American Jo u rn al of Primatology 37:143-175 (1995) Development and Social Dominance Among Group-Living Primates MICHAEL E. PEREIRA Duke University Primate Center, Durham, North Carolina Organisms are integrated systems whose physical and behavioral components codevelop and coevolve. Ontogenetic requirements in one domain are satisfied in part by prior or concurrent developments in another. This work explores how characteristic growth patterns in two primate groups interact with ecological, social, and other life-history constraints to promote the development of particular systems of agonistic relationship. First, the markedly size-dimorphic savanna baboons are contrasted with relatively nondimorphic macaques, where the pubertal growth capacity of males, relative to that of females, is comparatively modest. In baboons and other dimorphic Papionines, maturing males can be expected to invest more heavily in successful feeding competition, and known variation in the ontogeny of male-female dominance relations is well explained by this prediction. Data from five of the best-known species, for example, suggest that the female inclination to promote offspring dominance over male peers before puberty diminishes with increases in relative male size and growth potential a t puberty. Potential mechanisms for the development of this pattern are discussed. Next, ontogenies are considered for ringtailed lemurs, a highly social, monomorphic prosimian primate in which seasonal scheduling of growth causes a large proportion of adult size to be achieved before weaning. In this species, daughters invariably develop strong alliances with their mothers, and pubertal females must overturn adults in dominance to remain in large natal groups. Despite life-history parallels between ringtails and the focal Papionines, the lemurs do not collaborate agonistically in ways that ensure matrilineal “inheritance” of dominance status, as seen in the monkeys. Body weight and individual fighting ability appear to determine dominance relations among infants, and asymmetries established before weaning typically remain stable until sexual maturation. Anatomical and behavioral data suggest that low visual acuity prevents ringtailed lemurs from developing a system of agonistic intervention that could stabilize adult dominance hierarchies and mediate rank inheritance. In any case, failure to promote the dominance of close kin is argued to have influenced life-history evolution in ringtailed lemurs extensively, including aspects of growth, reproductive biology, and social structure. These analyses identify foci for future research and illus- Received for publication May 5, 1993; revision accepted September 19, 1994 Address reprint requests to Michael E. Pereira, Dept. of Biology, Bucknell University, Lewisburg, PA 17837. 0 1995 Wiley-Liss, Inc. 144 I Pereira trate the importance of bidirectional effects and feedback in the development and evolution of primate life histories and behavior. 0 1995 Wiley-Liss, Inc. Key words: primates, life history, development, growth, social dominance, social systems INTRODUCTION DEVELOPMENT AND BEHAVIOR If [we] were concerned only with the unsolved problems of biology, 90 per cent of [our attention] would be devoted to two topics: behaviour and development. In these fields, we are not even certain what kind of solution we are seeking. [Smith, 19861 The organism is a n integrated whole, genotype with phenotype . . . in t u r n part of a nexus of ecological and sociocultural relationships which extends from the past and into future generations. Development and evolution are therefore intimately connected. . . not separate as conceived within Neo-Darwinism. [Ho & Fox, 19881 There is no holding nature still and looking a t it [Whitehead, 19201. Life is a complicated phenomenon [sensu Salthe, 19851, and principals of development and behavior remain elusive. Individual organisms are integrated systems whose components comprise anatomy and physiology, including the hormonal and neurologic subsystems that exist in some species to help structure and guide behavior. Expression of the genome inherited a t conception firmly directs initial aspects of development, and some genetic variability among individuals is ultimately reflected in divergent life histories. Male vs. female ontogeny in any sexually reproducing species offers one compelling example. Natural selection can also foster genetic variability, or differential genetic expression, among members of one sex or populations of a species, when divergent life-history “strategies” maximize reproductive potential for different sets of individuals in particular environments [e.g., Etter 1989; Crow1 & Covich, 1990; Reznick et al., 1990; Shuster & Wade, 19911. Nevertheless, individual genes code only for proteins. Distinctive cell or tissue types are not represented a s such in the genetic code, let alone such things as fully developed pituitary glands or gonads or the developmental and behavioral processes influenced by their interaction. All such high-order phenotypic characters are the products of development: the inter-nested, self-organizing processes of organismic change and integration that occur, a t every level, across the life spans of individuals, groups, populations, and communities [Oyama, 1985; Ho, 19881. The very essence of development is responsiveness to the environment, and both environment and response can include influences of and on genetic expression. Understanding organismic development is paramount to progress in virtually every biological subdiscipline, and considerable work in many-including genetical ecology, systematics, and life-history theory-is devoted to the goal [e.g., Schlichting & Levin, 1986; Stearns & Koella, 1986; van Noordwijk et al., 1988; Reznick, 1990; Salthe, 1993; Hall, 19941. Across a n animal’s life span, its behavior mediates between its physiology and its environment in the broadest sense. Thus, behavior can be expected to play crucial roles in development. Animals modulate behavior to thermoregulate, to respond to caretakers, to disperse and identify conspecifics, to find and compete for resources, to avoid predators, and to care for offspring. Much behavior in each of these categories is heavily canalized: just as traditional taxonomy describes degrees of physical resemblance among classes of animal, so too behavioral repertoires have repeatedly been shown to distinguish phyletic groups [e.g., Struh- Development an d Dominance Among Primates I 145 saker, 1970; Huntingford & Turner, 1987; Macedonia & Stanger, in press; Pereira & Kappeler, in press]. This should not surprise, given that behavioral subsystems, within and between individuals, coevolve with associated physical subsystems. Ontogenetic requirements in each domain are met in part by prior and concurrent developments in the other. Examples to recall are many: bone and muscle must interact for either to develop normally [Gray, 19771; mammals denied patterned visual input early in life fail to maintain the neuroanatomy necessary to discriminate shapes visually [Thompson, 19751; and Hines  showed long ago how the intimate mother-infant relationship in primates depends initially on antecedent neurological developments underlying the infantile grasp reflex. Development and behavior, then, are crucial and reciprocally dependent elements of animal life histories, and, as life-history theory has developed, investigators of behavioral ecology in primates and other mammals have used it increasingly as a framework for their research [e.g., Altmann, 1980; Rubenstein, 1986; Bekoff et al., 1987; van Noordwijk et al., 19931. Because evolution is, a t its essence, the ecological control of development, and because no single-life-history feature better distinguishes primates among mammals than protracted development [Pereira & Fairbanks, 19931, a n important theoretical adjustment for upcoming years of behavioral primatology will be to recognize mating systems research as but one component of research on developmental systems. From this vantage, biologists begin to ask how aspects of physical and behavioral development interact and, a t another level, how developmental phenomena simultaneously structure and respond to systems of social behavior. These two questions lie at the heart of this paper, in which I provide overviews of development of adult body size (somatic growth) and of social dominance in separate primate groups and propose functional and specific causal relationships between these ontogenetic domains. The primates comprise two of the very few groups for which appreciably detailed information has become available on both developmental processes. On the one hand, I interpret data on macaques (Mucaca spp.) and savanna baboons (Papio cynocephalus subspp.), cercopithecid Anthropoids hereafter referred to as the Papionines (though few relevant data exist for other members of this tribe). On the other, I discuss ringtailed lemurs (Lemuridae: Lemur cuttu), a species behaviorally much unlike any other lemur and the most gregarious primate in the prosimian suborder. The work is neither a conventional review nor a traditional empirical report. It is meant to contribute by helping to relate work on primate behavior, including some on perception and cognition, more closely to the theoretical framework of life-history analysis and to relate life-history analysis to concepts of behavioral development. Readers should note a t this juncture that published information on growth and on development of dominance for even our focal taxa is substantially incomplete. No part of me, in presenting this work, means to imply that suggested interpretations are unassailably supported by existing data. To the contrary, missing data preclude not only extension of my analysis to closely related taxa but even satisfactory evaluation of ideas in relation to the focal species, undeniably among the best-described of all primates. As such, many of my interpretations are solely predictive or openly speculative. Most important, however, the two analyses together provide a basis from which the data most important to further evaluation of these and competing ideas can readily be targeted during future research on primate life history, development, and behavior. This paper does bring together information on some well-documented patterns of development, patterns that have been analyzed only separately before but need also to be cointerpreted. The analysis is facilitated by the fact that the focal groups 146 I Pereira share basic commonalities in life history, including certain close similarities in social behavior. Also, I have personally studied representatives of each ( M .fuscutu: 1977-1979; P. c. cynocephalus: 1980-1984; L . cattu: 1985-present [methods and more complete results in Pereira, 1986, 1988a,b, 1989, 1993b,c; Pereira & Weiss, 1991; Pereira & Kappeler, in press]). It lies beyond my present objective to provide any of the many missing data or to try to interpret all related phenomena (e.g., variation in papionine dimorphism). Rather, I seek to identify plausible relationships between characteristic patterns of growth and dominance development in two dominance-oriented groups of primates. In concluding, I attempt to show how primate social systems will only ever be fully understood through multifaceted analysis of individual development in relation to all aspects of life history. Primate Social Dominance, Development, and Assumptions Many group-living primates reliably develop species-typical systems of agonistic interaction that are organized around social dominance. In a dominance relationship, a subordinate individual employs a repertoire of submissive behavior to circumvent and allay aggression by a dominant groupmate [Bernstein, 19813. In species where dominance is frequently and unambiguously expressed-including all featured in this work-dominants unequivocally use their status and aggression to garner access to resources (e.g., food, mates, shelter), even to the extent of expropriating it from subordinates. While it is conceptually reasonable that one individual might dominate another in conflicts over only certain types of resources (e.g., food but not mates), this is not generally found to be true among nonhuman primates with salient dominance behavior. Instead, dominants in these taxa use their status and aggression in efforts to obtain all sorts of resources, whether or not it seems sensible to researchers! Primates exhibiting such dominance behavior are the only species to which all aspects of the present analysis could reasonably be applied. The first of three principal assumptions underlying this analysis is that dominance exists in our focal taxa because it can enhance for superiors access to resources and mitigate for inferiors rates and effects of aggression received, thereby promoting individual survival and reproductive success. These are not new or radical ideas [Allee, 1938; Tinbergen, 19531. Neither do they ignore important bodies of recent research showing that (1)alternative tactics enable subordinates to access resources (e.g., alliance formation), (2) particular demographic and ecological factors diminish the effectiveness of dominance (e.g., small, dispersed food), (3)primates often withhold their dominance (e.g., versus kin or “friends”), (4) different styles of dominance exist among even closely related taxa [Thierry, 1985; de Waal, 19891, and ( 5 ) many primates seem not to do dominance a t all [e.g., Rowell, 1988; Watts, 1994; Pereira & Kappeler, in press]. These factors all reduce the predictability of effects of agonistic asymmetries between primates and help keep primate agonistic relations an important and complex domain of scientific inquiry. None contradicts our first basic premise, however (see Harcourt 119871 and Silk [1993al on dominance and reproductive success and Barton and Whiten [19931 on dominance and feeding competition). Our remaining assumptions relate to the nature of development in primates. Mammals are considered juvenile from the time that they could survive the death of their caretaker until they mature sexually [Pereira, 1993al. From the viewpoint of evolution, with the principal objective of reproduction, juvenility should not exist a t all in a life history, whenever possible. Delay of maturation is often beneficial, however, in an animal’s effort to survive an interim harsh season or simply to maximize the resources available to sponsor growth [Pereira, 1993al. That re- Development and Dominance Among Primates / 147 sources must be allocated among maintenance, growth, and reproduction is a basic prediction of life-history theory that has received widespread empirical support in research on both plants and animals [Roff, 19921. Many anthropoid primates present an unusual pattern, however, in that many are moderately large but do not grow as fast as they are physiologically capable. Formerly, this slow growth was presumed to function in relation to the time primates needed to learn all that they seemed to have to learn, including the complexities of their social behavior [e.g., Poirier, 1972; cf. Schulz, 19691. Reviewing much recent research, Janson and van Schaik [19931 showed that, in fact, most learning seems largely accomplished long before maturation in primates. Other pivotal consequences of life in large social groups, they argued, are that immatures are sheltered from predation risk while they experience immediate disadvantages in feeding competition. Juvenile primates, the authors suggested, exploit the option of slow growth in their protected environment to safeguard themselves against high instantaneous risk of death due to malnourishment. Our second assumption, then, is that primates are inherently risk-averse throughout most of prereproductive development [Janson & van Schaik, 19931. As nonreproducers, juveniles can enhance their immediate fitness only by promoting their chances of survival. While certain behavioral adjustments may augment future fecundity, juvenile primates should favor survival over potentially improved futures whenever faced with conflicting options [e.g., van Noordwijk et al., 19931. Whenever dominance acquisition entails particularly risky agonistic conflict for immatures, therefore, it would be reasonable to infer that probability of survival is at stake. Primates do not differ from most other determinate growers in that they postpone reproduction until growth is essentially completed. Our third assumption, then, is that natural selection favors individuals that exploit opportunities to accelerate or maximize growth (Rubenstein  presents models). Following all three assumptions, we should expect immatures in focal taxa to act to maximize their dominance status within whatever constraints are imposed by existing social structure. Also, we should expect primate mothers to do whatever they can to help maximize offspring dominance. Other behavioral options that reliably offset the naturally low dominance status of juveniles should also be pursued (e.g., social association, support, and alliances) [Pereira, 1988a; van Noordwijk et al., 19931. Finally, if restricted time frames characteristically exist within the overall growth period during which dominance can markedly promote growth, due to discontinuities of growth effort Le., spurts), special effort in dominance acquisition should be timed to occur before or as they begin. In the absence of growth spurts, new efforts in dominance acquisition may occur in conjunction with other major life-history challenges (e.g., dispersal, group transfer, first reproduction). Focal Taxa and Sources of Data Among the Papionini, we consider the highly size-dimorphic savanna baboons (Papio cynocephalus subspp.), the relatively nondimorphic rhesus and Japanese macaques (Macaca mulatta; M . fuscata),and the moderately dimorphic longtailed and toque macaques (Macaca fascicularis; M . sinica). While these three groups of monkeys share pervasive similarity in life history and social system [Pereira, 1992; below], males differ in .their prereproductive development of dominance relations. I argue that divergent patterns of growth among these large Anthropoids determine the extent to which adult females attempt to control the dominance relations of immature males. The analysis recalls Jarman’s [ 19831 treatment for large herbivores, illustrating that species often attain a given degree of adult size 148 I Pereira dimorphism via disparate growth schedules and that species-typical growth profiles arguably interrelate adaptively with aspects of socioecology and mating system. We consider next the ringtailed lemur (Lemur catta), a prosimian primate sharing basic life-history features with the focal Papionini while also showing important differences. Comparative study of such sociobiologically similar but phyletically dissimilar species help us to identify potential cause-effect relations among aspects of behavior, development, and ecology. Both ringtailed lemurs and the focal Papionines form semiclosed,multimale-multifemale social groups among which mature males transfer [Jones, 1983; Pusey & Packer, 1987; Sussman, 19911. In each setting, agonistic relations among groupmates are mediated unambiguously by classical dominance relations [de Waal & Luttrell, 1985; Pereira & Kappeler, in press]. Mothers provide nearly all direct care for infants, including carriage across months of lactation [Klopfer & Klopfer, 1970; Altmann, 19801 and mother-daughter bonds intensify as females mature and seek to integrate themselves among the adults of their natal groups [Pereira & Altmann, 1985; Pereira, 1993c; Pereira & Kappeler, in press]. Unlike the monkeys, ringtailed lemurs have short mating seasons and very short, closely synchronized estrus periods [Jolly, 1966; Evans & Goy, 1968; Pereira, 1991; Sauther, 19911. In addition, ringtailed lemurs exhibit no body size dimorphism [Kappeler 1990a1, adult females invariably dominate males [Jolly, 1966; Kappeler, 1990b1, and dominance relations among members of a given sex are not always transitive [Pereira, 1993c;Pereira & Kappeler, in press]. Also crucial to our analysis is that ringtailed lemurs respond to annual photoperiodic cycles to schedule not only their reproduction but also their growth and other life-history adjustments seasonally [Pereira 1993bl. I suggest that environmental seasonality maintains a particular neuroethological constraint that prevents ringtailed lemurs from developing a system of rank inheritance like that of the Papionines, which in turn further augments the importance of rapid growth and direct struggles for dominance among infants in this species. To minimize disruptive citation throughout the essay, many principal articles on which it is based are cited here. Some data have long been available, such as some of those on dominance development [e.g., Kawamura, 1958; Koford, 1963; Sade, 1967; Cheney, 1977,1983; Lee & Oliver, 1979; Berman, 1980; Walters, 1980; Datta, 1983a,b,c; Netto & van Hooff, 19861 and weight growth in Papionine monkeys [van Wagenen & Catchpole, 1956; Mori, 1979; Sugiyama & Ohsawa, 1982; Coelho, 19851. Other information was published only more recently [e.g., Johnson, 1987, 1989; Turnquist & Kessler, 1989; Chapais, 1988, 1992; Chapais et al., 1991; Strum, 1991; Altmann et al., 1993; Chapais & Gauthier, 1993; Pereira, 1988a,b, l989,1992,1993b,c, 19941, and other data were heretofore unpublished (see figure legends and Acknowledgments), including many of my own. ACQUISITION OF DOMINANCE IN PAPIONINE MONKEYS Basic Patterns Most papionine females remain in their natal group for life, while the large majority of their male peers disperse after maturing and seek to establish residency in nearby social groups [Pusey & Packer, 19871. As adults, closely related females typically occupy adjacent ranks in their group’s hierarchy of dominance relations, individually and collectively dominating Zowborn females (of lowerranking matrilines) while being dominated by highborn females (of higher-ranking matrilines). Several studies have demonstrated stability for matrilineal dominance hierarchies exceeding a decade [reviewed by Pereira, 19921, stability so Development and Dominance Among Primates I 149 reliable, it appears, that females adjust offspring sex ratios in relation to their matrilineal status [van Schaik & Hrdy, 1991; see also de Waal, 19931. Whereas many young males probably transfer into groups containing brothers when possible, no standard, systematic effects of kinship on male dominance relations are known. Instead, adult males depend heavily on their size and independent agonistic prowess to acquire dominance [e.g., Hausfater, 1975; Sugiyama, 1976; van Noordwijk & van Schaik, 1988; Hamilton & Bulger, 1990; Sprague, 19921. Observational work on development revealed both expected similarities and unexplained differences between the dominance system of rhesus and Japanese macaques, which was studied first, and that of savanna baboons (Fig. 1). As in the macaques, male and female baboons came first to dominate particular age peers as infants, then overturned certain older immatures a s juveniles, and finally overturned certain adults only after having approached puberty. As in juvenile macaques of both sexes, juvenile female baboons outranked one another according to maternal rank and became dominant to only the lowborn among older females. By contrast, juvenile male baboons consistently outranked all female peers and outranked one another according to age or size, irrespective of matrilineal membership. In addition, young male baboons achieved dominance over older highborn as well as lowborn females, typically overturning even several highborn adult females well before puberty. Other immature Papionines, by contrast, were very rarely ever observed to contravene the aforementioned patterns by “overachieving” in rank acquisition. Exceedingly few females, for example, ever targeted older highborn females for rank reversal [Netto & van Hoof, 1986; Walters, 1980; Pereira, 1989, 1992; Chapais, 19921. Mechanisms Understanding ontogeny entails identifying mechanisms, and real progress has been achieved in this area for papionine rank acquisition and maintenance. Conjointly, field and laboratory work have emphasized the importance of social cognition and patterned adult female intervention into juveniles’ conflicts. In research on Amboseli baboons, for example, female intervention was differentiated by juvenile sex (Fig. 2). Relatively high-ranking females intervened relatively frequently in immature females’ conflicts with other females and invariably to support the highborn animal, juvenile or adult [Walters, 1980; Pereira, 19891. Those same adults, by contrast, intervened in young males’ conflicts infrequently and supported males without regard to rank relations between the matrilines of males and their opponents [Pereira, 1989; see also Netto & van Hooff, 19861. The systematic adult intervention into juvenile females’ conflicts both ensured and limited them to the acquisition of matrilineal dominance rank. The juvenile males, by contrast, were comparatively free to antagonize and ultimately dominate highborn females [Pereira, 19921. These results revealed that baboon females recognize not only the sex of juvenile individuals, but also their matrilineal membership and the relative dominance status of their matriline. They also suggested that systematic adult female agonistic intervention, according to existing dominance relations among matrilines, is the principal mechanism underlying the inheritence and stability of dominance rank for these female monkeys. Experiments with other Papionines in captivity confirmed and extended these interpretations. By having them distinguish pairs of photographs showing related vs unrelated groupmates, Dasser [19881 showed that female longtailed macaques ( M . fusciculuris) recognize allies within their groups. And, by removing and replacing related and unrelated sources of agonistic support, Chapais [19881 and colleagues [Chapais et al., 19911showed 150 I Pereira ADULT FEMALES i 7 @ 2 8 m 5 418217 ID4 JUVENILES 2 @ 6 6 birth order Rhesus /Japanese Macaques mo Ihe r ‘s rank 0 1 birlh order Savanna Baboons Fig. 1. Schematic illustration of papionine species differences in juvenile dominance relations. Males are represented by squares, females by circles. Matriarchs have double-letter acronyms, and their daughters’ numbers indicate birth order; three-character acronyms identify matriarchs’ grandoffspring. Adult females invariably outrank all young juveniles in dyadic interactions. Juvenile male and female rhesus and Japanese macaques outrank one another according to maternal rank, whereas juvenile male baboons outrank all female peers and outrank one another according to age. that the inheritance and maintenance of matrilineal dominance rank in female Japanese macaques depends on the hierarchy-reinforcing patterns of intervention that characteristically occur among them. More recently, these researchers detailed how Japanese monkeys first experience systematic adult female intervention long before weaning [on other spp. see Berman, 1980; Datta, 1983a,c;Horrocks & Hunte, 19831 and showed that infants learn to behave dominantly toward lowborn groupmates partly by observing their mothers do so [Chapais & Gauthier, 19931. Our interpretation of all of these studies is corroborated by the common observation of persistently unstable dominance relations among unrelated adult females in artificially composed groups of captive macaques. Given the great similarities in life history and social structure between Development a n d Dominance Among Primates / 151 T i % Interventions Reinforcing Hierarchy Fig. 2. Pattern of adult female intervention in agonistic interactions ofjuvenile male (top) and female (bottom) savanna baboons. Bars indicate, in relation to sex of opponent, percentages of support to juveniles that reinforced existing hierarchy of dominance relations among matrilines. macaques and savanna baboons, observed differences in the ontogeny of male dominance relations offer a n opportunity to explore relationships between the development of primate individuals and that of their social systems. Heretofore, well-justified focus on female development led to relative neglect of issues surrounding male development. One perspective that emerged was that adult females can be expected to be less involved in young males’ rank relations because males are destined to disperse [Pereira, 1989; Lee & Johnson, 19921. Successful development, however, is a t least as important to sons as to daughters across the years preceding their dispersal, and existing data suggest that adult female macaques do promote matrilineal rank acquisition by juvenile males. Why then do female baboons promote rank acquisition only for females against other females? Why do immature male baboons invariably dominate their female peers? And why do they relatively easily come to outrank even highborn adult females? My attempt to provide answers to these questions begins with a n examination of papionine size dimorphism and the manner in which it develops. G r o w t h patterns and adult agonistic relations. Anthropoid primates schedule growth and achieve size dimorphism differently than do most other animals. Virtually all nonprimate endotherms exhibit maximal growth rates shortly after birth and progressive decline in growth rate beginning around the time of sexual maturation [Brody, 1945; Pereira, 1993al. In size-dimorphic species, members of the larger sex are typically somewhat larger at birth and grow faster postnatally than those of the other [e.g., Jarman, 1983; Ricklefs, 1983; McLaren, 19931. In large anthropoids, by contrast, growth rates decline after rapid neonatal growth and remain suppressed until puberty, when the males in most species and females in some show a disinhibition termed the “adolescent growth spurt” [Watts, 1985, 1986; Leigh, 19921. Large samples of neonatal or juvenile weight data typically reveal the average male to be slightly heavier than his average female counterpart, but these differences are exceedingly small and accompanied by great variability. 152 J Pereira Two important points emerge here. First, immature papionine females are slightly larger or smaller than individual male peers in any given social group as a result of their birth dates. Second, juvenile males and females remain much smaller than adults for years. It is also likely that juvenile nutritive requirements are considerably smaller than those of reproducing females, due to both size differences and the relatively small energetic allocations juvenile Anthropoids make toward growth [Janson & van Schaik, 19931. Considering these factors alone, we likely explain why cercopithecine adults, male and female, dominate all young juveniles on independent bases (i.e., apart from third-party effects; Fig. 1). Following puberty, male rhesus and Japanese macaques in the best-known free-ranging populations outweigh females by 15-30%, on average. By contrast, mature male savanna baboons typically weigh 80-100% more than do adult females. Associated with this difference are significant contrasts in adult social relations. The adult female macaques, for example, readily collaborate to attack adult males. Moreover, some females independently dominate some adult males, and high-ranking females can influence male dominance status and group membership [reviews by Smuts, 1987; Pereira, 19921. In contrast, agonistic coalitions by adult female baboons against males are rare and ineffective [Packer & Pusey, 19791, adult male baboons invariably dominate individual females, and there s no known effect of maternal rank on the dominance relations, migration patternj, or reproductive success of male baboons [Altmann et al., 19881. In sum, compared to their macaque counterparts, adult male baboons are so large a s to be agonistically unassailable from the viewpoint of adult females, whereas this taxonomic difference is not manifest among juveniles, where females are as large a s males, regardless of species, and all are smaller than adult females. Large juvenile male size, then, cannot explain taxonomic differences in the development of males’ dominance relations [cf. Lee & Johnson, 19921. On purely physical grounds, young juvenile male baboons are as easy for adult females to coerce and socialize as are young juvenile male macaques. Pubertal development and prior female control of juvenile males. Female primates should promote offspring dominance whenever feasible to help maximize offspring access to nutriment during difficult foraging periods and, especially, critical growth periods. In the relatively nondimorphic species, mothers can and do help sons and daughters alike to dominate lowborn male and female peers, thereby maximizing their chances for survival, extensive growth, and early reproduction [e.g., Drickamer, 1974; Paul & Thommen, 1984; see also Rubenstein, 19931. In baboons, by contrast, adult females support neither sons nor daughters over lowborn male peers. This, I suggest, is because the required agonistic interventions are too risky for these adult females when they matter most, just before and a t puberty. The dramatic pubertal growth spurt in baboons can generate a doubling of male body weight in just over 2 years, whereas pubertal female baboons show little to no acceleration of weight growth. In rhesus and Japanese macaques, by contrast, the substantial male growth spurt is paralleled by a more moderate pubertal acceleration of female growth, such that average sex differences in adult weight are comparatively modest. The growth capacity of maturing male baboons, therefore, exceeds that of their macaque counterparts relative to the nutritive requirements of conspecific females. All else equal, maturing male baboons should comPete more aggressively, against peers and adult females, over access to food. Inadequate nutrition could jeopardize their health and reduce adult body size, compromising their potential for long and effective reproductive careers. Even if Development an d Dominance Among Primates / 153 growth can be postponed in response to nutritive shortage, age at first reproduction would be compromised [Hamilton & Bulger, 19901. Direct comparison of papionine growth trajectories, in fact, suggests several related factors that should encourage and help maturing male baboons to compete relatively aggressively against females (Fig. 3). Along with the near absence of a female growth spurt, males in this species attain a much larger proportion of adult female size before initiating their spurt (-82%) than do male rhesus ( - G O % ) , increasing for them the viability of aggressive tactics a s puberty approaches. Also, the potential for continued growth after puberty seems reduced for both sexes in baboons in comparison to macaques [see also Leigh, 19921. Two predictions deserving attention in future research, then, are that successful foraging is more important, and aggressive competitive tactics more prominent, in maturing male baboons than in their rhesus or Japanese macaque counterparts. In my own research, food was at stake in most juvenile male but not female aggression toward unrelated peers and adult females, and males were five times more likely than females to use contact forms of aggression [Pereira, 1988bl. Now, most macaques breed seasonally, while most baboons do not [Lindberg, 19871. If seasonality exacerbates feeding competition among mothers or their weanlings [e.g., Wasser & Starling, 19881, females might be favored that maintain as much agonistic influence over males as possible [Jolly, 19841. “Male dominance” among juveniles in the most dimorphic seasonally breeding Papionines, however (Fig. 41, suggests that growth patterns, not environmental seasonality, primarily determine the degree to which females constrain juvenile male dominance relations [on Barbary macaques, M. syZuunus, see Kuester & Paul, 19881. This may also hold among Cercopithecini, where DeBrazza’s monkey (Cercopithecus neglectus), the most dimorphic guenon, may show general male dominance among juveniles [preliminary data in Kirkevold & Crockett, 19871, whereas the less dimorphic vervet monkeys ( C . uethiops) exhibit the rhesus/Japanese macaque pattern of matrilineally ordered dominance relations among all juveniles [Cheney, 1983; Horrocks & Hunte, 1983; see also Cheney, 1977 on the relatively nondimorphic chacma baboons, Pupio c. ursinusl. Females in cercopithecine taxa showing relatively great adult size dimorphism, then, appear not to help daughters maintain dominance over lowborn male peers, and, in the extreme case of savanna baboons, neither do they assist sons. The most dimorphic macaques constitute cases of intermediate papionine size dimorphism, and mothers in these species appear to provide intermediate levels of assistance: static data (Fig. 4) suggest that they help primarily sons maintain dominance over lowborn male peers. Our uncertainties here are due to the fact that all of the crucial types of data on adult intervention into juvenile conflicts-classified by not only matrilineal membership, but also sex and role ofjuvenile and opponent and type of intervention and response [discussion in Pereira, 19921-have not been published for macaques of any kind [for a variety of other detail on intervention behavior see Datta, 1983a,b,c; Bernstein & Ehardt, 1985; Netto & van Hoof, 1986; Chapais, 1988; Chapais et al., 19911. A simple algebraic model accounts simultaneously for effects of pubertal male size and potential for growth relative to females: Here, female agonistic effort to control juvenile male dominance behavior, Cf, relates inversely to the product of relative male size a s the growth spurt begins, S , (proportion of adult female size), and potential for male growth during puberty, G, Rhesus Macaques -- / - I I I h M e. Longtailed Macaques 7- 74% increase a4 .- Be 3 2 2 3 I 0 25 1 2 3 5 A - I I 4 6 / n 7 8 7 8 I M c 20 9 C 10 5 0' -. 0 I 1 2 3 4 1 5 6 Age (yeam) Fig. 3. Patterns of growth in Papionines showing relatively slight (top),moderate (middle), and great (bottom) adult size dimorphism. Infants are weaned in each taxon around or before 1 year of age. Beginnings and ends of pubertal male growth spurts were taken directly from associated growth velocity curves in each original dataset [rhesus: van Wagenen & Catchpole, 1956; longtails: van Schaik e t al., unpublished data; see also Janson & van Schaik, 1993; baboons: Coelho, 19851. Using data from captive, provisioned representatives of each species allows comparison of maximal male growth capacities. S, highlights proportions of prime adult female weights comprising male weights a t outsets of pubertal growth spurts (see text). G, for each taxon is proportion of male size increase divided by duration of growth spurt (e.g., rhesus: 1.0712.3). Development and Dominance Among Primates I 155 4 yr-olds 3 yr-olds . Timsel Group uE Group A Group D Fig. 4. Juvenile dominance relations in two relatively dimorphic macaque species (adult maldfemale weight ratio approximately 1.50).Timsel Group of longtailed macaques (M. fascicularis, Sumatra) [van Noordwijk, unpublished data]. Groups A and D of toque macaques (M. sinica, Sri Lanka) [Baker, unpublished data; also Baker-Dittus, 19851. Juveniles' matrilineal ranks shown in symbols; individual identities in subscript. Threeyear-old male longtail KL dominated both four-year-oldsin his group. (maximal proportion of size increase divided by duration of spurt). This model renders predictions on physical or behavioral development for any macaque or savanna baboon population, including any of our focal taxa characterized by different degrees of prime adult weight dimorphism from those cited here (without obesity; see Pereira and Pond [19951 on variable tendencies toward obesity within primate genera). Taking data from Figure 3, for example, the index predicts relatively great female control of juvenile male rhesus macaques (Cf -4.51, relatively low female control of young male baboons (Cf -3.11, and intermediate female control of young male longtailed macaques (Cf -4.0) [for cross-sectional cumulative weight growth data in M. sinica see Cheverud et al., 19921. Current knowledge suggests that when the relative size and growth capacity of pubertal males reduce this index toward the baboon value, adult females operating in a multimale papionine social system stop trying to control the ontogeny of male dominance relations altogether. Canalized cognition of sex-typical behavioral attributes? Papionine females' perspectives on agonistic interaction with mature males clearly vary in accord with species-typical dimorphism and schedules for its development. These are taxonomic differences in social cognition-female cognition of males and their agonistic attributes, presumably complemented by differences in male cognition (e.g., below). An intriguing question that remains asks what mechanisms underlie the development of taxonomic differences in the sexes' perceptions of themselves and one another. I argue, for example, that male baboons' great pubertal size and growth are paired functionally with great motivation to outcompete others for food and that females who try to compete with maturing males more often incur injuries than females doing so in less dimorphic taxa. This alone could cause female baboons to develop a disinclination to fight with mature males. But what causes baboon females not to fight with juvenile males? Three datasets suggest that female baboons may have somewhow evolved a general disinclination to interact aggressively with males. First, baboon mothers do not assist even young juvenile offspring in dominating male peers. One might argue that this 156 I Pereira simply reflects that dominance among juveniles functions not to mediate resource access, but rather to establish precedents in relations that become important around maturation. This inference is, in fact, supported by both the seeming lack of immediate cause for many juvenile conflicts [Pereira, 1988b; Johnson, 19891 and the new theoretical perspective on slow anthropoid growth [Janson & van Schaik, 19931. On the other hand, mothers assist all or some offspring to dominate male peers in all other well-known Papionines, and other data considered in this work also support the prediction that female primates typically help to maximize offspring dominance. Second, in all relevant data reported to date, juvenile males’ efforts to overturn adult female baboons in dominance are found to have been resisted only weakly in comparison to those of juvenile females. Indeed, amusing sights during my own fieldwork involved several relationships in which tiny 2-year-old males independently elicited submissive signals from much larger mature females. Finally, in all research examining juvenile male-female relations in highly dimorphic baboon populations, females have ceded dominance to males of roughly the same size [cf., Cheney, 1977 on Pupio c. ursinus].This has occurred almost invariably despite the facts that immature female baboons are not systematically punished by adults for fighting with young males [Pereira, 19891, many actually exceed particular male peers noticeably in size, and many are members of higher-ranking families [e.g., Pereira, 1988bl. The consistency of these observations, among age classes and study sites, suggests that female baboons perceive males per se as inappropriate targets for solo agression and that this perception is stabilized remarkably early in life. The mechanism may lie instead with male behavior. Males in dimorphic species might have evolved an orientation toward forming agonistic alliances with one another, for example, because females cannot safely assist them in fights with other males. In Amboseli, juvenile males received agonistic support as often as did juvenile females, and their support came predominantly from male peers and older immature males [Pereira, 19891. Also, adult male coalitions are a prominent feature of savanna baboon natural history; data on them outstrip those on any other coalitions among unrelated primates [Noe, 19921. Far fewer data on male-male coalitions have accumulated, by contrast, in the voluminous literature on rhesus and Japanese macaques [e.g., Watanabe, 1979; Bernstein & Ehardt, 1985; Sprague, 19921, whereas the other Papionine well known for intragroup male-male alliances is one of the more dimorphic macaques (bonnets, M.rudiutu) [Silk 1993bl. Of course, both things may be true: male baboons might be predisposed to form agonistic coalitions, while female baboons are naturally inclined not to fight with males. But also a less adaptationist developmental cascade remains equally viable. All developing cercopithecine males exhibit some social affinity [Fairbanks, 19931, In baboons, young males’ older associates are unusually formidable allies, as discussed earlier. Female baboons may simply learn early on that conflict with even one young juvenile male often leads to an undesirable tangle with one or more much rougher ones. As these females learn consequently not to fight with males, males learn that it is easy to harass and out-compete females, especially when acting together. This hypothetical ontogenetic cascade posits for baboons neither evolved female predispositions to avoid conflicts with males, nor unique male predispositions to collaborate. It remains one, however, that, in conjunction with common patterns of association and species-typical patterns of growth, could promote cognition of sex-typical agonistic capacities that is taxonomically extreme. Male and female perceptions of one another throughout development would stabilize observed adult Development and Dominance Among Primates I 157 modes of male-female interaction, which in tu rn would promote parallel sex-typical behavior among immatures. We should continue to respect the possibility that all three mechanisms discussed have, in fact, come into play over evolutionary time, providing the mechanistic redundancy characteristic of integrated life history traits. Before dismissing out of hand possible roles for predispositions in agonistic relations between the sexes, one should reflect on accumulating data regarding the evolution and development of “female dominance” in ringtailed lemurs. ACQUISITION OF DOMINANCE IN RINGTAILED LEMURS We t ur n now to ringtailed lemurs (Lemur catta), the prosimian primate for which several aspects of life history, including social structure, most closely resemble those in the papionine taxa (see Introduction). The following overview combines heretofore unpublished data with others recently presented elsewhere [Pereira, 1993b,cl. Basic Patterns Adult and adolescent ringtailed lemurs invariably dominate all younger group members, and all juveniles dominate all infants [Pereira, 1993c, 19941. In my 9 years of research at the Duke University Primate Center (DUPC), infant ringtailed lemurs have invariably established dominance relations among themselves by 4-5 months of age, 1-3 months before weaning (data from 16 cohorts). Also, birth peers’ dominance relations have always been transitive and completely stable, barring illness, until maturation. Infants generally outranked their lighter peers [Pereira, 1993~1,and neither infant sex nor small age differences (<3 weeks) nor maternal weight o r dominance status affected either weanling weight or dominance rank. Large age differences, however (>3 weeks), invariably did: infants conceived during second or later sets of estrous cycles during mating seasons [see Pereira, 19911consistently have the lowest weaning weights and dominance ranks in their cohorts. Eight of nine such youngsters born before 1992 showed belowmedian body weights and dominance ranks in their cohorts by puberty. Puberty in ringtails occurs around 15 months of age at the DUPC and around 26 months at Berenty, as evidenced by testicular enlargement and the onset of genital scent-marking [Jones, unpublished data; Pereira, unpublished data]. At both study sites, dominance relations changed around puberty, both among adolescents and between adolescents and adults [Pereira, 1993c, 19941. The invariant ringtailed lemur phenomenon of mature female dominance over all males began to emerge gradually a t this time, and adolescents’ agonistic relations with adult females also differentiated: only maturing females were included in the seasonal phenomenon of targeted aggression. During premating and birth seasons, mature and maturing females in the DUPC and Berenty populations spontaneously target female adversaries for persistent, intense aggression that can result in dominance reversal, infanticide, and/or social eviction Wick & Pereira, 1989; Koyama, 1991; Pereira, 1993c, 1994; Pereira & Kappeler, in press]. Mechanisms Adult female intervention in immatures’ conflicts. Since the dominance relations of immature ringtailed lemurs do not correlate with maternal attributes and rarely change before puberty, juvenile ringtailed lemurs do not systematically “inherit” dominance as do juvenile papionine monkeys [Pereira, 1993~1.Quantitative behavioral observation corroborated that adult female ringtails make no patterned effort to influence the dominance relations of offspring. In my initial 15 158 I Pereira Fig. 5. Adult female intervention in conflicts of juvenile and adolescent ringtailed lemurs consistently promoted neither inheritance of maternal dominance status (top four bars) or female dominance over males (bottom bar). All interventive aggression was moderate to severe (i.e., caused victims to jump away or flee). Top bar: Maternal intervention vs. age peers. Second bar: Maternal vs. adult females. Middle bar: Nonkin intervention vs. all opponents. Fourth bar: Nonkin intervention into only immature females' fights, against all opponents. Bottom bar: All adult female intervention between females and males. month study, for example, only eight of 26 immature subjects ever received maternal support against peers, and six of these eight received such support only once [Pereira, 1993~1.In addition, maternal aggressors dominated their offsprings' opponents' mothers in only 50% of interventions (Fig. 5). Moreover, immatures never responded to maternal support by rejoining to coattack their former aggressor, which is a crucial aspect of rank acquisition for Papionines [e.g., de Waal, 1977; Walters, 1980; Pereira, 19891. Finally, agonistic intervention by nonkin females also was not patterned in ways that could have promoted either inheritance of maternal dominance status or the development of female dominance in this species (Fig. 5). In spring 1994, a long-term bottom-ranking adult female in one study group overturned the matriarch and all three of her adult daughters, providing dramatic testimony to the fact that female ringtails do not act to promote or secure the dominance of kin. Competition for dominance among infants. In most dyads, dominance relations appeared to be settled through experience in rough-and-tumble play, as this was virtually the sole mode of nonfilial social initiative exhibited by infants [also Gould, 19901. But also, intense grappling commonly erupted spontaneously between 3-month-old infants that were very closely matched in age or size (Table I), and grapples never occurred between infants more than 40 days apart in age. Most grapples broke out during wrestling play rather than foraging, and all sent combatants to the ground, where they bit each other violently about the head and shoulders and raked one another with their feet. When nearby adult females noticed grapples, they typically charged any noninfant within about 5 m (n = 14). More rarely (n = 51, females (n = 3) attempted to intervene, but, none was ever aggressive toward either grappler. Each nonalpha female that attempted to intervene (one/group) was attacked immediately by a dominant female. Grappling clearly established dominance relations (Table I). In many pairs, two or more grapples have been observed over a 1-2 week period. Clear winners Development and Dominance Among Primates / 159 TABLE I. Relative Age Differences and Ultimate Dominance Rank Differences Between Grappling Infant Ringtailed Lemurs Rank differences 1 Relative age difference” Dominance rank difference at weaning 2 3 4 5 1 4 4 1 1 1 1 2 4 0 0 0 “Infants of each cohort ranked by age; grapplers’ differences in age rank shown; whereas similarities in weight may have exceeded similarities in age [Pereira, 1993~1,birth cohorts could rarely be weighed close to days of grapples. (n = 8 before 1993)remained a t conflict sites, taking over no resource, while their opponents ran to their mothers [also Pereira, unpublished data]. During subsequent play or conflict over food or partners, grapple winners readily intimidated former opponents, eliciting the species’ vocal signal of subordination (“spat” call [Pereira & Kappeler, in press]). In almost all cases, grapplers subsequently occupied adjacent dominance ranks (Table 1)[Pereira, unpublished data]. Changes at puberty and targeted aggression. In every year of my research, fully mature adults have been the first males seen to issue submissive signals to maturing females, always before mating began and almost invariably in the absence of female aggression (1985-1994). Females’ dominant male peers, by contrast, have typically become submissive only by the end of pubertal mating seasons. Thus, female sexual maturation seems to induce a change in mature males’ perception of young females, leading males spontaneously to behave submissively to them. We have suggested evolution via sexual selection [Pereira et al., 1990; Pereira, 1991; Pereira & Weiss, 19911, with females accepting only submissive males as mates, thereby ensuring their own access to food in a harshly seasonal, semiarid environment. Female dominance in ringtailed lemurs, in that case, would reside in mature male neurophysiology. Irrefutably, males do not feel compelled to submit unconditionally to female peers until they fully mature themselves [Pereira, 1993~1. One or more females in four of five adolescent cohorts in my initial study of ringtailed behavioral development were selected by adults for targeted aggression, and long-term data showed that maturing females had to overturn some adult females in dominance t o remain in large or growing natal groups [Pereira, 1993~1. Maturing females received agonistic support primarily from their mothers (Fig. 5) and also significantly increased their own rates of intervention in adult female conflicts (Fig. 6). Unexpectedly, however, no evidence suggested that mature females sought actively to influence the dominance relations of kin. Maternal intervention was not only rare (mean: 0.6%of all conflicts), it was also unpatterned in relation to maternal dominance relations (Fig. 5). In addition, neither juvenile nor maturing females showed greater anticipation of maternal support than did male peers. Despite receiving more adult aggression, for example, adolescent females took no greater responsibility than did their male peers for time spent near their mothers, and only young juveniles-male and female alike-markedly increased rates of filial approach in response to adult female aggression [Pereira, 1993~1.Finally, following seasons for targeted aggression and their associated rank reversals, ringtailed mothers and their mature daughters often did not dominate the same sets of female groupmates (Fig. 7). 160 I Pereira males " ..... "" juvenile adolescents Age Class Fig. 6 . Ontogeny of agonistic intervention in immature male and female ringtailed lemurs. At puberty, females radically increase their rates o f intervention in adult female conflicts, while males continue to intervene in others' fights only rarely. Seasonality, synchrony, growth, dominance, and aggression. Lemur rates and scheduling of growth contrast sharply with known anthropoid phenomena [Kirkwood, 1985; Kappeler, 1992; Pereira, 1993bl. Though their mothers were a n order of magnitude smaller than most papionine females, for example, infant ringtails grew as fast or faster than do infant Papionines, gaining 4-8 g of body weight per day, on average, across their first 7 months [Pereira, 1993bl. Thus, the ringtailed infants attained about 35% of average adult weight by weaning, whereas infant Papionines achieve only about 25% of adult female weight by weaning (Fig. 3) and take at least twice a s long to do so. After the first half of lactation (0-3 months), ringtailed infants entered a 4-5 month period, extending beyond weaning (approximately 6 months of age), during which growth rates remained high (moderate provisioning: X = 4.6glday; n = 10) or accelerated (heavy provisioning: X = 7.5 glday; n = 5; F = 9.19, P < 0.01). Next, around their eighth month, juveniles invariably exhibited sudden, substantial reductions in growth rate (65-75%), regardless of provisioning level, and growth remained suppressed for the next 5-7 months [Pereira, 1993bl. Twelve months after youngsters' first summer of rapid growth, 15-20-month-old immatures matured sexually and experienced 3-4 consecutive months of elevated growth rate. These and other data [Pereira, 1993bl revealed basic photoperiodic control of growth rate, and possibly also social behavior, in relation to predictable seasonality of nutrition in the wild. Very high rates of growth occurred opportunistically during and just after the photoperiod of the rainy season in southern Madagascar (Fig. 8). All grapples to establish dominance relations were observed a t the outset of this period, beginning just after the summer solstice, when infants began helping to sponsor their own rapid growth (Fig. 9). Growth rates were invariably suppressed thereafter across most of the photoperiod of the southern harsh season. Campaigns of targeted aggression were also abandoned at this time, each year Development a n d Dominance Among Primates / 161 0 n Lcl @a @ Group Lc2 Group T Group a Fig. 7. Stable, intransitive dominance relations among mature females in three study groups of ringtailed lemurs. Lcl and Lc2 groups a t DUPC (1989-1990); T group at Berenty Reserve (1992). In each case, females dominated all those listed beneath them for several consecutive months, except where upward arrows show low-rankers that stably dominated otherwise topranking female (see Fig. 1for acronym scheme). Each subscript a identifies adolescent female; each subscript y indicates individual independently estimated to be youngest among mature females (by author and two other fieldworkers). Numbers to left of T group identify three cliques, as defined by mutualistic association and grooming patterns. In Lcl and Lc2 groups, such cliques include all motherdaughter pairs. when female adversaries had failed to evict one another [Vick & Pereira, 1989; Pereira, 1993~1. Physical and behavioral development in ringtailed lemurs have coevolved in a social context in which adult females reliably fail to intervene to determine the outcomes of immatures’ conflicts. Thus, infant ringtails seem to grow fast to become dominant to continue growing fast, before markedly reducing growth effort and engaging their first long harsh season. Rates of growth and probably metabolism [Pereira 199313, 19941 are inevitably substantially suppressed for most of their dry season. By maximizing size, youngsters maximize their capacities in foraging, competition, and fat storage, which conjointly help to minimize risk of dry season mortality [Pereira 1993a,b; Pereira & Pond, 19951. The paramount importance of extensive infantile growth is corroborated firmly by the accelerated and extended growth characteristic of late-born infants. Growth rates of semiindependent late-born infants exceeded those of older infants in 7 of 8 months prior to autumnal reductions (Septembers and Octobers, excluding October, 1993), and in 9 of 10 months following reductions (Table 11) (rapid growth one month is typically followed by relatively slow growth the next, so it is conservative to treat consecutive months as independent data points in these comparisons). Analysis of effects of age vs. size using an entire 6 year database revealed that it is small size, not young age, that delays the reduction of growth rates in the autumn [Pereira, 1993131. Relationships among infant growth rate, dominance, and survivability have probably influenced life-history evolution in ringtailed lemurs. While mating seasons in many group-living primates are well defined, for example, few are so sharply delineated a s those of ringtailed lemurs, where female groupmates typically all conceive within 7-20 days of one another [Jolly, 1966; Pereira, 1991; Sauther, 19911. I propose that reproductive synchrony among female ringtailed 162 i Pereira 10 FE WS SE F E W 120 - 6 4 l l 4 l - T 1 2 3 4 5 6 Month of Life Fig. 8. Mean growth velocities across the first 2 years of life, under high provisioning (solid line) and moderate provisioning (dashed line), for infants whose births were clustered between the end of March and April. Solstices, equinoxes, and sample sizes indicated. Mean monthly rainfall values for the same photoperiods in southern Madagascar (dotted line). lemurs functions to rule out insurmountable size advantages among neonates about to race for the size needed to convey dominance [for detailed analogy on rate of embryonic development, hatching synchrony, and nestling competition in birds see Ricklefs, 19931. In turn, birth synchrony feeds back to reinforce the developmental patterns of frequent rough play and agonistic grappling, as necessary, among infants to establish dominance relations. Size differences around weaning should have far-reaching effects among healthy survivors because immatures’ dominance relations typically remain stable and should affect development continuously. Maturation rates on three “planes” of nutrition predict that dominant juveniles mature faster. Provisioning enhances development at the DUPC [Pereira, 1993b1, where almost all females bear their first infant a t 2 years of age. At Berenty, by contrast, only a few females produce their first infant at the age of 2 years [Jolly & Koyama, personal communication], and, on still lower nutrition at Beza-Mahafaly, some 3-year-olds fail to produce their first infant [Sussman, 1991; Sauther, 19921. By enhancing growth and nutrition, dominance may also help juveniles to develop superior agonistic capacity by puberty. In large Duke study groups, only females that overturn adult females in dominance secure reproductive positions [Pereira, 1993~1.Whereas maturing males are not involved in targeted aggression, they disperse and must overcome intense aggression by males resident in other groups before successfully immigrating [Sussman, 1991; Pereira & Weiss, 19911. Development an d Dominance Among Primates / 163 I 0No.Grapples -A- Growth Rate - Time Feeding 1 Fig. 9. Codevelopment of growth rate, self-feeding, and agonistic relations in infant ringtailed lemurs. Juxtaposition of timing of grapples (n = 27, 1981-19901, average infantile growth rate (1986-1992), and mean percentage time spent feeding (seven 1992 infants). As infants begin to contribute significantly to their own nourishment, rates of growth often first decline, then accelerate IPereira, 1993b1, and intense mutual aggression commonly erupts during play between infants that are very closely matched in size (see also Table I). Why No R a n k Acquisition? Especially on seasonal bases, female ringtails commonly intervene in others’ fights, and, in so doing, they sometimes shield kin from aggression. But, overall, characteristic patterns of intervention seem to represent principally individual opportunism, each female essaying to overturn, harass, and potentially evict her own adversaries [Pereira, 1993c; Pereira & Kappeler, in press]. Why do female ringtailed lemurs not genuinely collaborate to promote kin and stabilize hierarchical relations? By doing so, powerful females could help their matrilines dominate others, grow larger [Taylor, 1986; Vick & Pereira, 19891, and maintain their ranges [Koyama, 19911, thereby enhancing reproductive success. So reasoning, in fact, I predicted at the outset of my research that female ringtails would show the same patterns of intervention as do papionine females. Especially given the mutualistic advantages of the papionine system [Chapais, 1992; Pereira, 19921, I continue to believe that female ringtailed lemurs would effect “top-down” agonistic intervention, if they could. Why can’t they? To do so, females must be able to recognize group mates visually, identify allied subgroups (e.g., mother-daughter pairs), and remember the directionality of dominance between them. Forest-living ringtailed lemurs present abundant evidence of visual recognition daily, including female targeting of specific adversaries and male repulsion of potential immigrants [Pereira & Weiss, 1991; Pereira, 1993~1.During many episodes, however, I have also seen aggressors err, sprinting to attack and suddenly stopping after starting toward the wrong animal (Table 111) [Pereira, unpublished data]. Almost invariably, mistaken 164 I Pereira TABLE 11. Autumnal Growth Rates of Clustered and Individual Late-Born infant Ringtailed Lemurs* Birth date” September October November December 7.00 6.20 (1.66) [31 9.90 5.83 (2.33) 161 4.10 1.34 (1.72) 171 3.90 2.94 (0.89) 28 June 20 March 7.90 5.80 (0.00) [41 6.30 8.98 (2.48) 141 7.80 3.55 (0.98) 141 3.30 0.20 (2.03) [41 7 June 22 March 7.50 7.29 (2.15) [91 NA 4.50 2.80 (0.67) [91 NA 22 June 9 April 3.70 3.45 (1.55) [61 6.20 5.29 (3.46) 161 3.70 1.38 (2.43) 161 2.00 2.25 (0.75) [41 17 May 17 March 10.50 6.45 ( 1.40) 4.10 1.13 (1.13) 1.20 0.24 (0.86) “71 “71 5.80 2.31 (0.83) 171 1986 Late-born Others 10 July 10 April “71 1987 Late-born Others 1989 Late-born Others 1991 Late-born Others 1993 Late-born Others [51 *Grams per day; means, standard deviations (in parentheses), and sample sizes (bracketed) shown for clusters of infants born at normal time each year. aAverage date of birth shown for clusters of infants born at normal time of year. targets have been, also to my eyes, among the group members most closely resembling known adversaries. Ringtailed lemurs appear least able to recognize groupmates reliably when they are first noticed fighting or otherwise moving rapidly. It is probably for this reason that the targeted aggression phenomenon so prominently features aggressors’ a s well as victims’ constant monitoring of one another’s locations and activities. Whereas lemurs evidently recognize one another by scent (e.g., Table 111) and sound [Macedonia, 19861, neither capacity can ensure that razor-sharp canine teeth applied to one of two whirling bodies would not injure the intended beneficiary. And, in my experience, much higher proportions of escalated dyadic conflict in lemurs than in papionine monkeys involves full-scale grappling, with all eight hands and feet and both mouths attached between opponents. On the basis of all my observations, I believe that peripheral neuroanatomy resulting in relatively low visual acuity precludes frequent spontaneous intervention by ringtailed lemurs on behalf of kin and current dominants. All prosimians lack several anthropoid specializations of the visual system. Even ringtails, among the most diurnal of prosimians, lack fovea, for example. This and related aspects of visual anatomy provide ringtailed lemurs less than one-fifth the visual acuity enjoyed by Papionines, humans, and other Anthropoids (Table IV). As allowed above, sociocognitive, rather than perceptual, constraints may instead intervene to preclude matrilineal dominance inheritance for ringtailed lemurs. Also, the various possibilities do not exclude one another. The exciting idea here is that one or Development and Dominance Among Primates / 165 TABLE 111. Selected Examples of Visual Recognition Errors by Aggressive Ringtailed Lemurs 24 April 1986-Adult female LY had targeted young immigrant males DI and HI for intense antiinfanticidal aggression; today, she spotted her son of the same age, AN, approaching from 10-15 m; as often done to DI and HI, she stared, rose, and charged; LY pulled up sharply 1 m from AN, who had simply stopped walking, and they departed one another peaceably 11 December 1990-Near the boundary between group territories, young adult male GL spontaneously charged AX, a peer with whom he had been making transfer excursions; GL stopped suddenly 1 m from his target, sniffed him, and walked away 14 April 1991-Adult female CO saw two pubertal males wrestling in the leaf litter and charged to attack; immediately after grabbing one of them by the pelage, she dropped him and walked off, apparently having discovered that he (HC) was her son 8 July 1992-Four months ago, second-ranking adult female CN initiated targeted harassment of the low-ranking female BU; today, she noticed BU tumble into a bout of wrestling play with juvenile and adolescent groupmates and interrupted her foraging to rush over to the interaction, 10 m away; upon arriving, she stood bipedally, bent over the two remaining players, and paused for 2-3 seconds; CN sniffed first the body of her brother (NT); then, upon sniffing BU, she immediately grabbed and bit her more neuroethological limitations seem likely to constrain the development and evolution of social structure in ringtailed lemurs, with surprisingly far-reaching ramifications for life-history evolution in these primates. DEVELOPMENT OF INDIVIDUALS AND THEIR SOCIAL SYSTEMS Investigation of relationships among classical life-history traits, behavioral development, and animal social structure has just begun. Focus on these issues can be expected to increase in research on nonhuman primates, due to our affinities with these animal taxa and our desire to understand the development of complex social systems [e.g., Cheney & Seyfarth, 1990; Harcourt & de Waal, 19921. One purpose of this article has been to emphasize that we can expect to find behavioral processes-including developmental, perceptual, and cognitive aspects-to be integrated features of the particular life histories under study. As in all of biology, a principal objective for future research on behavior will be to identify developmental mechanisms. How do life histories-of individuals and their groups-self-organize? What causal and functional relationships are responsible for the consistencies in physical, behavioral, and social development observed across populations and generations? Heretofore, research on development has been conceived as a different endeavor from that concerned with evolution. Progressively more often today, these two domains of inquiry are properly viewed as inextricably related and mutually supportive [Buss, 1987; Ho & Fox, 1988; Roth, 1991; Gottlieb, 1992; Salthe, 1993; Hall, 1994). Certainly, to achieve meaningful understanding of diversity in social systems, normative behavioral development of individuals must be analyzed in relation to characteristic patterns in physical development, reproduction, and ecology. Likewise, I argue below, full analysis of these life-history features must attend to effects of behavioral development and social systems. Growth and Adult Social Behavior Shape Behavioral Development Our overview of physical and behavioral development in two groups of primates introduced substantial evidence of causal and functional relationships be- 166 / Pereira TABLE IV. Primate Visual Anatomy and Performance* Prosimians Galago Tupaia glis senegalensis Specialized retinal structures Photoreceptors Maximum density per 100 mu Axial eye length (mm) Mm retina/degree of visual acuity Convergence: central photoreceptors to ganglion Visual acuity (min of arc) None Only cones 21 7 0.09 0.5:l 6.2 Area centralis Only rods 88 15 0.19 12:l 4.3 Lemur catta Area centralis 1 cone: 5 rods 20 15 Anthropoids Saimiri Macaca Homo sciureus mulatta saviens Fovea Fovea Fovea Foveal cones Foveal cones Foveal cones 60 15 50 20 38 24 0.19 0.18 0.25 0.29 8:1 4.5 1.5:l 0.75 1.5:l 0.75 1.5:l 0.75 *Neuringer et al., 1981; Neuringer, personal communication. tween these ontogenetic domains. In particular, given marked discontinuities in development, the riskiest aspects of dominance acquisition were found to be timed closely with the onset of accelerated growth and maturation. Male and female Papionines complete their rise in dominance over adult females just before or as growth spurts and maturation begin. Also, infant ringtailed lemurs establish their dominance relations just as they begin to help sponsor their own rapid growth. The next year (or next, depending on nutrition), following dry season suppression of growth rate, rapid growth is resumed, females sexually mature, and only then do those living in large or growing groups strive to overturn some adults in dominance, which enables them to begin reproducing without dispersing. Also supported were our assumption of juvenile risk aversion and prediction that juveniles seek to maximize their dominance within constraints imposed by social structure. Adult Papionines intervene systematically in infants’ competitive interactions before infants themselves seem aware of matrilineal social structure. But also, infants respond quickly within the system. They readily begin behaving in a dominant manner toward lowborn peers, and dominance relations are well established by weaning. Papionine immatures rarely strive to “overachieve” in dominance, and efforts to dominate much larger or relatively high-ranking group members are postponed until larger sizes are attained [Datta, 1983a; de Waal, 19931. But also, youngsters instigate fights with older lowborn groupmates when likely supporters are nearby and solicit assistance over longer distances when necessary [Pereira, 19921. In the more dimorphic species, young males exploit females’ apparent disinclinations to oppose them, moving readily into positions of dominance over female peers and some adult females well before puberty. Infant ringtailed lemurs strive demonstrably for high dominance among their birth peers, and probability of survival is likely to be at stake. When necessary, ringtails stage intense, conspicuous grappling bouts at extremely young ages to establish their dominance relations. Almost certainly, grappling renders ringtailed infants more vulnerable not only to injury, but also to predators and infanticidal adults [Pereira, 1993~1.The value of size to survival is suggested by basic photoperiodic regulation of growth effort and the significantly accelerated and extended growth of late-born and other small infants. Like so many immature Development and Dominance Among Primates I 167 animals in temperate regions [Boyce, 1988; Pereira, 1993a1, young ringtailed lemurs have a deadline to meet: inevitably, their first long dry season fast approaches. By maximizing their dominance, ringtailed infants promote their chances of extensive growth and energy storage by mid-autumn [Pereira, 1993b,c; Pereira & Pond, 19951. Restriction of dominance struggles and high growth effort to the season of plentiful food minimizes risk of mortality due to malnourishment for this bottom-ranking class of group members. Bidirectional Effects in Life-History Evolution Two major life-history features, one traditional and one nontraditional, provided basic context for our analyses. Each arguably imposes important constraints on the development and evolution of the social systems discussed. The traditional feature was pattern of growth. Regardless of why dimorphism varies among papionine taxa, attendent variation in its development appears to influence the manner in which males and females come to interact agonistically, generating basic variation in social structure. The experiences of juvenile female baboons, for example, multiply confirm for them that males are inappropriate agonistic opponents. Juvenile males, meanwhile, experience that females are easy to dominate, especially whilst collaborating with other powerful males. These social patterns, reinforced throughout development, become prominent among adult savanna baboons. By contrast, such experiences are made rare for developing rhesus and Japanese macaques by the modest relative sizes and growth capacities of pubertal males in these taxa. Consequently, female rhesus and Japanese macaques maintain relatively great agonistic influence over male behavior, and males in these taxa continue to orient their coalitionary inclinations as or more heavily into their relations with females as they do into their relations with males [e.g., Koford, 1963; Packer & Pusey, 19791. Research on populations of varying degrees of dimorphism would provide tests of these ideas. The species differences in growth pattern and prereproductive experience that I highlight may act as initial conditions [sensu Salthe, 19851 that promote the development of additional contrasts in sociobiology. Consider, for example, “special” relationships, or male-female “friendships” in Papionines. Males and females contribute to and, seemingly, benefit from special relationships differently in different taxa. Male baboons never receive agonistic support from their female friends, for example, whereas male macaques do [e.g., Chapais, 1983a,b, 1986; Smuts, 19851. Conversely, male baboons possess a commodity [Noe et al., 19911 that no male rhesus or Japanese macaque does: absolute agonistic power over females. Related perhaps is that, compared to male baboons, male macaques perform much more grooming of their friends and less often seem favored by them as mates [Smuts, 1985; Chapais, 1983a,b; Hill, 19901. The second contextual variable for our analyses was a nontraditional point of focus in life-history analysis but a classical feature of research on social behavior: dominance behavior itself. We don’t yet know why some primates practice dominance while others do not [e.g., Pereira & Kappeler, in press]. But the presence or absence of this mode of agonistic relationship can reasonably be expected to influence life-history evolution, including aspects of growth and social structure. I have argued, for example, that male baboons subordinate females and females avoid conflict with males because dominance can mediate access to food in this species. Accordingly, taxonomic variation in relative size and growth capacity of pubertal males across taxa might not promote the observed variation in dynamics and functioning of special relationships (see above) if dyadic dominance was unimportant to papionine monkeys. 168 I Pereira Ringtailed lemurs well illustrate how classical life-history traits may respond to aspects of social behavior and how positive feedback can develop in life history evolution. Earlier, I suggested that birth synchrony evolved in ringtails because mothers are unable to intervene behaviorally to promote offspring dominance and because infants compete intensely for dominance around mid-lactation. Birth synchrony, in turn, increases the need for dominance competition among infants, further enhancing the value of rapid growth. If dominance were unimportant to the members of this species (e.g., Eulemur fulvus rufus [see Pereira & Kappeler, in press]), growth and reproduction might exhibit more relaxed and flexible seasonality. Contest competition would be reduced for infants, with peers and adults, before and during dry seasons. Ringtailed lemurs provide other examples of complicated relations among lifehistory features. What selection pressure demands that high visual sensitivity (night vision) be conserved? I suggest annual temperature cycles [see also Morland, 19931. Ringtails spend the summer and early fall not only growing rapidly, but also growing hair rapidly and accumulating white adipose tissue a t superficial depots [Pereira & Pond, 1995; Pereira, unpublished data]. During peak summer temperatures, ringtails extend their characteristic midday “siesta” [Jolly, 19661 from midmorning until late afternoon and spend much of that time panting and licking their palms and wrists, in efforts to reduce body temperature. Their strategy of coping with environmental seasonality, ironically, includes growing heavy winter coats during the hottest months. To help with this, much daily activity during summer and early fall is probably shifted t o the nighttime [see also Jolly, 19661. Ringtails and other gregarious diurnal and semidiurnal lemurs are thought to have evolved from nocturnal ancestors [Martin, 19901. This inference is supported by an overall life-history response to seasonality that seems better adapted to a nocturnal life-style. As yet, I suggest, that life-history strategy has obstructed a complete shift to diurnality and associated social structures, such as dominance hierarchy maintenance and matrilineal rank inheritance. CONCLUSIONS 1. Research on growth and behavioral development in papionine monkeys and ringtailed lemurs has underscored the integrated nature of animal life histories, from environmental seasonality through sensory, reproductive, and developmental biology on to social cognition. Understanding the development of primate social systems will depend on understanding individual development in relation to all aspects of male and female life histories. 2. Patterns of growth and social structure influence the development of dominance relations in primates. When characteristic discontinuities in growth effort exist, for example, relatively risky aspects of dominance acquisition occur just before or as growth spurts begin in papionine monkeys and ringtailed lemurs. Also, female papionines rarely try to dominate females from families higher ranking than their own. See also conclusions 3 and 4. 3. Patterns of development can influence reproductive biology. Reproductive synchrony, for example, probably evolved in ringtailed lemurs because (1)females are unable to intervene to promote offspring dominance, (2) infants grow rapidly in part to attain the large size that conveys high dominance, which continues to enhance growth rate and probability of survival, and (3) birth synchrony precludes an insurmountable initial advantage for any female’s infants. 4. Patterns of development influence social structure. Across multimale papionine taxa, for example, increases in pubertal size andlor growth capacity of males relative to females are associated with decreases in female inclination to t r y and Development and Dominance Among Primates / 169 dominate males, regardless of age class. Male and female perceptions of males and females as potential partners and opponents in social conflicts seem to be reinforced bidirectionally across the life span and relate importantly to known differences in social structure. 5. Aspects of growth, reproduction, and social structure in primates are probably influenced by characteristic patterns of dyadic social behavior. The phenomena cited in conclusions 3 and 4, for example, may depend importantly on the characteristic expression of dominance behavior in these monkeys and lemurs. 6. In ringtailed lemurs, an integrated set of physiological responses to photoperiodic cycling corroborates the suspected origin of these primates among nocturnal taxa. 7. Certain responses to photoperiod, such as fat storage and hair growth in summer and fall, may require ringtailed lemurs to retain good nocturnal vision, and consequent limitation of visual acuity may constrain social structure (e.g., by precluding maternal rank inheritance). ACKNOWLEDGMENTS I thank the Director, Dr. K. Glander, for permission to research at the DUPC, and Dr. A. Jolly, Dr. H. Crowley, and especially Mr. J . de Heaulme for both permitting and facilitating my research a t the Berenty Reserve. L. Martin, F. Kaestle, J. Opperman, A. Wang, L. Yow, L. Santini, C. Dina, and J . Schackleford assisted with behavioral observations, and K. Alford-Madden, D. Brewer, S. Cavigelli, P. Kappeler, L. Martin, T. Mendelson, F. Stewart, and L. Vick assisted in obtaining body weight data from DUPC ringtailed lemurs. To many researchers I am deeply grateful for permissions to present unpublished data: on juvenile dominance relations, M. van Noordwijk and A. Baker; on growth trajectories, C. van Schaik; and on visual anatomies and acuities, M. Neuringer. D. Hill, S. Perloe, D. Sprague, and L. Wolfe advised me on the intervention behavior of adult male macaques, and A. Jolly and N. Koyama provided historical information on ringtailed social groups, especially T Group, at Berenty. Data on infant grappling between 1981 and 1983 were documented by L. Taylor . 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