Human life histories in an evolutionary and comparative context

This dissertation utilizes life history theory to describe traits that are derived in humans through comparisons with other primate species. Modern human life histories are unique in that they are slower, exhibiting distinctly long postmenopausal life spans and later ages at sexual maturity as a result of a reduction in adult mortality since the evolutionary split the last Pan-Homo ancestor. Faster reproduction with shorter than expected interbirth intervals and earlier weaning ages are likely the result of cooperative breeding featuring postmenopausal grandmothers. Life history traits are distinguished from life history related variables (LHRVs) which are used to makes inferences about life history variables in extinct taxa. Body mass LHRV is a strong predictive life history proxy, but brain size and dental development are only weakly associated and inferences using them should be made with caution. Age at first birth is a central variable in demographic life history models as it identifies the beginning of fertility. For most mammals, age at first birth is closely aligned with the timing of physiological maturity. Humans live in varying ecologies that influence maturation rates and have marriage institutions that can constrain sexual access to fecund females. With few exceptions, the floor of the range of human age at first birth is remarkably consistent at about 17-18 years. Women who experience their first births before this age suffer maternal and infant costs. Heterogeneity, the inherent variation in individual quality, may have an important impact on the timing of life history events. Individuals of lower quality in severe conditions are prone to culling, leaving a subset of robust individuals who thrive in measurable ways. A test of this heterogeneity hypothesis is conducted using a subset of historic vital records from the Utah Population Database. Results show that mothers of twins have a more robust phenotype with lower postmenopausal mortality, shorter average interbirth intervals, later ages at last birth, and higher lifetime fertility than their singleton-only bearing counterparts. Thus, bearing twins may be a useful index of maternal heterogeneity.

HUMAN LIFE HISTORIES IN AN EVOLUTIONARY AND COMPARATIVE CONTEXT by Shannen Lorraine Robson A dissertation submitted by the faculty of The University of Utah in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Anthropology The University of Utah August 2011 Copyright © Shannen Lorraine Robson 2011 All Rights Reserved T h e U n i v e r s i t y o f U t a h G r a d u a t e S c h o o l STATEMENT OF DISSERTATION APPROVAL The dissertation of Shannen Lorraine Robson has been approved by the following supervisory committee members: Kristen Hawkes , Chair 04/27/2011 Date Approved Douglas Jones , Member 04/27/2011 Date Approved James O'Connell , Member 04/27/2011 Date Approved Eric Rickart , Member 04/27/2011 Date Approved Ken Smith , Member 04/27/2011 Date Approved and by Elizabeth Cashdan , Chair of the Department of Anthropology and by Charles A. Wight, Dean of The Graduate School. ABSTRACT This dissertation utilizes life history theory to describe traits that are derived in humans through comparisons with other primate species. Modern human life histories are unique in that they are slower, exhibiting distinctly long postmenopausal life spans and later ages at sexual maturity as a result of a reduction in adult mortality since the evolutionary split the last Pan-Homo ancestor. Faster reproduction with shorter than expected interbirth intervals and earlier weaning ages are likely the result of cooperative breeding featuring postmenopausal grandmothers. Life history traits are distinguished from life history related variables (LHRVs) which are used to makes inferences about life history variables in extinct taxa. Body mass LHRV is a strong predictive life history proxy, but brain size and dental development are only weakly associated and inferences using them should be made with caution. Age at first birth is a central variable in demographic life history models as it identifies the beginning of fertility. For most mammals, age at first birth is closely aligned with the timing of physiological maturity. Humans live in varying ecologies that influence maturation rates and have marriage institutions that can constrain sexual access to fecund females. With few exceptions, the floor of the range of human age at first birth is remarkably consistent at about 17-18 years. Women who experience their first births before this age suffer maternal and infant costs. Heterogeneity, the inherent variation in individual quality, may have an important impact on the timing of life history events. Individuals of lower quality in severe conditions are prone to culling, leaving a subset of robust individuals who thrive in measurable ways. A test of this heterogeneity hypothesis is conducted using a subset of historic vital records from the Utah Population Database. Results show that mothers of twins have a more robust phenotype with lower postmenopausal mortality, shorter average interbirth intervals, later ages at last birth, and higher lifetime fertility than their singleton-only bearing counterparts. Thus, bearing twins may be a useful index of maternal heterogeneity. iv This dissertation is dedicated to Ann Kelsey and Dr. Lois Alexander Merkler. TABLE OF CONTENTS ABSTRACT ...................................................................................................................... iii LIST OF FIGURES ........................................................................................................ viii LIST OF TABLES ..............................................................................................................x ACKNOWLEDGEMENTS ............................................................................................. xii INTRODUCTION ..............................................................................................................1 Chapter 1 THE DERIVED FEATURES OF HUMAN LIFE HISTORY ..............................5 Summary ......................................................................................................................6 Derived human life history traits .................................................................................8 Life history contrasts ..................................................................................................12 Effects of derived human life history .........................................................................19 Conclusions ................................................................................................................32 Acknowledgements .....................................................................................................33 References ..................................................................................................................34 2 HOMININ LIFE HISTORY: RECONSTRUCTION AND EVOLUTION ........47 Abstract ......................................................................................................................48 Introduction ................................................................................................................48 Part I. Life history and life history-related variables of extant hominids ..................49 Part II. Inferring the life history of extinct taxa .........................................................60 Summary ....................................................................................................................71 Conclusion ..................................................................................................................71 Acknowledgements .....................................................................................................71 References ..................................................................................................................71 Appendix: Notes for body mass and brain size data as used in Tables 3-4 ................78 3 AGE AT FIRST BIRTH IN HUMANS: EVALUATION OF A DEMOGRAPHIC VARIABLE WITHIN THE CONTEXT OF LIFE HISTORY ........................................................................................................80 Abstract ......................................................................................................................81 Introduction ................................................................................................................82 Variation in human age at menarche .........................................................................84 Human adolescent subfecundity and the consequences of early teen pregnancy .......87 Variation in human age at first birth ..........................................................................90 Marital fertility ...........................................................................................................91 Great ape comparison ................................................................................................94 Evaluating Charnov's life history model ...................................................................97 Discussion ..................................................................................................................99 Acknowledgements ...................................................................................................101 Literature cited .........................................................................................................102 4 TWINNING IN HUMANS: MATERNAL HETEROGENEITY IN REPRODUCTION AND SURVIVAL ..................................................................124 Abstract ....................................................................................................................125 Introduction ..............................................................................................................125 Demographic data and methods ...............................................................................126 Results ......................................................................................................................127 Discussion ................................................................................................................128 References ................................................................................................................130 vii LIST OF FIGURES 1-1 Phylogenetic relationships of the great ape species ............................................... 8 1-2 Neonatal weight relative to maternal weight ........................................................ 17 1-3 Percent of adult brain size achieved by age .......................................................... 23 2-1 Phylogenetic relationships of the great ape species .............................................. 50 2-2 Comparison of modern human and chimpanzee absolute (panel A) and relative (panel B) brain growth trajectories ....................................................................... 57 2-3 The more speciose (splitting) taxonomy .............................................................. 60 2-4 Estimated body mass plotted against first appearance date for the fossil hominin taxa recognized in the splitting taxonomy .............................................. 64 2-5 Estimated body mass plotted against first appearance date for the fossil hominin taxa recognized in the lumping taxonomy ............................................. 65 2-6 Estimated endocranial volume plotted against first appearance date for the fossil hominin taxa recognized in the splitting taxonomy ..................................... 67 2-7 Estimated endocranial volume plotted against first appearance date for the fossil hominin taxa recognized in the lumping taxonomy ..................................... 67 2-8 The relationship between crown formation and eruption sequence in modern humans, Pan and P. boisei .................................................................................. 68 3-1 Average ages at menarche and first birth for 21 small-scale natural fertility societies ............................................................................................................. 116 3-2 Modern mean (or median) age at menarche for 67 contemporary countries worldwide and 17 small-scale natural fertility societies ...................................... 117 3-3 Modern mean (or median) age at first birth for 56 developing countries worldwide and 17 small-scale natural fertility societies ...................................... 118 3-4 The period between human age at menarche and age at first birth (unpaired populations) results from adolescent subfecundity and marital fertility ............... 119 3-5 Median age at first marriage and first birth among women aged 25-49 in 56 developing countries .......................................................................................... 120 3-6 Comparison of age at menarche and age at first birth for the great apes ............. 121 ix LIST OF TABLES 1-1 Primary life history parameters of female great apes ............................................ 11 1-2 Human and chimpanzee brain size at birth and adulthood by sex ......................... 23 1-3 Eruption and crown formation schedules for permanent teeth .............................. 25 2-1 Life history and life history related variables and their present availability for extinct taxa .................................................................................................... 50 2-2 Primary life history variables for female great apes, mainly for wild populations compared to those of modern humans, mainly foragers ........................................ 52 2-3 Comparison modern human and chimpanzee absolute and relative brain size ...... 56 2-4 Eruption and crown formation schedules for permanent teeth of extant great ape species .................................................................................................. 56 2-5 (A) Splitting and (B) lumping hominin taxonomies and skeletal representations within the taxa in the more speciose taxonomic scheme ...................................... 61 2-6 Body mass estimates for extant great ape species, modern humans and the hominin taxa as defined by the splitting and lumping hominin taxonomies .......... 63 2-7 Cranial capacity estimates for the hominin taxa recognized in the splitting and lumping taxonomies ...................................................................................... 66 2-8 The presence of modern human-like LHRVs within the taxa recognized in a splitting hominin taxonomy ................................................................................. 70 3-1 Reproductive and general information for small-scale natural fertility , societies (foragers, horticulturalists, and agriculturalists) .................................. 122 3-2 Reproductive and general information for historic populations (1940 or earlier, before widespread availability of contraception) ................................................ 123 4-1 Descriptive statistics of the Utah population database ........................................ 126 4-2 Mortality hazard ratios for women living past age 50 ........................................ 127 4-3 Linear regression results for the effects of bearing twins on lifetime parity ........ 128 4-4 Linear regression results for the effects of bearing twins on average interbirth intervals ............................................................................................. 128 4-5 Linear regression results for the effects of bearing twins on total reproductive span .............................................................................................. 129 4-6 Linear regression results for the effects of bearing twins on age at last birth .................................................................................................................. 129 xi ACKNOWLEDGEMENTS I thank my indefatigable committee chair and mentor Kristen Hawkes, for challenging my analytical curiosity and fostering a deep appreciation for detailed scholarship. I also thank my committee members Doug Jones, James O'Connell, Eric Rickart, and Ken Smith for their time, patience and endurance over these many years. I am grateful to the four coauthors who have generously given their permission to use collaborative material as part of this dissertation. Chapter 1 was coauthored with Kristen Hawkes and Carel van Schaik, Chapter 2 was coauthored with Bernard Wood, and Chapter 4 was coauthored with Ken Smith. These collaborations with senior researchers were invaluable personal and professional learning experiences for this graduate student. I am indebted to the legion of family, friends, instructors, colleagues and fellow classmates who have extended their time and support on behalf of this endeavor. In particular I thank my parents, Gail, Ken, and Gigi, and my husband, Anthony, for all of their love and encouragement along this journey. Finally, I thank SAR Press, John Wiley and Sons, and Proceedings of the Royal Society for permission to reprint work previously published. Many individuals have contributed to the topics covered herein but I alone am responsible for the conclusions, as well as any errors or omissions in this dissertation. INTRODUCTION This dissertation describes the pattern of human life history in an evolutionary context and highlights the empirical advantages of comparisons between humans and nonhuman primates for identifying distinctively human features. Researchers interested in reconstructing human evolutionary history traditionally focus on fossil, archaeological, developmental, and ethnographic studies. Comparative primatology provides an additional complimentary line of evidence. Examination of interspecific variation from a phylogenetic perspective reveals the evolutionary history of derived and ancestral traits across the order, highlighting those specialized human traits that require explanation. Most life history studies focus on females, because female fertility and mortality determine population growth and age structure. Following Schultz's original illustration, the major life events of a female mammal are age at weaning, age at sexual maturity, the pace and timing of reproduction, age at end of fertility and lifespan. The timing of these variables are correlated, responding invariantly to shifts in extrinsic adult mortality rates. Herein I first compare modern human life histories to those of other great apes species to identify those traits that are derived in humans and which are likely to be shared by our closest ancestor. Life history variables are distinguished from life history-related variables (LHRVs), traits that are linked with, or can be used to make inferences about, life history but are not life history traits themselves. LHRVs are important to evaluate as they provide an opportunity for estimating life history events that are difficult to measure directly as well as providing proxy life history parameters for extinct taxa. All great apes exhibit slow life histories but compared to other primates human life histories are the slowest, exhibiting long postmenopausal lifespans and later ages at first birth, pointing to a reduction in human adult mortality since we shared a last common ancestor. Gorillas, though the largest of the great apes, have relatively fast life history pace, likely the result of a specialized folivorous diet. Humans also exhibit a faster than expected reproductive rate with distinctively shorter interbirth intervals and early weaning, a pattern likely derived from a unique form of cooperative breeding featuring vigorous postmenopausal grandmothers. Three LHRVs - body mass, brain growth trajectories, and dental development - were compared to the timing of life history variables to determine their usefulness as proxies for extinct taxa. Body mass proved to be the best predictor of life history events, while brain growth and dental development are weakly related proxies and inferences from them should be made with caution. Many researchers claim that the human brain grows at a faster rate and for a much longer post-natal period than chimpanzees, resulting in a significantly larger absolute and relative adult brain size. However, few studies have demonstrated this pattern empirically. A common assumption is that human brain growth extends beyond weaning, perhaps even until maturity, and accounts for the extended human subadult period. In Chapters 1 and 2, I compile and plot several age-specific brain size datasets for humans and chimpanzees. These data show that chimpanzees and humans have a similar percentage of adult brain size at birth, relative rates of brain growth, and achieve adult 2 brain size at similar ages, around 3-4 years old. Both chapters discuss how these data challenge many of the assumptions about human altriciality and its influence on delayed juvenility. Similarly, paleoanthropologists have high expectations for dental development patterns as proxies for life history events. However, evaluation of life history-related variables for extinct hominins in chapter two shows that there is no evidence of any hominin taxa possessing a body size, brain size, or dental development pattern reflecting the modern human pattern. Age at first birth is a central variable in demographic life history models because it identifies the beginning of fertility. For most mammals, age at first birth is closely aligned with the timing of physiological maturity. Humans, however, live in varying ecologies that influence maturation rates and have marriage institutions that can constrain sexual access to fecund females. Using data from the published literature, in Chapter 3 I examine the human pattern of age at menarche, age at first birth, and age at marriage to characterize relationships among them. I identify the observed variation in each of these variables and review the proximate mechanisms that influence their timing. These data show that, with few exceptions, the floor of the range of human age at first birth is remarkably consistent at about 17-18 years old across space and time. Women who experience their first births before this age suffer maternal and infant costs. I investigate the effect of age at marriage on age at first birth and find that, although there is broad variation in age at marriage across cultures, there is a strong tendency for marriage age to just precede female sexual maturity. I propose that, in general, female sexual maturity determines martial age rather than the reverse. Comparisons with nonhuman great ape 3 species confirm relatively late ages for all aspects of human sexual maturity, a pattern consistent with our slow life history. Finally, I consider the contribution of demographic heterogeneity to secular shifts documented in reproductive timing of women. While humans usually give birth to singletons, dizygotic twinning occurs at low rates in all populations worldwide. In Chapter 4, I consider two hypotheses that might account for the persistence of twinning. One hypothesis is that maternal depletion reduces the effectiveness of controls on embryo number, so that older mothers in poorer condition are less able to reject second embryos. Alternatively, twinning, while costly, may indicate mothers with greater capacity to bear that cost. Drawing from the vast natural fertility data in the Utah Population Database (UPDB), we compared the reproductive and survival events of 4,603 mothers who bore twins and 54,183 who had not. These mothers were born between 1807 and 1899, lived to age 50, and married once to men who were alive when their wives were 50. Results from proportional hazards and regression analyses are consistent with the second hypothesis. Mothers of twins exhibit lower post-menopausal mortality, shorter average interbirth intervals, later ages at last birth, and higher lifetime fertility than their singleton-only bearing counterparts. We conclude that bearing twins is more likely for those with the robust phenotype and a useful index of maternal heterogeneity. 4 CHAPTER 1 THE DERIVED FEATURES OF HUMAN LIFE HISTORY by Shannen Lorraine Robson, Kristen Hawkes, and Carel van Schaik Reprinted with permission from The Evolution of Human Life History, K Hawkes and R Paine (eds.), the School of American Research Press, pp.17-44. 6 2 The Derived Features of Human Life History SUMMARY Shannen L. Robson, Carel P. van Schaik, and Kristen Hawkes This chapter compares and contrasts the life histories of extant great apes in order to construct a hypothetical life history of the last common ancestor of all great apes and to identify features of human life history that have been derived during the evolution of our lineage. Data compiled from the published literature indicate some variation across the living taxa, but all great apes have relatively long lifespans and late maturity. Therefore, we infer that a slow life history is the ancestral state of all great apes. We examine variation in the timing of brain growth and aspects of den­tal development and find that they are not correlated in the life history varia­tion across these species. We conclude that acijustment in growth and development, though constrained by life history, are imperfect predictors of life history variables. Our comparisons show that humans have the slowest life history of the great apes, with a notably longer adult lifespan and an older age at first birth. We investigate the two important features of human life history that deviate from the expected great ape pattern: shortened interbirth intervals and vigor­ous postmenopausal longevity. Human infants are weaned earlier than 17 7 ROBSON, VAN SCHAlK, AND HAWKES expected for their age at maturity and before they are capable of independent feeding. Because females conceive soon after weaning an infant, women typically have multiple dependent offspring simultaneously. The pattern of human age-related fertility decline appears to be conserved. Reproductive senescence occurs at essentially the same age among all great apes, suggesting that the marked postmenopausal survival of human females is a derived trait resulting from selection for slower rates of somatic aging. The human pattern of shortened interbirth intervals and "stacking" dependents could have evolved only if human mothers had reliable sources of help. Related post­menopausal and prereproductive females, without infants of their own, likely gained inclusive fitness benefits from supplying that help. Despite variability in the statistics of deaths and births, every species shows strong central tendencies in demographic variables as a result of underlying, biologically anchored, individual predispositions for growth, development, reproduction, and aging (Harvey and Clutton­Brock 1985). Our species is no exception. Although there have been frequent allusions to dramatic changes in human life history as a result of changes in sources of mortality (Olshansky, Carnes, and Cassel 1998) , our species shows all the hallmarks of one designed for slow develop­ment and long life, with female fertility declining to menopause well before aging advances in other physiological systems. Thus, like any other species, humans possess a clearly delimited life history. And, for other species, it is a productive working hypothesis to regard these features as adaptations that evolved through natural selection. To set the agenda for the rest of this volume, it is essential that we obtain a clear picture of the changes that have taken place in hominin life history since the point of departure: the origin of the very first bipedal ape, five to seven million years ago. Ideally, we would also esti­mate when the major changes or novelties evolved during hominin evolution, aSSOCiating the shifts with adaptations to the new habitats colonized and lifestyles adopted by new hominid species. This task is fraught with difficulties, however, because values for extinct species tend to be reconstructed through processes with many steps, each with a particular uncertainty, or through relationships of unknown validity for the species involved (Skinner and Wood, chapter 11, this volume) . We can map the similarities and differences between modern 18 8 THE DERIVED FEATURES OF HUMAN LIFE HISTORY ~:-3MYA .1 Bornean orangutans Sumatran orangutans 12-15 MYA 3 MYAl Bonobos T 5-7 MYA. Chimpanzees Humans Gorillas FIGURE 2.1 Phylogenetic relationships of the great ape species. Estimated time of divergence of the orang­utan, gorilla, and chimpanzee/bonobo lineages nom the hominid lineage (G1azko and Nei 2003). Estimated time of bonobo/chimpanzee divergence (Wildman et a1. 2003). Estimated time of Bornean/Sumatran orangutan divergence (Zhang, Ryder, and Zhang 2001). humans and our closest living relatives, the great apes, with much less uncertainty and use these comparisons to infer the likely changes in life history over the radiation of our own lineage. DERIVED HUMAN LIFE HISTORY TRAITS Humans are part of the wider radiation of great apes. As shown in figure 2.1, our closest relatives are the two species of chimpanzee (genus Pan): the common chimpanzee (P. troglodytes) and the bonobo (P. paniscus). There is one other extant African great ape, the gorilla (Gorilla gorilla), which comes in various distinct subspecies. In Asia, a separate lineage of great apes evolved, of which two species of orang­utan (Pongo pygmaeus and P. abeJii) are the only living representatives (Zhang, Ryder, and Zhang 2001). Which Apes Resemble the First Hominin? Using some composite estimates based on the living great apes to reconstruct the common ancestor at the root of the hominin lineage would be permissible only if these taxa have changed little since then. On one hand, there is some support for this assumption: the molecu­lar and morphological similarities among the great apes suggest that they have been more conserved than the hominin radiation (Moore 19 9 ROBSON, VAN SCHAlK, AND HAWKES 1996). On the other hand, many assume that some parallel evolution has taken place in the African hominoid lineages, especially with respect to their locomotion. Because chimpanzees and gorillas are terrestrial knuckle walkers, it has long been considered parsimonious to assume that our common ancestor was too. However, Schmitt's (2003) recent examination of the locomotor biomechanics among extant primates suggests that human bipedalism most likely evolved independently from an arboreal ancestor. Because this change implies that the African great apes became more terrestrial over time, it may be argued that their late Miocene arboreal ancestors had slower life histories, given the general correlation between terrestriality and faster life history (van Schaik and Deaner 2003). If such parallel evolution is important to life history, then the still strictly arboreal orangutan may provide the best estimate for the earliest hominins. Therefore, if the African apes did not change independently, then the earliest hominins had a life history similar to our closest living relatives, the chimpanzee and bonobo, or if they did, one closer to the more arboreal orangutan. The utility of reconstructing a common ancestor from shared patterns and similarities between phylogenetically close extant relatives is obvious, but caution should be used in assuming that shifts in hominin life his­tories always favor one direction. The recently discovered Homo flore­siensis, a "hobbit"-size hominid (Brown et al. 2004; Falk et al. 2005) may exemplify how selection can favor a faster life history from a slower ancestor within our genus. Gorillas require special consideration because they are unusual among the great apes in that they achieve the largest body size in the shortest time. Adult body size is the result of both the duration and the rate of growth before maturity. Relative to other primates, all great apes grow for a longer time and achieve larger adult body sizes. Gorillas, however, grow much faster than the rest of us. On average, primates grow more slowly than other mammals and are therefore smaller at adulthood than nonprimate mammals of similar ages at first birth. Humans, chimpanzees, bonobos, and orangutans grow even more slowly than the primate average (Blurton Jones, chapter 8, this volume). But this is not true of gorillas. Variation in growth rate across the mammals is closely tied to variation in the rate of offspring pro­duction (Charnov 1991; Charnov and Berrigan 1993). Gorillas grow 20 10 THE DERIVED FEATURES OF HUMAN LIFE HISTORY more quickly and also produce babies at shorter intervals than the other great apes (table 2.1). The reasons gorillas exhibit rapid growth are debated, but analyses by Leigh (1994) show that growth rates among primates co-vary with diet. Leigh (1994) examined the diet ecology and growth rates offorty­two anthropoid primate species and found that those with more foliv­orous diets tend to grow faster than those with more frugivorous ones. All great ape species, including gorillas, favor fruit when it is abundant, but chimpanzees and orangutans specialize on fruit and extractive foods (such as insects) and sometimes vertebrate meat (chimpanzees more so). To some extent, bonobos (and gorillas, in particular) fall back on vegetative foods that tend to be abundant but of lower quality (Malenky et al. 1994; Conklin-Brittain, Knott, and Wrangham 2001). The first australopithecines were thought to have diets dominated by fruits and seeds (Schoeninger et al. 2001). If diet ecology influences growth trajectories, then we would expect the earliest hominins to have growth and reproductive rates closer to those of chimpanzees and orangutans than to gorillas. Also, fossil evidence suggests similarities between chimpanzees and australopithecines (versus gorillas) in body sizes (McHenry 1994). Average growth rates for living humans are close to the rates for chimpanzees, bonobos, and orangutans (Blurton Jones, chapter 8, this volume). For these reasons, we consider the values of chimpanzees and orangutans as the endpoints of the range of estimates for the first hominins and refer to gorillas only when relevant. Data Sources To develop proper comparisons between people and living great apes, we primarily rely on the life history parameters estimated from hunter-gatherers, because their diets, mobility, foraging styles, and population densities most likely resemble those of modern humans before the invention of agriculture. Although we note estimates for some of these variables from a broader range of human populations in the text, in table 2.1 we used composite estimates from different detailed studies of extant hunter-gatherers whenever possible. This reduces concern about possible effects of improved diets and medical care on rate of development and senescence. It can be argued that the estimates are conservative in that ethnographically known populations 21 11 ROBSON, VAN SCHAlK, AND HAWKES TABLE 2.1 Plimary Life History Parameters of Female Great Apes (Arranged by Phylogenelic Distance from Humans), Mainly for Wild Populations, Compared with Those of Humans, Mainly Foragers Great Ape Species Orangutan (Pongo pygmaeus and P. abeJii) Gorilla (Gorilla gorilla) Bonobo (Pan paniscus) Chimpanzee (Pan tmglodytes) Human (Homo sapiens) Maximum Lifespan (Years) 58.7a 54.0a 50.0+b 53.4a 85.0c Age at First Birth (Years) 15.6d 1O.Oe 14.2f 13.3g 19.5h Adult Female Weight (kg) 36.0i 84.5 (71-98)j 33.0 (27-39)j 35.0 (25-45)j 47.0 (38-56)k Gestation Length (Days) 260m 255m 244n 225m 270m Sources: a. Judge and Carey (2000), b. Erwin et aL (2002), c. Hill and Hurtado (1996); Howell (1979); Blurton Jones, Hawkes, and O'Connell (2002), d. Wich el aL (2004), e. Alvarez (2000); for humans, only data from two roraging populations, the Ache and [Kung, f. Kuroda (1989), g. Average age at first birth for five P. troglodytes populations: Bussou, 10.9 years (Sugiyama 2004); Gombe, 13.3 years (WalliS 1997); Mailale, 14.56 years (Nishida e( at 2003); Tai, 13.7 years (Boesch and Boesch­Achermann 2000); and Kibale. 15.4 years (vVrangham in Knott 2001), h. Average age at first repro­duction from four human foraging groups: Ache, 19.5 years (Hill and Hurtado 1996); !Kung, 19.2 years (Howell 1979); Hadza, IS.77 years (Blurton Jones. unpublished data); and Hiwi. 20.5 years (Kaplan el a1. 2000), i. Smith and Jungers (1997); mean of subspecies, j. Average (range reporled in parentheses) compiled from Smit.h and Jungers (1997); Zihlman (1 997a); and Smith and Leigh (1998) , k. Average 01' range (reported in parenlheses) of ethnographic samples frorn Jenike (2001:table 5), 111. I-Iarvey, Martin, and Clutton-Brock (1987). n. Median gestation length [or bono­bas in captivity reported by de Waal and Lanting (1997:190) from Thompson-Handler (1990), o. Average or range (reported in parentheses) compiled [rom Smith and Jungers (1997); Zihlman of hunter-gatherers occupied only a subset of habitats initially colo­nized by modern people, mostly environments that are marginal for agriculture. The nonhuman great ape data primarily come from long-term field studies, and these data are improving over time (see table 2.1 for source references). In all the reports of wild studies, the ages of many adults were estimated; all maximum lifespans were based on estimates with unknown errors, Maximum lifespans in the table are therefore 22 12 Neonate Weight (kg) 1.56 (1.31-1.81)° 1.95 (1.6-2.3)° 1.38 (1.30-1.4S) ° 1.90 (1.4-2.4)° 3.00 (2.4-3.6)P THE DERIVED FEATURES OF HUMAN LIFE HISTORY Neonate as a % of Maternal Weight 4.3% 2.3% 4.2% S.4% S.9% q Age at Weaning (Years) 7.0e 2.8e 4.Se 2.Se Interbirth Intel'val (Years) 8.0Sd Age at Last Birth (Years) (1997a); and Smith and Leigh (1998) t p. Average neonatal weight of seventy-eight groups worldwide (range reported in parentheses) from Iv1eredith (1970). q. Calculated from data reported by Poppitt and colleagues (1994) on linked maternal/ neonatal ""eight ror eight populations, r. Average of two P. paniseLls populations: Warnba, 4.5 years (Takahata, Ihobe, and Idani 199G). and Lomako, 8.0 years (Fruth in Knott 2001). s. Average interbirth interval of six P. troglodytes populations: BOSSOll. 5.3 years (Sugiyama 2004); Combe. 5.2 years (Wallis 1997); Mahale. 5.6 years (Nishida et 31. 2003); TaL 5.7 years (Boesch and Boesch-Achermann 2000); Kanywara, Kibale, 5.4 years (Brewer-Marsden, Marsden, and Emery-Thompson n.d.); and Budongo, 5.6 years (Brewer-tvlarsden, Marsden, and Emery-Thompson n.d.), t. Average human interbirlh interval oC three foraging groups: Ache, 3.2 years (Hill and Hurtado 1996); !Kung, 4.12 years (Howell 19(9); and Hiwi. 3.76 years (Kaplan et al. 2000), u. Average of latest recorded age at last birth in four P. troglodytes populations: Combe, 44 years (GoodalJ Institute); Mahale, 39 years (Nishida et at. 2003); Tai, 44 years (Boesch and Boesch­Achermann 2000); and Bossou. 41 years (Sugiyama 2004), v. Hill and Hurtado (1996); Howell (1979); and Martin and colleagues (2003). taken from individuals of known ages in captivity. The mortality pro­files constructed for wild populations do not indicate stable or growing populations for any of the species, which implies that observed mor­talities are higher than they have generally been until quite recently. LIFE HISTORY CONTRASTS Comparisons of data in table 2.1 show that extant humans evolved the following changes in character states from the other great apes. 23 13 ROBSON, VAN SCHAlK, AND HAWKES Maximum Potential Lifespan The maximum potential lifespan of humans is clearly longer than that of the other great apes by several decades. Even among human foragers without access to any medical support, some people live into their 70s and 80s (R. B. Lee 1968; Howell 1979; Hill and Hurtado 1996; Blurton Jones, Hawkes, and O'Connell 1999, 2002). In contrast, chim­panzees in the wild usually die before they reach 45 (Hill et al. 2001), and orangutans before age 50 (Wich et al. 2004). This difference in lifespan remains even under captive and modern medical conditions; maximum recorded longevity for great apes is around 60 years (Erwin et al. 2002), whereas the oldest human on record died at 122 (Robine and Allard 1998). These data show that humans have gained an increase in maximum lifespan relative to the ancestral state of at least twenty to thirty years. Maximum lifespan and average adult lifespan are correlated variables (Sacher 1959; Hawkes, chapter 3, this volume). Chimpanzee (Hill et al. 2001) and orangutan (Wich et al. 2004) females in the wild who survive to age 15 can expect to live only an additional fifteen to twenty more years (probably more for orangutans), whereas hunter-gatherers at age 15 can expect to live about twice that long (Howell 1979; Hill and Hurtado 1996; Blurton Jones, Hawkes, and O'Connell 2002). Longer adult lifespans reflect lower adult mortality. When extrin­sic adult mortality is as low as it is among great apes, adults can live long enough to display signs of declining physiological performance and eventually die from age-specific frailty. Ricklefs (1998) showed that in species with adult lifespans similar to chimpanzees, about 69 percent of adult deaths result from age-related causes. Selection can favor slow­er rates of aging if the fitness benefits of extending vigorous physical performance exceed the costs of increased somatic maintenance and repair. Slower rates of aging may account for the difference between human and nonhuman great ape maximum lifespans (Hawkes 2003). There is little systematic evidence documenting age-specific declines in physical performance in nonhuman great apes, but qualitative descrip­tions suggest that, as expected from their relatively shorter lifespans, chimpanzees do age faster than humans. Goodall (1986) classified chimpanzees at Gombe as old aged beginning at age 33. Finch and Stanford (2004:4) report that individuals age 35 or more years "show 24 14 THE DERIVED FEATURES OF HUMAN LIFE HISTORY frailty and weight loss" and the "external indications of senescence include sagging skin, slowed movements, and worn teeth." As chim­panzees in the wild reach their mid-30s, they appear to age rapidly and die within a decade. In contrast, studies of physical performance among people who hunt and gather for a living show that vigor declines more slowly with age. Measures such as muscle strength in hunter-gatherer women decrease slowly over many decades (Blurton Jones and Marlowe 2002; Walker and Hill 2003). Comparable system­atic performance data on great apes are needed to test whether they do, in fact, age more quickly than people. Age at First Birth As expected from an extension in lifespan, age at first reproduc­tion among humans is much later than among other great apes and has increased from the ancestral state by four to six years. The age at first birth of female chimpanzees and bonobos in the wild, while vari­able, shows a central tendency toward 13 and 14 years, respectively. For gorillas, the mean age at first birth is 10 years, and orangutans bear their first offspring around age 15.6 years. Mean age at first birth among human foraging populations is 19.5 years. These central tendencies persist for all great ape species in spite of differences in environment and ecology among populations in the wild. The affluence of captivity seems to have only a modest effect on age at first birth. It is often assumed that superabundance enhances physical condition, accelerates the timing of first birth, and extends longevity. However, there is evidence that the husbandry practices and socioecological conditions of many captive colonies do not always maximize the welfare of great apes and often increase incidents of vas­cular disease, obesity, and stress (DeRousseau 1994; Finch and Stanford 2003). Captive chimpanzees and bonobos bear their first offspring when they are around 11 years old (Bentley 1999; Knott 2001; Sugiyama 2004). Even though this mean is earlier than the central tendency of age at first birth among their wild counterparts, it is within the age range of at least one wild population. Age at first birth for gorillas in captivity is virtually identical for those in the wild (9.3 versus 10 years). Captive orangutan females show the largest shift in age at first birth from their wild counterparts. Markham (1995) reports age at first birth 25 15 ROBSON, VAN SCHAlK, AND HAWKES for orangutans in captivity as 11.5 years, almost four years earlier than orangutans in the wild. Whether in the wild or captivity, though, orang­utans have the latest age at first birth and remain the "slowest" of the nonhuman great ape species. Similar to captive great apes, there is also surprisingly little variation in average age at first birth among humans. Even under current condi­tions of ample food supply and medical care, human females, on aver­age and cross-culturally, bear their first offspring after they are 18 years old (Bogin 1999a; Martin et al. 2003). Data from historic human records indicate that average age at first birth occurred even later, in the early to mid-20s (Le Bourg et al. 1993; Westendorp and Kirkwood 1998; Korpelainen 2000, 2003; Low, Simon, and Anderson 2002; Smith, Mineau, and Bean 2003; Grundy and Tomassini 2005; Helle, Lummaa, and Jokela 2005; Pettay et al. 2005). These data emphasize the limited plasticity of life history traits even in light of resource abundance. Maternal Body Size Later age at first birth enables energy to be invested in growth over a longer juvenile period, so most mammals with slower life histories also have larger body sizes (Purvis and Harvey 1995). Of all the primates, great apes are the longest-lived and latest maturing, as well as the largest-bodied. As previously discussed, gorillas are unusual in that they grow faster than the other great apes, including humans, achieving a much larger adult size. The remaining great ape species share a similar growth rate and achieve body sizes that generally vary with the duration of growth before maturity (Blurton Jones, chapter 8, this volume). Chimpanzees, bonobos, and orangutans bear their first offspring between the ages of 13 and 16 and have similar body weights, around 35 kg. Human females have a later average age at first birth, 19.5 years, increasing the duration of growth four to six years longer than Fan or Fongo species. As a result, human females in extant foraging societies are about 10-15 kg larger than chimpanzee, bonobo, or orangutan females. Modern foragers are generally smaller than the estimated body sizes for people before the Mesolithic (Ruff, Trinkhaus, and Holliday 1997; Jenike 2001). Ethnographic hunter-gatherer means may therefore underestimate the average maternal-size differences between humans and our common ancestor. 26 16 THE DERIVED FEATURES OF HUMAN LIFE HISTORY Gestation Length and Size at Birth Larger mothers have greater resources for offspring production, and great ape mothers translate this energy into larger, more expensive babies (Stearns 1992; see Hawkes, chapter 4, this volume:figure 4.7). As noted above, the rate of offspring production co-varies with growth rate (Charnov and Berrigan 1993); gorillas grow faster and produce babies at shorter intervals than the other great apes. Chimpanzees, bonobos, orangutans, and humans grow more slowly, more slowly even than the average primate but for a longer period of time, resulting in large mothers who produce large babies. Human females, with the longest duration of growth, have the largest maternal body sizes and produce the largest offspring. Larger human neonatal size is achieved through a comparably longer length of gestation, ten to thirty days longer than the other great apes (Haig 1999; Dufour and Sauther 2002). Although this dif­ference seems slight, human newborns spend the last weeks before par­turition accumulating remarkably large adipose fat stores (Southgate and Hey 1976), and these fat stores likely account for the compara­tively larger size of human neonates. Across the mammals, neonatal fat stores scale allometrically with body size (Widdowson 1950). Human neonates, however, are more than three times fatter than expected for a mammal of their size (Kuzawa 1998). At birth, 12 to 15 percent of human neonatal body weight is adipose tissue (Fomon et al. 1982). Although there are no data documenting the body fat of great ape infants, the qualitative difference in the amount of body fat between human and great apes is apparent. Schultz (1969:152) made the general observation that "most human babies are born well padded with a remarkable amount of subcutaneous fat, whereas monkeys and apes have very little, so that they look decidedly 'skinny' and horribly wrinkled." Estimating neonatal size relative to maternal size is difficult because there is extreme variation in adult body size both inter- and intra-individually and within and among populations (see table 2.1 for ranges). Nevertheless, graphing data reported by Poppitt and col­leagues (1994) show that neonatal weight scales allometric ally with maternal weight (figure 2.2). Bigger mothers bear larger infants, but the increase in the ratio of neonatal mass to maternal mass declines allometrically (slope of 0.746) with maternal size-6.4 percent for the 27 17 ROBSON, VAN SCHAlK, AND HAWKES 3.9 3.7 ti:O 6 3.5 {$ til ... @ .<:: tl.O 'iii 3.3 ~ ".@.. 3.1 «l C 0CIJ 2.9 ;\;;' '" Z 2.7 2.5 40 45 5 0 55 60 65 Maternal weight (kg) FIGURE 2.2 Neonatal weight relative to maternal weight (data from Poppitt et a1. 1994). Neonatal weight scales allometrically with maternal weight at a slope of 0.746. smallest mothers and 5.8 percent for the largest mothers in Poppit and colleagues' sample. Among extant human populations, neonatal size is somewhat larger relative to maternal body weight than other great ape species (Leuttenegger 1973). This difference is inflated when ethno­graphic hunter-gatherers are used to represent maternal size and may result from late Pleistocene decreases in adult size. Using two methods to estimate body mass, Ruff, Trinkhaus, and Holliday (1997) deter­mined that adult individuals in our genus were about 10 percent larg­er during the Pleistocene. Age at Weaning and Interbirth Intervals Species with slow life histories generally have later ages at weaning and longer interbirth intervals. Great apes exemplify this pattern. They wean their dependent offspring relatively late, especially the frugiv­orous chimpanzees and orangutans (around ages 4.5 and 7 years, respectively), and have long interbirth intervals (5.5 and 8 years, respectively). Humans, however, have the slowest life history in many respects, but we wean our infants comparatively early. Human foragers typically wean their infants by age 3 and have mean inter birth intervals 28 18 THE DERIVED FEATURES OF HUMAN LIFE HISTORY of around 3.7 years. Like age at first birth, human weaning ages are similar across a broad range of ecologies. Weaning age for humans is consistently "between 2 to 3 years and generally occurs about midway in that range" (Kennedy 2005:7). Many ways have been proposed to estimate expected ("natural") weaning age from other human life history variables, and most predict later weaning age than practiced (Sellen 2001 a). Harvey and Clutton­Brock (1985) predicted an average weaning age of 3.36 years based on a correlation between maternal and infant body size, but Charnov and Berrigan (1993) noted that mammalian infants are generally weaned when they achieve one-third of maternal body weight (Lee, Majluf, and Gordon 1991), which for humans occurs around 6.4 years. B. Smith (1992), following Schultz (1956), found that across a sample of pri­mates, weaning age correlated with the eruption of the first permanent molar, around 6.5 years in humans. It is clear that the observed human weaning age of 2 to 3 years is earlier than these predictions. This is all the more remarkable because other aspects of our life history have slowed down relative to the ancestral state (Smith and Tompkins 1995) . Age at Last Birth and Menopause Among mammals, oocytes are produced in the fetal ovaries until the third trimester of gestation, when the mitosis of germ cells ends. At this point, females have a fixed initial store of oocytes that is then sub­ject to a process of continual depletion, or atresia, over their lifetime until the number of remaining follicles nears zero (vom Saal, Finch, and Nelson 1994; O'Connor, Holman, and Wood 2001; A. Cohen 2004). In humans, the cycle of ovulation and menstruation is generated by an endocrinological feedback loop that requires a sufficient oocyte store O. Wood 1994). When there are too few oocytes remaining to stimulate ovulation, estimated at around one thousand follicles (Richardson, Senikas, and Nelson 1987), cycling ceases. All menstruating primates can potentially experience the senescent cessation of menses, or menopause, if they live long enough. In nonhuman species, however, reproductive senescence usually corresponds with somatic senescence, and few species live beyond the depletion of their oocyte store. This is well documented in captive populations of macaques (for 29 19 ROBSON, VAN SCHAlK, AND HAWKES example, M fuscata, Nozaki, Mitsunaga, and Shimizu [1995]; M muiatta, M. Walker [1995]; M nemestrina, Short et al. [1989]), where individu­als live longer with senescent impairments than they can in the wild. Data on reproductive senescence in great apes is scant, but histological examination of captive chimpanzee females' ovaries suggests that the process of oocyte reduction is similar to that in humans (Gould, Flint, and Graham 1981). The few captive females that survived to meno­pause exhibited the same pattern of declining fecundity and variable cycling experienced by women (Tutin and McGinnis 1981) and around the same age (Gould, Flint, and Graham 1981). Several years before menopause in women, the hormonal system that regulates menstrual cycles, the hypothalamic-pituitary-ovarian (HPO) axis, begins to break down because the number of oocytes necessary for ovarian steroid production is reduced below a necessary threshold. During this period of "perimenopause," cycle lengths become long and irregular, and many are anovulatory. Inconsistent functioning of the HPO axis and the increase in pregnancy failure during peri­menopause result in a steep decline in the fertility of human females (Holman and Wood 2001). In noncontracepting human populations, average age at last birth precedes average age at menopause by about ten years (Gosden 1985). There are few data documenting the pattern of age-specific fertility decline in nonhuman great apes, but those avail­able for chimpanzees suggest that fertility nears zero at 45 years of age (Nishida, Takasaki, and Takahata 1990; Boesch and Boesch Achermann 2000; Sugiyama 2004), as it does in humans (Howell 1979; Hill and Hurtado 1996; Muller et a1. 2002; Martin et al. 2003). It appears that the age at which fertility declines in the other great apes is similar to that of humans (see Wich et a1. 2004 on orangutans). This similarity suggests that we all share the ancestral pattern of ovarian ontogeny and what is derived in humans is not an unusual rate or timing of repro­ductive decline but a slowed rate of somatic aging and a Vigorous, post­menopausal lifespan. EFFECTS OF DERIVED HUMAN LIFE HISTORY Many characteristics of growth and development depend on life history but are not, themselves, life history traits. The contrasts described above for females, excluding body size-maximum potential 30 20 THE DERIVED FEATURES OF HUMAN LIFE HISTORY lifespan (or average adult lifespan), age at first birth, gestation length, interbirth intervals and age at weaning, and age at last birth-are directly linked to population vital rates. In this section, we discuss links between the derived features of human life history and aspects of human growth, development, and sociality. Altriciality and Brain Growth The postnatal growth requirements of human brains have long been seen as the source of our slow maturation. Compared with infants of the other great apes, human infants have been considered "helpless and undeveloped at birth" (Gould 1977:369), incapable of indepen­dent movement until at least 6 months of age; neonatal great apes are able to cling to their mothers from a very early age. This relative altri­ciality (Portmann 1941) has been attributed to the relatively small size of the human neonate's brain, under the assumption that a rapidly growing and developing brain is incapable of coordinating fully devel­oped locomotor behavior (R. Martin 1990). There have been objec­tions to both primary aspects of this widely accepted perspective. First, Schultz (1969:154) pointed out that the minimal locomotor develop­ment of humans at birth is not unusual, that, in fact, "the apes are born as helpless and immature as the exceptionally large human newborn." Because chimpanzee and gorilla infants are carried by their mothers for approximately twenty postnatal weeks, Schultz (1969: 157) conclud­ed that this "flatly contradicts the frequently heard vague claim that man is unique in his being born utterly helpless in such a very imma­ture state as is very exceptional among primates." In addition, human babies are born with strong grasping reflexes equal to that of other pri­mates (Konner 1972) and use sophisticated behavioral strategies to maximize their survival (Hrdy 1999). Together, these observations sug­gest that the motor skills of human neonates are no more altricial than those of other great apes and that infants are not behaviorally under­developed. Second, human altriciality is said to be the result of a smaller rela­tive brain size at birth due to an obstetrical constraint imposed by a pelvis shaped for bipedality. For most mammals, the rapid rate of fetal brain growth ends at, or just after, parturition. For humans, however, the fetal pattern of brain growth is comparably steeper and continues 31 21 ROBSON, VAN SCHAlK, AND HAWKES for almost a year after birth. The continuation of rapid fetal brain growth rates during the first twelve postnatal months led Portmann (1941) to suggest that humans really have a twenty-one-month gesta­tion span: nine months in utero and twelve extra-uterine months that R. Martin (1990) termed "exterogestation." This suggests that human infants are born "early" because continued brain growth in utero would result in a head size too large for successful parturition (R. Martin 1983) . Recent analyses comparing the patterns of brain growth in chim­pan- zees and humans (Leigh 2004) invite doubts about the uniqueness of rapid postnatal brain growth. We examine these data below. There are few published data sets of brain sizes for individuals of known ages. Most authors present their original data in figures and report averages instead of original values, making intraspecies com­parisons difficult (Jolicoeur, Baron, and Cabana 1988; Cabana, Jolicoeur, and Michaud 1993). Of the complete data sets published, most are derived from autopsy and necropsy records, a unique sample of individuals with various pathologies that possibly misrepresents the "normal" population. These are cross-sectional data, not longitudinal, repeated measurements on the same individual to assess individual variation in brain size and growth. However, these data currently pro­vide the only opportunity for quantifying brain growth and develop­ment. Technological advances in brain imaging should make longitudinal data sets available for future comparison and analyses. We calculated human brain measures from Marchand's (1902) data set, which reports brain weight (wet, including meninges, in grams), stature (in centimeters), sex, and known or estimated chrono­logical age. Marchand assembled these data from German autopsy records documented between 1885 and 1900. The original data include a total of 716 human males and 452 females from birth to more than 80 years old. The variation in brain size with age and sex compares favor­ably with other reports (Dekaban and Sadowsky 1978; Kretschmann et al. 1979), indicating that Marchand's series can serve as a represen­tative sample. Our calculations use his data on all individuals 3 years old and younger. Brain weights for chimpanzees (Pan troglodytes) of known ages were drawn from necropsy data reported by Herndon and colleagues (1999). Brain weights were obtained fresh at Yerkes Regional Primate 32 22 THE DERIVED FEATURES OF HUMAN LIFE HISTORY Center from 76 captive individuals (33 females and 43 males) who died from natural causes or were euthanized when natural death was immi­nent. We used a subset of these data to calculate percent of adult brain weight at birth and to graph brain size from birth to 3 years. These data, summarized in table 2.2 and plotted in figure 2.3, chal­lenge three common assumptions about the uniqueness of human brain growth. First, chimpanzee and human infants are more similar in their percent of adult brain size at birth than usually assumed. It is con­ventionally reported that human neonatal brain weight is only 25 per­cent of adult size at birth whereas chimpanzee neonates have 50 percent of their adult brain weight at birth (Dienske 1986). But chimps are twice as close to adult size at birth as are humans; instead of a large interspecific difference in relative neonatal brain size, the difference is only about 10 percent. A larger sample of chimpanzee neonates may close this interval even more. This revision results from slightly lower percentage values for humans but primarily from the much smaller neonatal value for chimpanzees. Until now, relative chimpanzee neonatal brain size has been repeatedly based on the estimated cranial capacity of a single cranial specimen, known to be 74 days old at death (Schultz 1941). When plotted against Herndon and colleagues' (1999) values, this specimen is larger than neonatal size and falls where it should in the scatter, given its age of 2.5 months. Second, we find that chimpanzees and humans share a very simi­lar pattern of relative brain growth (see figure 2.2). Leigh (2004: 152), using the same data to calculate brain growth trajectories for chim­panzees and humans, concluded that "after the first 18 months of life, Pan and Homo are not substantially different in terms of growth rates." Third, humans reach adult brain size much earlier than widely claimed, some individuals by 3 years of age. Kretschmann and colleagues (1979) used the Marchand (1902) data to show that, on average, males achieve 95 percent of total brain size by 3.82 years old and females reach 95 percent values by 3.44 years old. This is much earlier than assumed by most researchers. Analyses indicate similarities in brain growth, relative neonatal brain size, and motor and behavioral skills at birth between humans and chimpanzees, challenging the characterization of humans as distinctively altricial. The similarities between chimps and humans do 33 23 ROBSON, VAN SCHAlK, AND HAWKES TABLE 2.2 Human and Chimpanzee Brain Size at Birth and Adulthood by Sex Average Average Percent Neonatal Adult of Adult Brain Brain Total Species Sex Weight (g) 1 Weight (g) 2 at Birth Homo sapien;'> Males 371 (n = 16) 1404 (n = 150) 26.4 Females 361 (n = 8) 1281 (n = 116) 28.2 Pan troglodytes4 Males 125 (n = 3) 406 (n = 17) 30.8 Females 146 (n=4) 368 (n = 17) 39.7 1. Neonate is defined as an individual between birth and 10 days old. 2. Average adult brain size was calculated as the mean of individuals between 20 and 40 years old by sex for humans and the mean of individuals between 7 and 30 years old for each sex in chimpanzees because this range safely precedes a known trend toward declining brain weight with age (Dekaban and Sadowsky 1978; Herndon et al. 1999). 3. References: Marchand (1902). 4. References: Herndon and colleagues (1999). 100 (lJ N 'Vc:i 80 '," L .1:l :";" 60 -0 oj '>- 0 (lJ i0s.0 40 c: (lJ U L (lJ ll.. 20 0 0 6 12 18 24 30 36 Age (months) FIGURE 2.3 Percent of adult brain size achieved by age. Black dots are chimpanzees (Herndon et a1. 1999; n = 26; males = 16. females = 10); open circles are humans (Marchand 1902; n = 160; males = 111. females = 49). The star represents Schultz's (J 941) 74-day-old specimen. 34 24 THE DERIVED FEATURES OF HUMAN LIFE HISTORY not support the view that our juvenility is longer because of the growth requirements of our large brains. Dental Development Like brain growth and development, the pattern of dental growth and development is commonly used as a marker of life history events. Efforts have primarily focused on uncovering correlations between the timing and sequence of eruption of the permanent dentition and age at weaning and maturity. Relationships between dental markers and life history would provide a means to make direct interpretations of maturation schedules during hominin evolution based on fossil teeth. Given the systematic relationships among life history traits, establishing the timing of one would provide grounds for hypothesizing others. Teeth are less sensitive than other tissues to developmental insults and short-term ecological fluctuations (Nissen and Riessen 1964; Garn et al. 1973; Liversidge 2003), making them relatively reliable maturation markers. Schultz's often reprinted graph depicting variation in timing of life stages across the primates (for example, in Schultz 1969) used the emergence of the first permanent teeth to mark the end of infancy and the emergence of the last permanent teeth to mark the beginning of adulthood. Comparing primate species, Schultz (1949) also observed variation in the sequence of tooth eruption across the order. In species that are weaned relatively early, molars erupt before the deciduous teeth are lost and the emergence of the anterior permanent dentition. Schultz presumed that permanent molars erupted first so that infants would be prepared to masticate food when weaned, a generalization that B. Smith (2000) calls "Schultz's rule." Slower-developing humans show a distinctive eruption sequence: the permanent anterior denti­tion emerges before the molars. Schultz speculated that the human shift in eruption sequence is directly connected to slower human life history and, in particular, our much longer period of juvenility. Building on Schultz's recognition of a connection between dental development and life history, B. Smith (1989a) showed that across the primates there is a strong correlation between the eruption of the first permanent molar (Ml), weaning age and eruption of the third molar (M3), and age at first birth. In addition to eruption schedules, crown and root formation increments have been used to assess develop­mental age (Moorrees, Fanning, and Hunt 1963). The daily growth of 35 25 ROBSON, VAN SCHAlK, AND HAWKES TABLE 2.3 Eruption and Crown Formation Schedules for Permanent Teeth Ml M3 Eruption Age at Eruption Mean Weanil"!g Mean Species Sex (Years) (Years)! CYears) a ------------------------------------------------ Orang Unknown 4.20 (-3.5-4.9)a 7.0 -10 -3.5a -10 Gorilla Unknown 3.50 (3.0-4.0) b 2.8 11.40 (9.70-13.10) 3.50 (3.0-4.0) b 10.38 (8.70-12.10) Chimp Female 3.27 (2.75-3.75)b 4.5 11.30 (9.75-13.08) 3.19 (2.67-3.75)b 10.71 (9.00-13.08) Chimp Male 3.38 (3.00-3.75)b 4.5 11.36 (10.00-13.58) 3.33 (3.00-3.58) b 10.27 (9.00-11.08) Chimp Unknown 3.323 (2.2-4.1)C 4.5 3.218 (1.9-4.1)C Human Female 6.35 sd 0.74b 2.8 20.50 6.15 sd 20.40 0.76b Human Male 6.40sd 0.7gb 2.8 20.50 6.33 sd 19.80 0.79b I-Iuman Unknown 5.84 (4.74-7.0)d 2.8 Top values represent maxillary teeth. and lower line. mandibular teeth. Ranges are reported in parentheses. a. Smith. Crummett. and Brandt (1994) and Kelley and Schwartz (2005) b. Smith. Crummett. and Brandt (1994) c. ronro\' and rvfahonf>v (1991) and 7ihlmf'm. BolIE'f, ami ROE',)rh (2004) report maxillary Ml at alveolar margin (et>limaung lour munths from gingival emergence) 3l4.1 years In a wild chimpanzee; they report dental characteristics of seventeen immature wild chimps of known ages and conclude thal "emergence of permanent teeth in wild chimpanzees is consIstently later than 90 percent of captive individuals" (Zihlman, Bolter. and Boesch 2004:10541). d. Liversldge (2003); mean (range) of fifty-six worldwide populations e. Macho (2001): Kelley and Schwartz (2005) f. Macho (2001) g. Reid et at. (1998) h. Liversidge (2000) i. See table 2.1 for rererences. 36 26 Age at First Birth (Years)i 15.6 10.0 13.3 19.5 THE DERIVED FEATURES OF HUMAN LIFE HISTORY Ml Crown Formation (Years) 3.01 (2.90-3.12)e 2.81f 2.70f 2.90f 2.85f 2.73f 3.03f 2.62f Average Molar Crown Formation (Years/ 3.13 2.85 3.39 3.07 11 Crown Formation (Years) 4.00g 4.90 (4.45-5.35)g 4.29 (3.33-4.54)h 3.90 (3.l2-4.50)h 12 Crown Formation (Years) 4.50g 5.07 (5.00-5.15)g 4.42 (4.17-5.40)h 37 27 ROBSON, VAN SCHAlK, AND HAWKES dental microstructures, primarily crown formation and enamel depo­sition, is an especially promising line of evidence that can link aspects of dental development to absolute calendar time (Bromage and Dean 1985; Benyon and Dean 1987). Like eruption schedules, crown forma­tion is also broadly correlated with life history variation across the anthropoid primates (Macho 2001). This correlation fails, however, within the narrow phylogenetic range we consider here. Table 2.3 shows that the patterns of dental maturation and eruption in great apes do not always correspond with one another, nor with the order of fast-to-slow life histories among these species. A comparison of age at weaning in table 2.1 with Ml eruption in table 2.3 illustrates this lack of correspondence. Ml eruption follows weaning age in gorillas and chimpanzees by nine months to one year, but by more than three years in humans, whereas it precedes weaning by a similar span in orangutans. Although the age of M3 eruption is much older in later breeding humans, M3s do not erupt at an older age in the later breeding chimps and orangutans, compared with goril­las. M3 eruption misestimates age at first birth in all the nonhuman great ape species by 1-5.5 years, erupting at around 11 years in gorillas and chimpanzees and 10 years in orangutans, whereas age at first birth occurs around 10, 13.3, and 15.6 years, respectively. These data show that the life history variation among the living great apes is not closely reflected in their molar eruption schedules. Comparison of crown formation rates in table 2.3 shows that microstructure development and life history variables correspond even less well. Not only are crown formation times quite similar among the nonhuman apes, failing to track variation in either weaning ages or age at maturity, but also there is "considerable overlap among great apes and humans" in the formation rates of both incisors and molars (Macho and Wood 1995b:23). The data show that researchers must temper expectations that individual aspects of dental development (such as anterior crown formation times) are tightly tied to age at first birth (Ramirez Rozzi and Bermudez de Castro 2004) and age at wean­ing (Macho 2001). The timing of tooth eruption, crown maturation, and other aspects of dental development (Godfrey et al. 2003) varies among great ape species. Although the range of this variation is not independent of life 38 28 THE DERIVED FEATURES OF HUMAN LIFE HISTORY history, the evidence reveals that the link is not a tight one. The robust associations among life history traits themselves reflect the necessary interdependence of population vital rates (Hawkes, chapter 3, this vol­ume) , but the demographic constraints on growth and development are quite indirect. Life histories may change without concomitant shifts in all aspects of development, and, conversely, selection might favor developmental adjustments within immature stages because of particular problems faced by infants and juveniles in each species (Godfrey et al. 2003). Interbirth Intervals and Juvenile Foraging A primary life history difference between human and nonhuman great apes is the faster rate of offspring production in human females. For large-bodied mammals that produce large-bodied babies, the span between two offspring (the interbirth interval) is typically long, result­ing in slow female reproductive rates (Harvey and Clutton-Brock 1985). In primates, conception closely follows weaning of the preced­ing offspring (Pusey 1983; Graham and Nadler 1990; Watts 1991; Lee and Bowman 1995), suggesting that interbirth intervals end when an infant can successfully feed itself. Weaning is strictly defined as the cessation of infant suckling, but this definition conceals the fact that weaning is primarily a transitional process, a gradual reduction in the portion of milk ingested and a concomitant increase in solid food con­sumption, not an abrupt cessation of lactation (Sellen, chapter 6, this volume). From the start of transitional feeding, primate infants forage for the solid food they ingest, although they occasionally obtain non­milk resources through passive food sharing (Feistner and McGrew 1989). The period of transitional feeding and the interbirth interval generally end when mothers have less fitness to gain from continuing their investment in the growing offspring than from beginning another pregnancy (Trivers 1974), usually at a time when an infant can suc­cessfully obtain all its own daily calories. Offspring dependence is generally defined as the period during which the offspring drinks milk from its mother, that is, the time from birth to weaning. Some suggest a broader definition of dependence, noting that the mother provides services in addition to lactation that contribute to offspring survival (for example, Pereira and Altmann 39 29 ROBSON, VAN SCHAlK, AND HAWKES 1985) . Primate orphans provide a good measure of the timing of inde­pendence from the mother. The available data, although largely anec­dotal, suggest that suckling infants generally do not survive the death of their mother. Great ape orphan survival approaches that of no orphans if the mother is not lost before weaning age (Pusey 1983; Goodall 1986; Nishida, Takasaki, and Takahata 1990; Watts and Pusey 1993). In contrast, human infants are weaned at an age when they are still largely incapable of independent foraging and therefore continue to depend on provisioning by older individuals (Lancaster and Lancaster 1983). Data for humans show that offspring suffer poor sur­vivorship if the mother dies during the first years of a child's life (Hill and Hurtado 1991; Sear et al. 2002; Pavard et al. 2005). Thereafter, death of the mother has less effect, not because the child is indepen­dent but because others supply support (Mace and Sear 2005). Weaning and nutritional independence are not synonymous in humans as they are among the other apes. Children are weaned earli­er yet are nutritionally dependent much longer than expected for a primate with our age at maturity. It is generally assumed that children require provisioning because they lack the ecological knowledge and complex foraging skills to forage independently. Gaining these skills is thought to require a long period of learning and practice during juve­nility, an "apprenticeship," in order for human children to forage com­petently for themselves (Kaplan et al. 2000; Kaplan, Lancaster, and Robson 2003). Recent studies challenge two common assumptions about the lim­itations of children's foraging efforts and capabilities. First, many for­aging skills do not require substantial time and practice for children to master (Bliege Bird and Bird 2002; Blurton Jones and Marlowe 2002). Rather, children's foraging strategies appear to be more strongly con­strained by their diminutive size, strength. and speed than by age and experience (Bird and Bliege Bird 2005; Tucker and Young 2005). Because children cannot acquire resources that require adult size, they forage from a different diet breadth. Calculations of juvenile foraging returns in child-accessible patches reveal that children are optimal for­agers, targeting resources that yield the maximum immediate return rate (Bird and Bliege Bird 2002, 2005). These studies show that when evaluated within the constraints of their small size and strength, chil­dren are strategic and skilled foragers. 40 30 THE DERIVED FEATURES OF HUMAN LIFE HISTORY Second, Hawkes, O'Connell, and Blurton Jones (1995) have shown that foraging children can contribute more to their own subsis­tence than is widely assumed. Hadza children actively participate in food acquisition soon after weaning and throughout childhood, and these efforts make important contributions to their own nutrition. A mother often incorporates the productivity of her offspring when selecting foraging locations or resources, by choosing the strategy "that maximizes the team rate she and her children earn collectively, even if the rate she earns herself is Jess than the maximum possibJe" (Hawkes, O'Connell, and Blurton Jones 1995:695, italics original). Nevertheless, even though human juveniles can forage on their own behalf, they reside in habitats selected by adults and rarely ideal for independent juvenile subsistence. Thus, human children, unlike other ape juveniles, remain dependent upon supplemental provisioning long after they are weaned. Stacking and Cooperative Breeding With an earlier age at weaning and shorter interbirth intervals, human mothers shoulder the simultaneous nutritional dependence of multiple sequential offspring, a phenomenon we may call "stacking": mothers move on to bear another baby before the preceding one is nutritionally independent. This characteristic of humans is absent among nonhuman great apes. Great ape mothers may be accompanied by weaned subadult offspring while carrying a dependent infant, but they do not provision their offspring once weaned. Sumatran orang­utans (van Noordwijk and van Schaik 2005) tolerate the presence of weaned juveniles, but these juveniles feed themselves and tend to leave their mother before the next infant is 2 years old (although there may be a longer association in the eastern subspecies P. pygmaeus morio of the Bornean orangutans [Horr 1975; M. Ancrenaz, personal commu­nication 2005]). Maternal association with multiple immature off­spring is more apparent in chimpanzees when a just-weaned juvenile and an older juvenile approaching adolescence may travel with their mother but, again, feed themselves. Orangutan immatures develop foraging competence at about the same age chimpanzees do, and their later weaning ages may be a response to the low productivity of the Southeast Asian rainforest, in which mothers cannot afford to travel with both a new baby and a weaned juvenile (van Noordwijk and van 41 31 ROBSON, VAN SCHAlK, AND HAWKES Schaik 2005). This finding highlights the benefits that juveniles gain from association with adults. In more gregarious species, mothers may have shorter interbirth intervals because their weaned offspring need not make independent ranging choices yet. Comparing weaning ages in orangutans, chimpanzees, and gorillas, interbirth intervals vary inversely with gregariousness, and intervals are shortest in our own, especially gregarious species. Humanjuveniles not only remain in association with their mothers but also continue to depend on provisioning after the birth of a younger sibling. The caloric returns necessary for multiple dependents may exceed the abilities of a single individual forager and require con­tributions from helpers other than the mother (Kaplan et al. 2000). Fathers have long been assumed to be the primary source of help. Men differ from the males in other great ape species by regularly acquiring food that is consumed by women and children, and it is assumed that paternal benefits to improved nutrition and survival of their own offspring account for the evolution of men's work (Kaplan et al. 2000). Forager men sometimes provide a substantial component of food for their own children (for example, Marlowe 2003); among hunter-gatherer societies, higher average subsistence contributions from men are associated with higher average female fertility (Marlowe 2001). But the motives for men's contributions and the benefits they earn are disputed. Social benefits may be more important than par­enting benefits in shaping these male activities. The returns from men's hunting are unpredictable, making it an unreliable strategy for family provisioning among low-latitude foragers (Hawkes, O'Connell, and Blurton Jones 2001b). When a hunter is successful, the meat is widely shared, so his family gets little more than others (Hawkes, O'Connell, and Blurton Jones 2001a). As in primates generally, the association of adult males with youngsters can sometimes serve as mat­ing effort, mate guarding, or social bridging (Flinn 1992; Smuts and Gubernick 1992; Kuester and Paul 2000). Nevertheless, even if compe­tition for social standing is the main motivation for men's food acqui­sition, especially big game hunting, the result does provide benefits for mothers and their children (Hawkes and Bliege Bird 2002). Features of our distinctive life history, long postmenopausallifes­pans and late age at first birth, provide two more reliable sources of 42 32 THE DERIVED FEATURES OF HUMAN LIFE HISTORY potential help to mothers with multiple dependents. Postmenopausal and adolescent females lack newborns of their own and are therefore inclined to provide allomaternal assistance to gain inclusive fitness benefits (Hrdy 1999). Ethnographic and historic data show that the presence of a grandmother (especially the maternal grandmother) increases the welfare of her grandchildren (Sear, Mace, and McGregor 2000, 2003; Jamison et al. 2002; Sear et al. 2002; Voland and Beise 2002; Lahdenpera et a1. 2004; Ragsdale 2004; Tymicki 2004). When cir­cumstances permit (Hames and Draper 2004), older adolescents pro­vide important help to their mothers through the caretaking of younger siblings (Tronick, Morelli, and rvey 1992). The fact that human mothers stack nutritionally dependent offspring points to the evolutionary importance of help from provisioners other than the mother in the evolution of our life histories (Hrdy 1999). CONCLUSIONS We have compared the life histories of humans and the living great apes to develop a hypothetical life history for a common ancestor and identify changes in our lineage. A general feature of living great apes is a slow life history, so we infer that this was also true of our common ancestor. Human life histories are even slower. Humans have a signifi­cantly longer lifespan, with adults living at least twenty-five years longer than the other great apes. Human age at first birth is four to six years older than for orangutans and chimpanzees, increasing the period of juvenility and opportunity for growth. Additional time to grow results in larger human mothers who produce absolutely and relatively larger babies. Two striking deviations have shaped the pattern of slowing in human life histories: our short interbirth intervals and our vigorous postmenopausal longevity. First, slower life histories typically include longer inter birth intervals. Although humans have the longest subadult period, attain the largest body size, and produce the largest infants, we have the shortest interbirth intervals. Human infants are weaned several years earlier than might be expected of an ape with our age at maturity. Also, because women (like most primate females) con­ceive soon after a child is weaned, they bear another baby before the preceding one is capable of independent foraging. Second, women 43 33 ROBSON, VAN SCHAlK, AND HAWKES stop bearing offspring by their early 40s. The age at which fertility declines to menopause appears to be essentially the same in women as in the other apes, indicating that this trait may be conserved across the great ape radiation. The distinctively early weaning of human infants and stacking of dependent offspring could evolve only if human moth­ers had a reliable source of help. Postmenopausal grandmothers and adolescents, because they themselves did not have infants, likely sup­plied that help. We have also highlighted the imperfect correspondence among various aspects of growth and development in brains and teeth and between those developmental variables and the life history traits that are tied to population vital rates. Our exploration of the cross-species variation among great apes and humans in these dimensions is only a beginning. More is clearly in order. Acknowledgments We thank Sarah Hrdy, Eric Rickart, Earl Keefe, Nick Blurton Jones, Dan Sellen, and the SAR participants for valuable input and discussion. We also thank Jennifer Graves for careful editing. 44 References Alvarez HP 2000 Grandmother hypothesis and primate life histories. American Journal of Physical Anthropology 133:435-450. 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Robson 1 and Bernard Wood 2 1 Department of Anthropology, University of Utah, Salt Lake City, UT, USA 2 Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, Washington DC, USA Abstract In this review we attempt to reconstruct the evolutionary history of hominin life history from extant and fossil evidence. We utilize demographic life history theory and distinguish life history variables, traits such as weaning, age at sexual maturity, and life span, from life history-related variables such as body mass, brain growth, and dental development. The latter are either linked with, or can be used to make inferences about, life history, thus providing an opportunity for estimating life history parameters in fossil taxa. We compare the life history variables of modern great apes and identify traits that are likely to be shared by the last common ancestor of Pan-Homo and those likely to be derived in hominins. All great apes exhibit slow life histories and we infer this to be true of the last common ancestor of Pan-Homo and the stem hominin. Modern human life histories are even slower, exhibiting distinctively long post-menopausal life spans and later ages at maturity, pointing to a reduction in adult mortality since the Pan-Homo split. We suggest that lower adult mortality, distinctively short interbirth intervals, and early weaning characteristic of modern humans are derived features resulting from cooperative breeding. We evaluate the fidelity of three life history-related variables, body mass, brain growth and dental development, with the life history parameters of living great apes. We found that body mass is the best predictor of great ape life history events. Brain growth trajectories and dental development and eruption are weakly related proxies and inferences from them should be made with caution. We evaluate the evidence of life history-related variables available for extinct species and find that prior to the transitional hominins there is no evidence of any hominin taxon possessing a body size, brain size or aspects of dental development much different from what we assume to be the primitive life history pattern for the Pan-Homo clade. Data for life history-related variables among the transitional hominin grade are consistent and none agrees with a modern human pattern. Aside from mean body mass, adult brain size, crown and root formation times, and the timing and sequence of dental eruption of Homo erectus are inconsistent with that of modern humans. Homo antecessor fossil material suggests a brain size similar to that of Homo erectus s. s., and crown formation times that are not yet modern, though there is some evidence of modern human-like timing of tooth formation and eruption. The body sizes, brain sizes, and dental development of Homo heidelber-gensis and Homo neanderthalensis are consistent with a modern human life history but samples are too small to be certain that they have life histories within the modern human range. As more life history-related variable information for hominin species accumulates we are discovering that they can also have distinctive life histories that do not conform to any living model. At least one extinct hominin subclade, Paranthropus , has a pattern of dental life history-related variables that most likely set it apart from the life histories of both modern humans and chimpanzees. Key words dentition; encephalization; evolution; growth and development; hominin life history. Introduction Compared to other great apes modern humans have a higher rate of survival, live longer, start reproducing later, and have shorter interbirth intervals (reviewed in Leigh 2001; Robson et al. 2006). To reconstruct the recent evolu-tion of these characteristics of modern human life history we review the life histories of closely related extant and fossil taxa. We also discuss the probable life histories of Correspondence Shannen L. Robson, Department of Anthropology, University of Utah, 270 South 1400 East room 102, Salt Lake City UT 84112, USA. E: [e-mail] Accepted for publication 22 January 2008 48 Hominin life history: reconstruction and evolution, S. L. Robson and B. Wood © 2008 The Authors Journal compilation © 2008 Anatomical Society of Great Britain and Ireland 395 (1) the hypothetical last common ancestor (LCA) of the chimpanzee/bonobo and modern human ( Pan - Homo ) clade, (2) the hypothetical stem hominin taxon, (3) the taxa that make up the major grades within the hominin clade, and (4) the evolution of life history within the major subclades within the hominin clade. Comparing the life history of the living primates most closely related to modern humans enables researchers to generate hypotheses about what modern human life history traits are conserved and which are derived. Direct evidence about non-human great ape life history has been gleaned by meticulous observation both in the field and from captive animals (see Kappeler & Pereira, 2003; van Schaik et al. 2006). These data, combined with molecular and other information about how their phylo-genetic histories are related (see Bradley, 2008), contri-butes to reconstructing the life history of the LCA of the Pan - Homo clade. But in order to investigate the more recent evolutionary context of modern human life history, researchers must examine whatever evidence is available about the life history of closely-related extinct animals. If we make the untested assumption (see below) that the common ancestor of the Pan - Homo clade had a life history that is more like that of modern chimpanzees than that of modern humans, we must look at the fossil evidence of creatures that are more closely related to modern humans than to Pan (that is the hominin clade) to investigate the recent evolution of modern human life history. Inferences about the life history of extinct hominin taxa must be extracted from fossilized remains of the hard tissues. Even this indirect information about the life his-tory of fossil hominins is useful. If the taxon is directly ancestral to modern humans (but see Wood & Lonergan, 2008; for the reasons why this hypothesis is difficult to test and verify for most early hominin taxa) it provides evidence about an earlier stage in the evolution of modern human life history. If the taxon belongs to an extinct hominin subclade it might help throw light on the factors that determine and constrain how life history is configured more widely within the hominin clade. In this contribution we have two primary aims: first to reconstruct the recent evolutionary history of hominin life history from extant and fossil evidence, and second to assess when, in what taxon or taxa, and at what pace, the distinctive components of modern human life history appear within the hominin clade. In the first section of our contribution we compare the life histories of the living great apes (orangutans, gorillas, chimpanzees, bonobos and modern humans) to identify traits that are likely to be derived in hominins, and thus suggest the likely life history of the Pan - Homo LCA, and the stem hominin. We distinguish life history variables (LHVs), traits such as age at weaning, age at sexual maturity, and life span that can only be measured in living populations, from life history-related variables (LHRVs). The latter are variables that can be used to make inferences about life history. Given the inability to collect standard life history data from fossil material, we evaluate how well three LHRVs, body mass, brain size and dental development, serve as accurate proxies for the timing of life history events in the extant great apes. In the second section we address how different taxonomic schemes influence the analysis of hominin life history patterns by using both a relatively speciose (or ‘splitting') taxonomy, as well as a less speciose (or ‘lumping') taxonomy (see Wood & Lonergan, 2008). We then summarize what can be deduced about the evolution of the major elements of life history within the hominin clade. This includes an assessment of when, and in which taxa, the distinctive aspects of modern human life history make their appearance. Finally, we consider the implications of these data for hypotheses about the first appearance of a modern human-like life history and evaluate how well the hominin fossil evidence supports the predictions made using comparative primate data. Specifically, we address three key questions: (1) Did the unique features of modern human life history appear suddenly as one integrated package, or did the components evolve independently and incrementally? (2) Did the onset of modern human life history coincide with the appearance of larger-bodied hominins with a modern human skeletal proportions, or did it appear later in hominin evolution? (3) Are modern human and modern chimpanzee life histories the only ways that life history has been configured within the Pan - Homo clade, or is there evidence within the fossil hominin record of creatures that have a different life history pattern? Part I. Life history and life history-related variables of extant hominids All organisms pass through major life stages and life history theory seeks to explain cross-species differences in the timing and covariation of these stages. It has been well established across a broad array of species that the timing of major life events tends to be correlated, even when the effects of body size are removed (Harvey & Read, 1988; Read & Harvey, 1989). A shift in the timing of one event results in a concordant extension or compression in the span between the occurrence of other events (Charnov, 1991). Primates in general, and great apes in particular, have slow life histories, with comparatively long life stages: late ages at maturity, low birth rates with small litter sizes, and long adult life spans (Charnov & Berrigan, 1993). The pace of life history is largely determined by age-specific mortality rates. Generally, species that suffer high rates of adult mortality, that is, a high probability of dying during one's reproductive years, tend to have fast life histories, whereas those with low adult mortality exhibit slower life histories (Harvey et al. 1989). Shifts in adult survival or mortality risk alter the pace of linked life 49 Hominin life history: reconstruction and evolution, S. L. Robson and B. Wood © 2008 The Authors Journal compilation © 2008 Anatomical Society of Great Britain and Ireland 396 history events, and also the constraints important for optimizing growth and development (Hawkes, 2006a). Many published lists of life history variables are confla-tions of two different categories of information (Skinner & Wood, 2006), which we distinguish in Table 1. The first category (A) consists of variables such as gestation length, age at weaning, longevity, interbirth interval, and age of first and last reproduction. These variables reflect popula-tion vital rates and the timing of life history events, and we will refer to these as ‘life history variables' (or LHVs). With the possible exception of weaning (Humphrey et al. 2007), we cannot yet make direct observations about life history variables on extinct taxa and thus we are reduced to making inferences about life history from qualitative or quantitative information about ontogeny gleaned from the hominin fossil record. This second category (B) consists of variables such as body mass and brain size (e.g. Sacher, 1975; Martin, 1981; Martin, 1983; Hofman, 1984; Smith, 1989, 1992; Smith & Tompkins, 1995; Smith et al. 1995; Godfrey et al. 2003) that have been shown empirically within extant primates to be constrained by, or correlated with, LHVs. To distinguish them from first-order life his-tory variables we follow Skinner & Wood (2006) and refer to the second-order category B variables as ‘life history-related variables' (LHRVs). We examine first what LHV data are available for the extant great apes, focusing solely on females for several reasons. Female fertility rates and mortality rates determine population growth and age structure and are typically slower than male potential reproductive rates. Males must compete for paternity opportunities set by female fertilities, a limitation that has important consequences for male life histories, especially with respect to reproductive strategies (Kappeler & Pereira, 2003). In addition, many important life history variables are either restricted to females (such as gestation length, lactation, and interbirth intervals) or are difficult to ascertain for males (such as parity). We then consider in more detail how (and, more importantly, how reliably) LHRVs can be inferred from the evidence pro-vided by the hominin fossil record. Which apes resemble the first hominins? Modern humans are part of the wider radiation of great apes as shown in Fig. 1. We follow the standard two species taxonomy for our closest living relatives in the genus Pan : the common chimpanzee ( Pan troglodytes ) and the bonobo ( Pan paniscus ). Although differences between the three chimpanzee subspecies are small (Fischer et al. 2006), recent evaluation of genetic differences among chimpanzees supports the traditional taxonomic designa-tion of three geographically distinct lineages (Becquet et al. 2007). The two other non-human great apes, gorillas and orangutans, are currently in a state of taxonomic flux. Gorillas were traditionally classified as a single species with various distinct subspecies, but recently the eastern and western gorilla populations have been accorded species status as Gorilla gorilla and Gorilla beringei , respectively (Groves 2001, 2003; Thalmann et al. 2007). Similarly, two species are recognized within the orangutan genus Pongo , Pongo pygmaeus from Borneo and Pongo abelii from Sumatra (Zhang et al. 2001). While these revisions recognize important species differences within orangutans and gorillas, there are insufficient species-specific long-term life history data to justify us distinguishing Table 1 Life history and life history-related variables and their present availability for extinct taxa Available for extinct taxa* Life history variables (LHVs) Gestation length No Age at weaning No? Age at first reproduction No Interbirth interval No Mean life span No Maximum life span No Life history-related variables (LHRVs) Body mass Adult Yes Neonatal Yes??? Brain mass† Adult Yes Neonatal Yes??? Dental crown and root formation times Yes? Dental eruption times Yes? *Availability designated as ‘Yes' means that reasonable sample sizes (but not necessarily reliable estimates) are available f