters of several small altricial ones. Life history traits are thus species-typical characters best defined as predispositions toward certain ranges of potential values among individuals in a given population (Roff 1992; Stearns 1992; Lee and Kappeler, chap. 3, this volume; Pereira and Leigh, chap. 7, this volume).
Variation in life history characteristics among mammals is enormous (Boyce 1988; Charnov 1991). A mouse is unlikely to live much beyond a year, almost two orders of magnitude less than the elephant, and some murid rodents have litters of ten or more, an order of magnitude greater than the elephants' singletons. Similar variation is found in the degree of development of young at birth, which varies from precocial to altricial (cf. Ricklefs and Starck 1998). Moreover, this interspecific variation in life history traits is not random; rather, life history characters are tightly intercorrelated across species (Portmann 1939; Eisenberg 1981; Harvey and Zammuto 1985; Harvey, Read, and Promislow 1989; Read and Harvey 1989; Charnov 1991; Harvey, Pagel, and Rees 1991), rendering a spectrum of life history "syndromes," from species with fast life histories (early maturation, large litters, short lives, etc.) to others with slow ones. Although larger animals inevitably tend toward slower life histories than smaller ones (Pagel and Harvey 1993), the size relationship is not entirely explanatory (Promislow and Harvey 1990). Significant variation in life history speed remains after controlling for size effects, especially in relation to grade shifts (see Purvis et al., chap. 2, this volume). Ultimately, particular life histories are considered to be adaptations to the rate of unavoidable mortality in the natural environment (Promislow and Harvey 1990; Charnov 1993; Harvey and Purvis 1999). How interspecific variability in traits defining life history rates is predictive of behavior remains to be examined in detail.
Primate Life Histories
Primate life histories are among the slowest among mammals (Harvey and Clutton-Brock 1985; Harvey, Martin, and Clutton-Brock 1987; Ross 1988; Charnov and Berrigan 1993; Lee 1996; Ross 1998). Primates' birth, growth, and death rates, in particular, are substantially lower than those of other mammals after controlling for differences in body size. Specifically, primates have relatively long gestation lengths, large neonates, low reproductive rates, slow postnatal growth rates, late ages at maturity, and long life spans in comparison to other mammals (Martin and MacLarnon 1988; Charnov 1991; Harvey and Nee 1991; Lee, Majluf, and Gordon 1991; Ross 1992a; Charnov and Berrigan 1993).
Whereas ultimate causes for the low developmental and reproductive rates of primates remain poorly understood (Charnov and Berrigan 1993), three main determinants have been suggested. First, the energetic costs of growing and maintaining primates' large brains have been suggested as constraints on these rates (Sacher and Staffeldt 1974; Sacher 1975; Armstrong 1983; Allman, McLaughlin, and Hakeem 1993a; Martin 1996). Theoretical objections and comparative data make this link unlikely, however (Harvey, Promislow, and Read 1989; Charnov and Berrigan 1993; but see modified view of Deaner, Barton, and van Schaik, chap. 10, this volume). Second, high juvenile mortality risk has been proposed as an ecological explanation for the comparatively slow growth of primates (Janson and van Schaik 1993), but the limited tests of this hypothesis to date are not consistently favorable (Ross and Jones 1999b; Godfrey et al., chap. 8, this volume). Finally, the arboreal lifestyle characterizing primates may have permitted the evolution of slow life histories (Eisenberg 1981; Martin 1995); recent tests both within primates and among mammalian orders do suggest a systematic link between arboreality and slow life histories (van Schaik and Deaner 2002).
The pronounced slow-fast continuum of life speed among mammalian orders is also found among primates. Small prosimians are sexually mature after less than one year of rapid growth, ultimately giving birth to two to four young once or twice annually, whereas great apes begin producing slow-growing singleton infants at four- to eight-year intervals after reaching seven to fourteen years of age (fig. 1.1). Such life history contrasts are pronounced between the prosimian and anthropoid grades and persist at lower taxonomic levels (e.g., among lemur and New World monkey families and genera: Harvey and Clutton-Brock 1985; Martin and MacLarnon 1985, 1988; Ross 1991; Kappeler 1995, 1996). Other traits more or less directly linked to life history variables, such as body size, brain size, metabolic rate, mode of infant care, habitat use, and diet, are also extremely diverse within the primate order (Leigh 1992c; Ross 1992a; Allman, McLaughlin, and Hakeem 1993a; Kappeler and Heymann 1996; Smith and Jungers 1997; Kappeler 1998a). This diversity in life history, in addition to their well-known diversity in social systems, makes primates an important taxon with which to examine relationships among life histories, ecologies and social behavior.
In sum, most primates have slow life histories, and thus long lives, and tend to produce, at long intervals, small litters of slow-growing young with long infant dependencies and also long juvenile periods of partial dependency. What relationships exist among these life history traits, ecological patterns, and social behavior?
Life History Effects on Socioecology
Life history traits should relate to social and ecological aspects of primate behavior in a variety of important ways. Progressing through the life cycle, we provide an overview of some demonstrated and potential links.
Prenatal and Postnatal Development
Durations of gestation and lactation among primates vary in duration between two and nine months and between two months and several years, respectively (Harvey, Martin, and Clutton-Brock 1987; Lee 1996). Maternal body size and litter size explain much, but not all, of this variation (Martin and MacLarnon 1985, 1988). The duration of postnatal maternal care is relatively difficult to quantify because weaning in primates is such a gradual process. Nonetheless, with appreciable variability within and among taxa, weaning appears generally to occur around the time when infants have reached about one-third of adult body mass (Lee, Majluf, and Gordon 1991; Lee 1996).
The relative lengths of prenatal and postnatal maternal investment have important consequences for behavior, especially for male reproductive strategies. Specifically, the ratio of lactation time to gestation time is a strong predictor of vulnerability to infanticide by males among eutherian mammals, including primates (van Schaik and Kappeler 1997; van Schaik 2000b), because females with relatively long lactations tend to undergo postpartum amenorrhea (i.e., lack postpartum estrus) to avoid concurrent gestation and lactation (van Schaik 2000b). Loss of an infant is unlikely to accelerate females' resumption of ovulatory cycling when lactation is brief relative to gestation. But when lactation is relatively long, infant loss generally brings females back into receptivity sooner, except in cases in which breeding is highly seasonal (van Schaik 2000a; cf. Jolly et al. 2000). Thus, males who have not sired current offspring but are in a good position to mate with females benefit from killing infants. Because weaning of primate infants occurs relatively late (Lee, Majluf, and Gordon 1991), primates have some of the highest lactation/gestation ratios among mammals and are therefore especially prone to sexually selected male infanticide (van Schaik 2000a), even in some taxa with seasonal reproduction (Jolly et al. 2000).
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Table of ContentsContents
Foreword Robert D. Martin....................xi
1 Primate Life Histories and Socioecology Peter M. Kappeler, Michael E. Pereira, and Carel P. van Schaik....................1
PART ONE Life History and Socioecology 2 Primate Life Histories and Phylogeny Andy Purvis, Andrea J. Webster, Paul-Michael Agapow, Kate E. Jones, and Nick J. B. Isaac....................25
3 Socioecological Correlates of Phenotypic Plasticity of Primate Life Histories Phyllis C. Lee and Peter M. Kappeler....................41
4 Matrix Models for Primate Life History Analysis Susan C. Alberts and Jeanne Altmann....................66
5 Puzzles, Predation, and Primates: Using Life History to Understand Selection Pressures Charles H. Janson....................103
6 Adaptations to Seasonality: Some Primate and Nonprimate Examples Jörg U. Ganzhorn, Susanne Klaus, Sylvia Ortmann, and Jutta Schmid....................132
PART TWO Development 7 Modes of Primate Development Michael E. Pereira and Steven R. Leigh....................149
8 Dental Development and Primate Life Histories Laurie R. Godfrey, Karen E. Samonds, William L. Jungers, and Michael R. Sutherland....................177
9 Human Life Histories: Primate Trade-offs, Grandmothering Socioecology, and the Fossil Record Kristen Hawkes, James F. O'Connell, and Nicholas G. Blurton Jones....................204
PART THREE Evolution of Primate Brains 10 Primate Brains and Life Histories: Renewing the Connection Robert O. Deaner, Robert A. Barton, and Carel P. van Schaik....................233
11 Life History, InfantCare Strategies, and Brain Size in Primates Caroline Ross....................266
12 Why Are Apes So Smart? Robin I. M. Dunbar....................285
PART FOUR Where Do We Go From Here? 13 Primate Life Histories and Future Research Stephen C. Stearns, Michael E. Pereira, and Peter M. Kappeler....................301
APPENDIX A Primate Life History Database....................313