Growth, Development, and Life History throughout the Evolution of Homo
Abstract
For over a century, paleoanthropologists have listed the presence of prolonged periods of gestation, growth, and maturation, extremely short interbirth intervals, and early weaning among the key features that distinguish modern humans from our extant ape cousins. Exactly when and how this particular scheduling of important developmental milestones—termed a “life history profile”—came to characterize Homo sapiens is not entirely clear. Researchers have suggested that the modern human life history profile appeared either at the base of the hominin radiation (ca. 6 Ma), with the origins of the genus Homo (ca. 2.5 Ma), or much later in time, perhaps only with H. sapiens (ca. 200–100 Ka). In this short review, evidence of the pace of growth and maturation in fossil australopiths and early members of Homo is detailed to evaluate the merits of each of these scenarios. New data on the relationship between dental development and life history in extant apes are synthesized within the context of life history theory and developmental variation across modern human groups. Future directions, including new analytical tools for extracting more refined life history parameters as well as integrative biomechanical and developmental models of facial growth are also discussed.
Introduction
Compared with our closest living relatives—the extant great apes—the sole surviving member of the genus Homo possesses a suite of features that make us quite distinct, including unusually large brains, obligate bipedality, a reliance on the production and use of tools, and a strikingly different life history. Generally, patterns of mammalian growth, development, and life history are thought of as lying along a spectrum somewhere between two end points that are colloquially referred to as “live fast, die young” and “live slow, die old.” Modern human life history incorporates elements of both schedules: long gestation periods, altricial offspring, enlarged brains, slow maturation rates, increased life span, and protracted periods of offspring dependence are suggestive of a “live slow” strategy, whereas relatively early weaning, short interbirth intervals, and the ability to overlap births (resulting in the presence of multiple offspring) are suggestive of a “live fast” schedule. Of interest to paleoanthropologists is whether this “modern human life history package” evolved as a single developmental module or accumulated in a mosaic fashion (with different attributes appearing at different points in time). Furthermore, it is of great interest to understand when this transition occurred and thus determine whether the human life history package appeared as part of a suite of fundamental adaptations at the base of the hominin clade; whether it evolved somewhat later, perhaps tied to the reorganization of the cranium and postcranium that characterized the earliest members of the genus Homo; or whether it appeared even later still, perhaps in the last hundred thousand years or so.
The last decade has been marked by a tremendous amount of research into reconstructing the pattern of growth, development, and life history of extant great apes, australopiths, and early to later members of the genus Homo. Novel analytical techniques, imaging modalities, and hard-fought observational data from naturalistic studies of great apes can now be synthesized to paint a broad view of the evolution of life history throughout the course of the human story. The goal of this paper is to review the current state of knowledge of the evolution of human life history within the comparative context of what we know about these attributes in populations of extant hominoids and fossil hominins. These data will be evaluated within the light of what is known about primate life history, ecology, diet, and so forth, and will be used to help suggest future avenues of inquiry into studies of hominin life history.
What Is Life History?
By marrying the principles of organic evolution with those of theoretical population ecology, life history theory seeks to understand the general rules that account for the tremendous variation in life cycles across all organisms (Stearns 1992). In short, life history theory views variation in the pattern, sequence, and pace of growth as the outcome of how natural selection operates on a series of trade-offs in the allocation of an organism’s energetic budget. Smith and Tompkins (1995:257) emphasized the importance of these trade-offs in defining life history as the allotment of an organism’s energy “towards, growth, maintenance, reproduction, raising offspring to independence, and avoiding death.” Bogin (1988:154) suggested that the life history of a species can be viewed as a strategy that determines “when to be born, when to be weaned, how many and what type of prereproductive stages of development to pass through, when to reproduce, and when to die.” Central to these and other definitions is the notion that energy is a limiting commodity that is distributed toward growth, maintenance (of tissues), and/or reproduction throughout the lives of individuals (Bogin and Smith 2000; Roff 2002; Stearns 1992). In a strict Darwinian sense, selection should favor an apportionment of energy in ways that reduce mortality and maximize fecundity. Thus, the application of life history theory to ontogenetic studies seeks to understand how the scheduling of key events in an organism’s life cycle (including but not limited to gestation length, age at weaning, interbirth interval, timing of maturation, age at first reproduction, frequency of reproduction, fecundity, and life span) better enable some individuals of a species to minimize mortality risks more effectively and thus increase overall fitness. This scheduling or sequence of events can be thought of as a “life history profile” and is, effectively, the product of how developmental variables (e.g., growth rates, age at skeletal maturation) interact with demographic variables (e.g., survival, reproduction, population growth) to influence individual survival (Godfrey, Petto, and Sutherland 2002; Ross 1998).
Aside from being viewed as an energetic trade-off, a species’ life history profile is directly linked to rates of extrinsic mortality, which is defined as the risk of death as a result of environmental conditions such as predation, disease, accidents, and so forth (Stearns 1992). High extrinsic mortality should favor shorter life spans, while lower extrinsic mortality results in a larger proportion of the population surviving to older ages. Compared with great apes, human populations are able to ramp up reproductive success because our life history profile is characterized by lower mortality rates, which has the effect of slowing down rates of maturation, delaying reproduction, and thus spreading it out across later years. For a large primate, a strategy including a prolongation of growth and development comes with some risk, as evidenced by recent data on the inability of orangutan populations (with late ages of reproductive maturity and interbirth intervals of ∼7 years) to recover from even slight reductions in population density (Knott, Thompson, and Wich 2009). At a finer scale of comparison (i.e., across populations of modern Homo sapiens), differences in subsistence strategies, environments, and mortality rates comingle to produce tremendous variation in patterns of human ontogeny (e.g., Migliano and Guillon 2012). For instance, in a survey of 22 small-scale societies, Walker et al. (2006) found that populations experiencing low survivorship (i.e., high mortality) during the subadult years were characterized by an overall pattern of accelerated development and thus reached the important developmental milestones of puberty, menarche, and first reproduction at relatively earlier ages. Interestingly, new evidence suggests that adverse early life conditions in humans, ranging from the biological (low birth weight for gestational age, breast-feeding duration) to the psychosocial (separation anxiety, family residential relocation, degree of parental involvement) mediate reproductive scheduling by accelerating the age at first pregnancy (Nettle, Coall, and Dickins 2010 and references therein). A more detailed understanding of exactly how such environmental constraints, broadly speaking, shape life history variation across human populations would be extremely informative. Similarly, uncovering the role developmental plasticity (the capacity of an individual to modify its ontogeny in response to shifting environmental conditions on a fairly rapid timescale—days, months, or a few years) plays in generating novel phenotypes that enhance the evolutionary potential, or “evolvability,” of developmental systems may help illuminate the process(es) whereby selection assembled the total package of modern human life history attributes over a period of several hundred thousand years (e.g., see Kuzawa and Bragg 2012; West-Eberhard 2003).
Reconstructing Hominin Life History Profiles
When viewed in the light of life history theory, it might seem impossible to infer such reproductive, physiological, demographic, environmental, and behavioral parameters from fossilized remains. However, the vast majority of the hominin fossil record comprises isolated teeth and dentognathic remains, and many of the important life history variables discussed above are tightly linked with aspects of developing dentitions. As a result, studies on the timing of particular dental developmental events figure prominently in paleoanthropological investigations that aim to reconstruct the life history profiles of fossil primates and hominins (e.g., Beynon et al. 1998; Bromage and Dean 1985; Conroy and Kuykendall 1995; Conroy and Vannier 1991a, 1991b; Dean et al. 1993, 2001; Godfrey et al. 2001; Mann 1975; Robson and Wood 2008; Schwartz et al. 2005; Smith 1989, 1993; Smith, Crummett, and Brandt 1994; Smith, Gannon, and Smith 1995; Smith et al. 2010a, 2010b; Zihlman, Bolter, and Boesch 2004).
Ever since the pioneering studies on primate growth by Schultz (1935, 1940, 1960) and Sacher (1959, 1975, 1978; Sacher and Staffeldt 1974), evolutionary biologists and paleoanthropologists have linked aspects of somatic and neural growth rates to reproduction, metabolism, and life span in an attempt to reconstruct aspects of early hominin maturation. The first study to flesh out the relationship between the sequence and pace of dental development and aspects of life history was by Schultz (1949), who observed that the permanent replacement molars emerge into the oral cavity before the shedding of deciduous teeth in faster-growing primates. This phenomenon has since been dubbed “Schultz’s rule” (Smith 2000) and accurately relates dental emergence sequences to maturation rates across primates as a whole, especially anthropoids (see Godfrey et al. 2005). It also allowed paleoanthropologists an opportunity to evaluate when the modern human developmental pattern (i.e., tooth crown development and emergence sequence) first appeared during the course of human evolution as it could be used to assess the relative developmental status of juvenile hominins (Smith 1986). Along with other studies examining the sequence of dental development and emergence in hominins (e.g., Conroy and Kuykendall 1995; Conroy and Vannier 1991a, 1991b), it became increasingly clear that the earliest hominins, and indeed even fossil species of the genus Homo, were characterized by dental developmental patterns, and thus maturational profiles, more similar to extant apes (at the time, meaning predominantly Pan troglodytes). This work was extremely important because the prevailing paradigm held that all hominins, including the earliest australopiths, possessed a modern humanlike maturation profile with the attendant prolonged infant and childhood dependency that was so fundamental to producing the social, cognitive, and cultural complexity that serves as the hallmark of our species (Mann 1975).
Given the intimate relationship between brain size, life span, and rates of maturation and the plasticity of certain reproductive parameters, Smith (1989) reasoned that the dentition should be one of the more stable markers of growth given its high heritability and resistance to environmental perturbations. She conducted a broad, interspecific comparison of dental maturation with various life history variables and revealed the extremely high correlation between brain size and the age at first molar (M1) emergence on the one hand and between M1 emergence age and various life history variables related to reproduction (gestation length, ages at weaning and first breeding, life span) on the other. This seminal study laid the groundwork for linking aspects of the timing or pace of dental development to critical components of a species’ life history and, equally importantly, provided a chronological marker for probing the maturation rates of fossils if information on the timing of key dental development events (i.e., M1 emergence) could somehow be retrieved from the fossil record.
At around the same time, a group of paleoanthropologists began to mine the rich vein of growth data contained within teeth. Based on some foundational work in dental hard tissue biology (Boyde 1963, 1964), a series of investigations began to appear that documented how to retrieve information on the absolute timing of dental development utilizing the growth record contained within enamel and dentine. The cells that secrete the dental tissues enamel and dentine (for reasons of brevity, cementum is not discussed here) leave a record of their activity in the form of short- and long-period incremental growth lines. These include, respectively, daily cross striations and Retzius lines in the enamel and the corresponding von Ebner and Andresen lines in dentine (Dean 1987, 2006; Schwartz and Dean 2000; Smith 2006, 2008). Careful counts of these lines reveal the time taken to form a tooth, including the tooth crown and however much root had formed at the time of death, thereby providing a detailed chronology of dental development that can, under the right circumstances, also yield precise ages for key events such as molar emergence (e.g., Beynon, Dean, and Reid 1991; Dean et al. 2001; Dirks 1998; Kelley and Schwartz 2010; Smith, Reid, and Sirianni 2006; Smith et al. 2010a, 2010b).
Data on molar emergence ages in hominins, while rare, are becoming more accessible, especially with the application of new, noninvasive imaging modalities that allow access to the internal dental growth record (e.g., Smith et al. 2007b, 2007c, 2010b). While it is critically important to establish a growing database on molar emergence ages in key hominin taxa, it is also necessary to chart more fully dental developmental variation in extant hominoids and to interpret that variation in light of a particular species’ population ecology, demography, and life history. For now, good population data on molar emergence ages exist only for P. troglodytes (Anemone, Mooney, and Siegel 1996; Conroy and Mahoney 1991; Kuykendall, Mahoney, and Conroy 1992; Nissen and Reisen 1945, 1964; Reid et al. 1998; Schultz 1940; Smith et al. 2007a, 2010a; Zihlman, Bolter, and Boesch 2004; though see Dirks 2003 and Dirks and Bowman 2007 for individual hylobatids; and Beynon, Dean, and Reid 1991; Winkler, Schwartz, and Swindler 1991; and Kelley and Schwartz 2010; and Willoughby 1978 for individual gorillas and orangutans). There is also a growing awareness that emergence ages for captive primate populations may be slightly advanced compared with wild populations (e.g., Kelley and Schwartz 2010; Smith and Boesch 2011; Zihlman, Bolter, and Boesch 2004), suggesting at the very least some caution in relying on databases derived exclusively from captive colonies. Expanding our knowledge of dental developmental variation across natural fertility populations of modern humans is another key element (e.g., Liversidge 2003) and will ultimately allow more fine-scale tests of how population-level variation in aspects of dental development (e.g., M1 emergence age) relates to that for various life history attributes.
Early Homo
It has generally been viewed that the origin of the genus Homo was characterized by a trend away from bipedal apelike forms to obligate terrestrial bipeds who were endowed with much larger brains and the capacity to manufacture and use stone tool technology and who also exhibited a shift in dietary and foraging adaptations. Fossil representatives of the genus Homo were first described by Leakey, Tobias, and Napier (1964) from material derived from Bed I, Olduvai Gorge, Tanzania, and were dated to 1.8–1.7 Ma. These authors viewed the material as distinct from australopith material given its possession of a larger, more globular and gracile cranium with a cranial capacity >600 cm3 and a concomitant reliance on the habitual production and use of lithic technology. Fossil evidence for even earlier representatives of Homo includes mostly isolated specimens from South Africa (Sterkfontein, ca. 2.6 Ma), Kenya (Chemeron, 2.4 Ma), and Malawi (Uraha, ∼2.5–1.9 Ma), with a maxilla from Hadar, Ethiopia (A.L. 666-1, 2.3 Ma) being the best candidate for the earliest Homo (Kimbel, Johanson, and Rak 1997; see recent review in Kimbel 2009), thereby extending the origin of Homo further back in time to at least 2.5 Ma, to a time when Africa was undergoing a transition toward cooler, drier conditions with an increase in more open habitats (see also Potts 2012). Regardless of the precise time and location of the origins of our own genus—though it is generally held to be within the critical interval of 3–2.0 Ma—many paleoanthropologists support the usage of Leakey, Tobias, and Napier’s morphological-behavioral complex (increased brain size, stone tool production) as the sole criterion for inclusion within the genus and would therefore recognize three securely attributed representative species of premodern early Homo in Africa: Homo habilis (1.9–1.4 Ma), Homo rudolfensis (1.9–1.8 Ma), and Homo ergaster and Homo erectus (1.9–0.9 Ma; see Antón 2012; Kimbel 2009; and Wood and Lonergan 2008 for recent reviews of the fossil evidence of Homo).
Not everyone would include the “transitional” species of H. habilis and H. rudolfensis within the genus Homo. Wood and Collard (1999) maintained that all members of a genus should occupy the same adaptive zone (and thus possess a similar adaptive strategy) and proposed a set of criteria for the inclusion of any species into the genus Homo. Based on its large body size, body proportions, reduced dentition, and commitment to long-range bipedality, they recommend that H. ergaster be the earliest hominin to satisfy their adaptive criteria, thereby relegating both of the earlier “Homo” species to the genus Australopithecus. Recent metric analyses, however, demonstrate similarities in some of these anatomical complexes (limb lengths and proportions) and suggest that reassigning these species may be unwarranted (Holliday 2012).
Regardless of generic assignations, many of the hominins before 2.5 Ma can be broadly characterized as relatively small-brained, large-toothed, non–stone tool producing human ancestors (though recent work suggests that some australopith taxa may have been using stone tools; McPherron et al. 2010). As such, it may seem reasonable to postulate some sort of grade shift in life history during this critical interval. Alternatively, species of early Homo (and Australopithecus for that matter) might each possess slightly different life histories, as these profiles are closely calibrated to local environment and ecologies, and the critical time interval for the evolution of Homo (3–2.0 Ma) is characterized by magnified climate variability and thus variable adaptive settings (deMenocal 1995; Potts 1996, 2012).
What Do We Know about Life History in Early Homo?
In short, not as much as we would like to know. This is in part because an organism’s “strategy” for parsing out energy for purposes of growth, maintenance, and/or reproduction (i.e., their gestation length, age at weaning, interbirth interval, timing of maturation, frequency of reproduction, fecundity, and life span) is not a durable part of the fossil record. Importantly, there are now some good attempts at deriving gestation length, interbirth intervals, and weaning age from hard tissue remains for certain primate taxa (see Dirks et al. 2010; Humphrey et al. 2008a, 2008b; Schwartz et al. 2002), though how fruitful they will be if applied to fossil human taxa is currently unknown.
For several decades, paleoanthropologists have viewed the evolution of modern human growth, development, and life history through the lens of a comparative dichotomy between modern Pan on the one hand and modern humans on the other. This is not unreasonable given that recent DNA analyses support a Pan-Homo clade to the exclusion of all other hominoids (e.g., Bradley 2008; Ruvolo 1994). It is interesting, however, that several early hominin specimens exhibit striking anatomical similarities with extant gorillas (Dean 2010). For instance, certain aspects of scapular morphology in the recently discovered Dikika skeleton and the mandibular morphology of other Australopithecus afarensis specimens bear a close resemblance to the condition in extant Gorilla (Alemseged et al. 2006; Rak, Ginzburg, and Geffen 2007). Unfortunately, not enough is currently known about development in Gorilla, or developmental variation among Gorilla spp., to speculate on the importance of this for understanding how best to model the mosaic pattern of great ape morphology/dental development evident within australopiths and perhaps early Homo (Dean 2010).
What we have been able to reconstruct about life history in early Homo, and indeed for several earlier and later hominins, is based on estimates of the pattern and pace of dental development or on the tight association between brain size and life history (or some skeletal correlate of life history). Thus, a series of key questions related to understanding the ontogeny of early Homo can now be asked. Is there evidence that the earliest hominins (including the earliest members of the genus Homo) matured in a way—had a chronology of dental development—that was similar to extant chimpanzees (and moreover, do all extant apes mature, dentally, in an identical manner)? Do the early hominins differ in the chronology of tooth emergence in ways that might suggest developmental heterogeneity in their reconstructed life history profiles? Do the earliest representatives of the genus Homo exhibit dental developmental chronologies that align them more closely with the penecontemporaneous australopiths or with geologically younger Neanderthals and archaic Homo sapiens populations?
Inferences from extant ape development
We know more about chimpanzee growth, development, diet, and ecology than we do for any other ape, and with the exception of baboons, perhaps for any other primate. Dean (2010) recently synthesized all that is known about dental development in Pan, revealing some interesting similarities with and differences from modern humans. Overall, chimpanzee dental development occurs along an accelerated schedule, taking ∼12 years compared with 18 years in modern humans. This acceleration is reflected in advanced median molar emergence ages that occur well before those of humans. The first mean gingival emergence ages for chimp M1s were reported to be 3.3 years (range of 2.6–3.8 years; Nissen and Reisen 1964). After three more decades of studies on captive chimps, median emergence ages for M1s are reconstructed as quite close to that original estimate, at 3.2 years (M1 range, 2.26–4.38 years; M1 range, 2.14–3.99 years; Kuykendal, Mahoney, and Conroy 1992). Thus, for several decades, it was generally taken that M1 emergence in Pan, and thus for African apes as a whole, occurred somewhere in the range of 3.0–3.5 years. By comparison, the range for modern humans calculated across global populations averages 4.7–7.0 years (Liversidge 2003).
Given the presence of the so-called “wild effect” (sensu Smith and Boesch 2011; see also Hamada et al. 1996; Kimura and Hamada 1996), it became critical to evaluate gingival emergence ages in wild populations. To date, the only reliable estimate for age at M1 emergence in noncaptive apes is a single individual of Pan troglodytes verus at approximately 4.1 years for the maxillary M1. The likely age of emergence for the mandibular M1 in this individual was approximately 3.8–3.9 years, resulting in a combined age of M1 emergence of approximately 4.0 years (Smith et al. 2010a; Zihlman, Bolter, and Boesch 2004). Interestingly, a recent analysis by Dean (2010) using data from the histological growth record of crowns and roots found that the predicted mean age of attainment for molar emergence in Pan M1 is 4.1 years, nearly coincident with that reported in the wild P. troglodytes verus individual.
To date, no reliable gingival emergence data exist for any great ape species other than the common chimpanzee. This deficiency may limit the accuracy and reliability of life history reconstructions for fossil hominins, and so it is critical to obtain M1 emergence data for both African and Asian apes and to obtain these data from noncaptive animals. Recently, reliable ages at M1 emergence were reported for orangutan (Pongo pygmaeus pygmaeus, 4.6 years) and gorilla (Gorilla gorilla gorilla, 3.8 years) obtained from wild-shot individuals in museum osteology collections (Kelley and Schwartz 2010). These data offer support for the likelihood of a later average age at M1 emergence in free-living chimpanzees than in captive animals. Although limited, they also suggest that the average age at M1 emergence in noncaptive extant great apes ranges from just younger than 4 years to just older than 4.5 years, or approximately 1 year later than the conventional range reported as ∼3.0–3.5 years.
These new comparative data allow an evaluation of just how consistent M1 emergence data are with the comparative life histories of extant Asian and African apes and modern humans. As can be seen from table 1, the new ape emergence data fit well with expectations based on the comparative life histories of living hominoids both in relation to one another and in comparison with that of modern humans. Ages at M1 emergence between 3.8 and 4.6 years for great apes represent ∼65%–80% of modern human emergence at ∼6 years (
years, mean ± 1 SD), signaling a close fit between ages at attainment (or duration) of some key life history events in great apes, as these life history attributes are also ∼60%–80% of the modern human value. As a side note, and by comparison, gingival emergence ages of 3.0–3.5 in extant apes would represent only ∼50%–60% of the average modern human value. These new data reinforce earlier studies (Smith 1989) that identified dental eruption as a reliable means by which to reconstruct life history profiles in extinct hominins.
Comparative life history and M1 emergence age (years) in extant great apes and humans
| Variable | Gorilla | Pan | Pongo | Homo |
|---|---|---|---|---|
| Age at first reproduction | 10.1a (51.3) | 14.3b (72.6) | 15.7c (79.7) | 19.7 |
| Interbirth interval | 4.3 | 5.8b | 6.9c | 3.4d |
| Survivorshipe | 20.6f (38.1) | 29.7 (54.9) | 43.0 (79.5) | 54.1 |
| Age at M1 emergence | 3.8 (65.5) | 4.0b (69.0) | 4.6c (79.3) | 5.8 |
| Cranial capacity (cm3) | 484 | 383 | 379 | 1,293 |
Unfortunately, reliable ages at M1 emergence are available for a very small number of fossils. It is difficult to extract these data given the relatively few specimens that died during the eruptive process of M1 and the difficulty in arranging for these specimens to be subjected to the latest in noninvasive imaging technology. Rather, utilizing the incremental growth record contained within dental hard tissues, estimates of the age at death for juveniles with mixed dentitions (both deciduous and permanent teeth present) near or subsequent to M1 gingival emergence do exist for a handful of australopiths and early and later species of the genus Homo. These age-at-death estimates can thus be used as the basis for estimating ages at M1 emergence (table 2; Kelley and Schwartz 2012). All of the australopith emergence age estimates resemble extant African apes more than they do modern humans, and this also holds for the earliest members of the genus Homo (H. erectus, H. ergaster) for which there are reliable data.
Estimated ages (years) at death and M1 emergence in great apes, australopiths, and Homo
| Species (specimen) | Estimated age at death | Age at M1 emergence |
|---|---|---|
| Great apes: | ||
| Pongo pygmaeus pygmaeus | 4.6 | |
| Gorilla gorilla beringei | 3.8 | |
| Pan troglodytes verus | 4.0 | |
| Australopiths: | ||
| Australopithecus afarensis (LH 2) | 3.25 | 2.9* |
| Australopithecus africanus (Sts 24) | 3.30 | 2.9* |
| A. africanus (Taung 1) | 3.73–3.93 | 3.3–3.5* |
| Paranthropus robustus (SK 62) | 3.35–3.48 | 3.8–3.9* |
| P. robustus (SK 63) | 3.15–4.23 | 2.9–3.2* |
| Paranthropus boisei (KNM-ER 1820) | 2.5–3.1 | 2.7–3.3* |
| Homo: | ||
| Homo erectus (Sangiran S7-37) | 4.4* | |
| Homo ergaster (KNM-WT 15000) | 8.3–8.8 | 4.5* |
| Homo neanderthalensis (La Chaise) | 6.7* | |
| Homo sapiens (Global) | 5.8 (4.7–7.1) |
An important way to evaluate these calculated ages at M1 emergence is in the context of its relationship with cranial capacity. As mentioned earlier, cranial capacity and age at M1 emergence are strongly correlated in extant anthropoids (Godfrey et al. 2001; Smith 1989), and both exhibit a high correlation with aspects of life history. As is evident in figure 1, all of the great apes fall on or above the regression line, with Gorilla having the relatively earliest age at M1 emergence, as might be expected given its more folivorous diet (see Godfrey et al. 2001). Humans fall well below the regression line, but it is most reasonable to attribute this to the tremendous increase in cranial capacity in human populations during the later Pleistocene, which has seemingly forced a partial dissociation between cranial capacity and age at M1 emergence. Without this dissociation, M1 emergence (with a predicted mean age of 7.1 years using the regression model versus the actual modern human interpopulation mean of ∼5.8 years) as well as the subsequent emergence of the more posterior molars would be delayed perhaps beyond ages that are fully compatible with weaning and the food-processing requirements of adolescent growth. All of the australopith and early Homo specimens (and thus, perhaps, species) also fall below the regression line, indicating that these species were also characterized by a relatively advanced age at M1 emergence for their brain size.
Bivariate plot of ln M1 emergence age in months (y) versus ln cranial capacity in cubic centimeters (x) for a sample of anthropoids (taxa include Callithrix jacchus, Saguinas fuscicollis, Saguinas nigricollis, Cebus albifrons, Cebus apella, Saimiri sciureus, Aotus trivirgatus, Trachypithecus cristata, Chlorocebus aethiops, Macaca fascicularis, Macaca mulatta, Macaca nemestrina, Macaca fuscata, Papio cynocephalus, Papio anubis, Pan troglodytes, Pongo pygmaeus, Gorilla gorilla, and Homo sapiens and are derived primarily from Smith [1989] with supplemental data from recent analyses, especially on great ape molar emergence; see references). Summary statistics for the ordinary least squares regression are as follows: 
, 95% confidence interval (CI; slope): 0.555–0.704, 
(
), and the 95% prediction intervals are indicated by the shaded region. Reduced major axis regression: 
, 95% CI (slope): 0.572–0.721. Ceboids are indicated by x, cercopithecoids are filled circles, great apes are filled squares, and H. sapiens is the open diamond. Australopith species are represented by triangles (from top left, clockwise: SK 48, DIK-1-1, Taung 1, OH 5) and Homo erectus (KNM-WT 15000 and Sangiran S7-37) by open squares.
The total range of variation in modern human M1 emergence age is quite large, spanning almost 2.5 years (reviewed in Liversidge 2003). Despite that, reconstructed emergence ages for some of the early Homo species do not extend into the range for modern humans. Importantly, we do not yet know exactly how, if at all, certain life history attributes covary with dental development within and among modern human peoples or how to integrate these sorts of important intraspecific data with the interspecific trends discussed here.
The earliest species of Homo: the “transitional” hominins H. habilis and H. rudolfensis
Based on detailed reconstructions of dental chronologies, it seems that australopiths fall well within the range of emergence ages known for captive and wild chimps, and none falls within the ranges known for modern humans. Thus, it is reasonable to conclude that early hominins possessed a life history profile more similar to modern African apes than to modern humans. Dental maturation data for the earliest members of Homo, however, are much more limited. To date, dental maturational data for H. habilis and H. rudolfensis consist of either reconstructed root formation times (OH 16, H. habilis) or crown formation times (KNM-ER 1805E, H. habilis; KNM-ER 1590, KNM-ER 1802, KNM-ER 1482B, H. rudolfensis; but see Antón 2012 as to species groups). Taken together, they suggest a dental developmental profile that was more modern apelike than modern humanlike, providing some tantalizing evidence that neither species likely possessed an extended period of childhood dependence (Dean 1995; Dean et al. 2001).
Later species of Homo
Given the extraordinarily complete and well-preserved juvenile specimen KNM-WT 15000, we perhaps know more about overall growth and development, and thus life history, in African H. erectus than any other early hominin taxon. Based on the lack of fusion of the distal elbow joint and the acetabulum in particular, KNM-WT 15000 was given an age of death at ca. 13 years, or the early part of the adolescent stage of growth (i.e., postpubertal; Ruff and Walker 1993). Interestingly, the mostly completed dentition (26 permanent teeth had emerged, all but the M3s and maxillary canines) suggested an age at death of ∼10.2 years. This discord of almost 3 years suggests a somewhat unique developmental trajectory for H. erectus (Smith 2004). Equally interesting is that based on a chimpanzee developmental standard, the state of somatic development suggests an age at death of 7–7.5 years, while the state of dental development suggests an age estimate of 7 years (Smith 1993). Each scenario carries vastly different implications for the life history profile of H. erectus, and dental developmental data hold the potential to resolve the discrepancy.
Data on the pace of development derived from the histology of enamel and dentine originally yielded an age-at-death estimate of closer to 8 than to 12 years of age (Dean et al. 2001). A more extensive analysis, informed by several more years of data on crown and root development in larger samples of humans and fossil hominins and thus based on clearer estimates of certain dental growth parameters, has confirmed this by suggesting that an age-at-death interval of 7.6–8.8 years is most appropriate (Dean and Smith 2009). Furthermore, the reconstructed age at M1 emergence based on inferences from incremental growth data is 4.5 years, just slightly outside the known ranges for extant captive (2.1–4.0 years) and wild (3.8–3.9 years) Pan and slightly earlier than that for modern humans (4.7–7.0 years). Given the relationship between brain size and dental development (see fig. 1), a brain size estimate for KNM-WT 15000 (810 cm3) generates a point prediction for M1 emergence age of 5.2 years (95% prediction interval: 3.2–8.7 years), suggesting that H. erectus likely possessed rapid maturation and was more modern apelike in overall growth and development and “certainly closer to the expectation for an ape of comparable dental and skeletal maturity (ca. 7.5) than for a human (ca. 10–15)” (Dean and Smith 2009:114). Taken together, these data make it unlikely that all or even some of the distinctive features of modern human life history were present ca. 2.0–1.5 Ma.
Slower maturation translates into later ages for achieving certain developmental milestones, such as the onset of puberty, adolescence, and so forth, and is intricately linked to the ability of mothers to wean offspring earlier and shorten interbirth intervals, thereby increasing fertility by having multiple, overlapping offspring. This “stacking” phenomenon is only possible because of the lower energetic requirements for fueling growth in slower maturing organisms compared with the tremendous energetic burden mothers would face having to subsidize the growth of fast-growing, multiple offspring (Dean and Smith 2009; Gurven and Walker 2006). Available data from modern hunter-gatherers suggest that humans follow the ecological risk aversion model (Janson and van Schaik 1993) that posits slow growth and the maintenance of small sizes for longer periods of time, reduces feeding competition, and translates into significant energetic savings. This energetic savings is offset by a period of accelerated growth, known as the adolescent growth spurt, which could be subsidized by older individuals, highlighting the importance of older individuals in contributing to the care and feeding of children (i.e., paternal care, “grandmothering,” etc.; e.g., Hawkes 2003; Hawkes et al. 1998; Kaplan et al. 2000). Thus, the human strategy can be seen as one where higher fertility is achieved by emphasizing more slow-growing children with a later growth spurt than few faster-growing ones (e.g., Bogin 1988, 1997; Gurven and Walker 2006; Leigh 2001; Leigh and Park 1998). The combined lack of evidence for protracted growth and for an adolescent growth spurt (Antón and Leigh 2003; Smith 1993; Smith and Tompkins 1995) in H. erectus and H. ergaster supports the assertion that fully modern human life histories had yet to evolve by 1.5 Ma.
Recently, several investigations have been launched to ascertain whether the modern human pattern of growth, development, and life history characterized Neanderthal (Homo sapiens neanderthalensis) populations (e.g., Bayle et al. 2009a, 2009b, 2010; Coqueugniot and Hublin 2007; Guatelli-Steinberg 2009; Guatelli-Steinberg et al. 2005; Macchiarelli et al. 2006; Ponce de León et al. 2008; Ramirez-Rozzi and Bermúdez de Castro 2004; Smith et al. 2007b, 2007c, 2010b). A convincing argument is mounting that dentally, Neanderthals may have experienced accelerated growth, which would in turn suggest that a growth profile that included prolonged dental development, and one that may have included most or all of the other human life history attributes, did not evolve until the appearance of H. sapiens. Unfortunately, very little is known about dental development in taxa postdating H. erectus and predating Neanderthals, but it would seem parsimonious to reconstruct dental development as being at least as accelerated in middle Pleistocene taxa such as Homo antecessor and Homo heidelbergensis. Limited data are not inconsistent with this hypothesis: certain growth parameters of anterior teeth in these species seem more similar to Neanderthals than to modern humans (Ramirez-Rozzi and Bermúdez de Castro 2004).
Reconstructing life history in early Homo
Given the available data, the full suite of modern human life history characteristics was most certainly not present at the base of the hominin lineage, nor was it present at the emergence of the genus Homo, but it likely occurred at some time during the middle to late Pleistocene. That does not mean, however, that all hominins before the appearance of H. sapiens possessed a life history that was completely modern apelike despite the fact that all of the included species of early Homo seem quite accelerated dentally. There are several possible interpretations of the relatively early M1 emergence ages of the hominins (reviewed in detail in Kelley and Schwartz 2012). Aside from scenarios regarding the manner in which these age estimates were generated or how incremental growth is charted, there are several ways to interpret these data.
Perhaps the ages at M1 emergence indicate the presence of relatively rapid life histories in australopiths and early Homo and thus are more similar to Gorilla than to Pan. This could be related to dietary differences: lower-quality food such as that preferred by primary folivores such as Gorilla gorilla beringei display more accelerated life history schedules and relatively precocious dental development than similar-size frugivores (Breuer et al. 2009; McFarlin et al. 2009).
While diet type and nutritional quality are still debated for many hominin taxa, it is clear that members of early Homo were committed terrestrial bipeds. Across primates, highly terrestrial species possess more accelerated life history schedules than nonterrestrial species (Deaner, Barton, and van Schaik 2003; Ross 1992, 1998), likely as a result of increased extrinsic mortality in the form of predation. Early hominins clearly succumbed to predation with some regularity, and the signal of relatively rapid life history profiles in australopiths and early Homo may be a direct outcome of selection operating on low survivorship by accelerating overall development to reach sexual maturity at an earlier age. In that context, dental development may be linked, perhaps through a mechanism such as pleiotropy, to overall somatic development and is therefore similarly accelerated.
Scenarios to explain early Homo life history need not rely on inferences based on diet or inferred mortality profiles alone. The combination of low nutritive value of ingested food with high rates of extrinsic mortality would have the result of selecting for individuals within populations that would grow at a slow rate and mature early, producing adults of small stature such as those found within contemporary hunter-gatherers of the rainforests (Kuzawa and Bragg 2012). High mortality on its own would also select for faster growth and early maturation, though at “normal” adult sizes. In this context, it is interesting to speculate that populations experiencing increases in nutritional quality along with high extrinsic mortality should grow faster to reach maturation earlier at larger adult sizes compared with ancestral populations with low nutritional quality and high mortality. As shown by McHenry (1992, 1994), Holliday (2012), and Pontzer (2012), there is good evidence for a general trend of an increase in body mass from Australopithecus to Homo (also see Ruff 2002 and references therein). If rates of extrinsic mortality were held constant, this could imply a transition from hominin populations with low nutritional quality to those with higher nutritional quality. This is not inconsistent with recent dietary reconstructions of early Homo, wherein H. erectus diets were reconstructed as far more varied than in preceding H. habilis (Ungar 2012; Ungar et al. 2011), perhaps suggesting that a broadening of the resource base was an important contributing factor to the evolution of larger body sizes and perhaps ultimately to shifts in life history. Interestingly, researchers have speculated on whether similar conditions may have led to selection for accelerated growth in Neanderthals and include scenarios where they experienced serious nutritional stress linked with elevated rates of young adult mortality (Oglivie, Curran, and Trinkaus 1989; Pettitt 2000; Trinkaus 1995; Trinkaus and Tompkins 1990). According to life history theory, both of these factors in combination would have the effect of selecting for rapid and early maturation.
A second possible interpretation is that reconstructions of the pace of life history are indeed more accurately reflected by brain size, and so the scheduling of at least some life history attributes occurred at a slower pace than would be inferred from simply evaluating M1 emergence ages alone. In other words, different life history parameters could be dissociated from one another so that selection could act on them individually or as smaller developmental subsets. It is critical to bear in mind that dissociations among developmental systems—the scheduling of dental events versus that of reproductive events, for instance—may not be as tightly linked across closely related species as they appear to be across hominoid genera. In fact, the clear associations between dental development and life history variables as well as among life history variables that exist when examined across primates as a whole are known to break down when examined across closely related species. The general trend for primates holds that larger species take longer to grow and reach sexual maturity; however, data on hylobatids suggest that it is the smaller-bodied Hylobates, not the larger Syndactylus that possesses a later age at sexual maturity and a longer life span (Dirks and Bowman 2007). That same study also demonstrated that the age at molar emergence is not correlated with age at menarche or the age at first reproduction in exactly the same way in both cercopithecoids and hylobatids. On an even broader scale, certain strepsirrhines “buck” the primate trend as a means of solving the problem of how to cope with highly seasonal and unpredictable environments. Compared with lemurids, large-bodied indriids exhibit extreme dental precocity while maintaining slower rates of somatic growth, thus allowing for relatively earlier weaning as a strategy to help reduce the metabolic burden on mothers (e.g., Godfrey et al. 2001). These are just a few examples of how an understanding of developmental dissociations, or “modularity” (sensu Leigh and Blomquist 2007), urges some caution in directly linking dental development and the scheduling of life history. An exciting avenue of future study would be to document the extent to which dental developmental profiles are correlated with life history attributes within populations of modern humans, an endeavor made easier these days by the ever-expanding data on the chronology of developing teeth in worldwide populations (see Liversidge 2003). This may ultimately yield clearer and more refined insights into the finer details of life history evolution across hominin species and especially within more closely related and even conspecific hominin populations. At the same time, these analyses may unveil the extent to which the human life history package is dissociable and allow us to begin to develop models of how shifting patterns of ecology, subsistence, demography, diet, and so forth, throughout the Homo lineage may have resulted in a more piecemeal acquisition of the fully modern human life history profile. Some new data suggest that this may be an interesting way forward. Very recently, DeSilva (2011) posited that infant∶mother mass ratios of ∼5% (generally ∼6% in modern humans; cf. 3% in extant chimpanzees) were already present in early australopiths. That author suggests that more modern humanlike birthing strategies, the adoption of alloparenting behavior, and so forth, may have been present >3 Ma, well before the origin of Homo. On the other hand, other aspects of the human life history package such as life span, for example, may be a more recent acquisition. New data on adult mortality patterns suggest similar population demographics for late archaic (Neanderthals) and early modern (Middle and earlier Upper Paleolithic) humans, an observation that weakens support for some sort of demographic advantage related to enhanced longevity for early modern humans (Trinkaus 2011).
Future Directions
Discoveries of new infant and subadult fossils along with advances in noninvasive imaging and analytical methods are providing opportunities to probe further the fossil record of human growth and development. For instance, it is likely that the age at which important life history events, such as weaning, will be assessable directly from the fossil record. The timing of weaning is a key life event for both mother and offspring, and analyses of life history variation as it relates to weaning across Primates provide one example of the selective basis of these sorts of developmental dissociations. Within Malagasy prosimians, selection has acted to accelerate weaning and dental development but has delayed the age at first reproduction (Godfrey et al. 2001; Richard et al. 2002; Schwartz et al. 2002). It has been suggested that some australopiths show rapid deciduous tooth wear, which was taken as evidence suggestive of relatively early weaning (Aiello, Montgomery, and Dean 1991; Dean 2006, 2010). It may now be possible to retrieve direct evidence for reconstructing weaning age and shifts in energy provisioning for offspring through the evolution of Homo. Across Primates, weaning is closely tied in time to the emergence of M1. However, human life history is characterized by relatively early weaning followed by a prolonged period of postweaning dependency. The advancement of weaning age throughout human evolution coupled with rapid and early brain growth implies a shift in how the rising energetic demands of offspring are met: initially, energetic costs are subsidized completely by the mother but then by members of the social group through the provisioning of weanlings (Humphrey 2010). This pattern of high maternal investment and alloparenting behavior is important because it is a clear determinant of birth spacing. Such a stratagem has also been suggested to characterize the earliest members of Homo (Aiello and Wells 2002). Recently, models have been proposed to establish the precise age at which organisms were weaned by accessing the isotopic record, in particular, strontium∶calcium ratios (Sr/Ca) preserved within dental hard tissues (e.g., Humphrey et al. 2008a, 2008b). Charting shifts in this ratio throughout the developmental period associated with early tooth tissue formation is one exciting way of reconstructing infant diet as well as tracking dietary transitions throughout early life. If early Homo and later-occurring archaic Homo populations were indeed characterized by relatively early weaning, then analyses of the isotopic chemistry throughout enamel development hold the potential to verify this with direct evidence for the age at weaning from the fossil record itself.
While continued probing of the fossil record to establish more precise demographic and maturational profiles holds the potential to yield key details in the evolution of human life history, another interesting way forward is to attempt to understand the processes that lie behind the slightly dissimilar patterns in dental development, and thus inferred life history profiles, among hominins. A host of studies have advanced our understanding of how dental developmental variation intersects with primate life history variation, but surprisingly little is known about the precise mechanism that governs, modulates, regulates, constrains, and so forth, the timing of molar eruption and as such the underlying processes that regulate these temporal events are largely unknown.
Recently, it was postulated that a set of biomechanical constraints regulates masticatory system configuration throughout ontogeny and therefore modulates the position and ultimately the timing of emerging molars within developing faces (Spencer and Schwartz 2008). Based on an ontogenetic sample of modern human crania, it seems that successive molar emergence events are predominantly a function of rates of facial growth such that successive molars (deciduous and permanent) emerge at a consistent position relative to the masticatory musculature (fig. 2). Moreover, there appears to be a consistent position of newly erupted molars (deciduous and permanent) relative to the temporomandibular joint (TMJ) that in an archaeological sample of modern humans is ∼40 mm (fig. 3). This ontogenetic arrangement ensures that there is a biomechanically optimal location for molar eruption anterior to the net vector of masticatory muscle effort (note position of white dots relative to dotted white line, fig. 2) and that each successive molar erupts into this optimal position only at a point during ontogeny when it is vacated as a result of facial growth. This all suggests covariation in rates of facial growth (indicated by the slope of the first part of the curve for each molar, fig. 2), the position of the masticatory musculature, the spatial position of an erupting molar, and the timing of molar emergence.
Bivariate plot of bite point positions for all teeth and masticatory muscle positions relative to the temporomandibular joint (TMJ; y-axis) versus age (x-axis) in a cross-sectional ontogenetic series of modern humans (Nubian archaeological sample housed at University of Colorado, Boulder). Bite points are measured as the distance of each tooth from the TMJ, measured in the occlusal plane, and are illustrated by the two vertical arrows (left) indicating bite points for the dm1 and dm2. Masticatory muscle position (for the superficial and deep masseters, temporalis, and medial pterygoid muscles) is defined as the point where each muscle’s resultant force crosses the occlusal plane relative to the position of the TMJ. Primary masticatory adductor position and orientation are based on a series of 2-D and 3-D linear and angular measurements and, taken together, capture what has been termed “masticatory system configuration” (see Spencer 1995, 1999). Note the consistent position of the dm2 (small white sphere) and the permanent M1, M2, and M3 (large white spheres) anterior to the masticatory muscles (i.e., above the white dotted line) at the time of emergence. Also note the differing rates of anterior growth of the dental arcade and masticatory muscles (as indicated by the slopes of second-order polynomials); space for emerging molars is a product of these different growth rates.
Consistent position of newly erupted molars relative to the temporomandibular joint (TMJ) as indicated by the length of the horizontal white line. The dot on the left of the line marks the position of the TMJ in lateral view, while the dot on the right marks the position of the newly emerged molar. Note that the line is the same length for individual human crania at the time of M1 emergence (top), M2 emergence (middle), and M3 emergence (bottom). This is illustrated graphically by the consistent width of the shaded rectangle. While the absolute distance is different, the same pattern of spatial consistency in molar position holds for an ontogenetic sample of wild-living Pan (see text).
The validity of this biomechanical model for modulating the timing of molar emergence has not been fully established. Indeed, whether this constraint operates across hominoids is not yet clear, but preliminary data on an ontogenetic series of western African chimpanzees (Pan troglodytes verus; 
) are striking: like the modern human sample, no significant differences are present between the position of each successively emerging molar and the TMJ (Kruskal-Wallis, 
, 
) despite the fact that, unsurprisingly, the absolute distance is slightly greater in this sample (∼48 mm).
A fuller mapping of the influence of these biomechanical constraints onto variation in the ontogeny of masticatory muscle position and explicitly testing hypotheses that integrate craniofacial architecture, muscle function, facial growth, and molar emergence across hominoids is currently underway. These are critical comparative data because selection for accelerated molar eruption, as seems to characterize early Homo relative to modern humans, should require a similar acceleration in facial growth. The delay in molar emergence ages in modern humans may therefore result from reduced rates of facial growth and extreme orthognathy, perhaps in combination with a developmental delay in facial growth. A later initiation of facial growth would result in a delay in clearance of a “biomechanically appropriate” space available for molar emergence.
In the absence of good ontogenetic data on craniofacial growth in early Homo, it is useful to evaluate how well this biomechanical model integrates craniofacial morphology with data on developmental rates within other members of the Homo lineage. This model predicts the advanced molar emergence schedules of Neanderthals to be related to a combination of their higher degree of midfacial prognathism and accelerated cranial growth trajectories. Some evidence in support of faster rates of craniofacial growth (Ponce de León and Zollikofer 2001; Ponce de León et al. 2008) and dental development (Smith et al. 2007c, 2010b) exist. Thus, selection may have accelerated age at weaning and thus ecological independence by advancing rates of cranial growth in a manner that permitted a more accelerated molar development/eruption schedule, which would represent an effective life history strategy under conditions of high extrinsic mortality. More thorough explorations of how the timing of molar development and emergence may result from the complex spatial interplay between growing faces and expanding neurocrania hold tremendous potential for illuminating the underlying mechanism that regulates molar emergence and, ultimately, for unlocking the linkages between dental development and life history events.
Finally, it is generally agreed that the earliest species of Homo evolved from Australopithecus, either in East or South Africa. The cranium from Bouri, Ethiopia, at 2.5 Ma attributed to Australopithecus garhi (Asfaw et al. 1999) and the associated cranial and postcranial material for the newly announced Australopithecus sediba from Malapa, South Africa, at 1.9 Ma (Berger et al. 2010) may therefore provide important clues for helping to better understand the complex interplay among morphological, ecological, reproductive, and behavioral adaptations that underlies the transition to and ultimate success of the genus Homo.
I would like to thank Leslie Aiello and Susan Antón for their invitation to participate in the Wenner-Gren workshop, all of the conference participants for their stimulating and thoughtful discussions throughout the conference, and the two anonymous reviewers for their input and constructive comments on this manuscript. The ideas and work laid out here are the results of many discussions and ongoing collaborations, especially with Chris Dean, Jay Kelley, Tanya Smith, Debbie Guatelli-Steinberg, Laurie Godfrey, Wendy Dirks, Bill Kimbel, Mark Spencer, Terry Ritzman, Kierstin Catlett, and Halszka Glowacka. I am grateful to the Institute of Human Origins at Arizona State University for their generous support.
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Notes
Gary T. Schwartz is Associate Professor of Anthropology at the Institute of Human Origins at Arizona State University (900 South Cady Mall, Tempe, Arizona 85287-2402, U.S.A. [[email protected]]).
