Middle Childhood and Modern Human Origins

Jennifer L. Thompson & Andrew J. Nelson

Published online: 12 August 2011# Springer Science+Business Media, LLC 2011

Abstract The evolution of modern human life history has involved substantialchanges in the overall length of the subadult period, the introduction of a novel earlychildhood stage, and many changes in the initiation, termination, and character of theother stages. The fossil record is explored for evidence of this evolutionary process,with a special emphasis on middle childhood, which many argue is equivalent to thejuvenile stage of African apes. Although the juvenile and middle childhoodstages appear to be the same from a broad comparative perspective, in that theybegin with the eruption of the first molar and the achievement of the majority ofadult brain size and end with sexual maturity, the detailed differences in theexpression of these two stages, and how they relate to the preceding and followingstages, suggest that a distinction should be maintained between them to avoidblurring subtle, but important, differences.

Keywords Middle childhood . Growth and development . Adolescent growth spurt .

Life history

The modern human pattern of growth and development evolved over the course ofseveral million years and is distinct in several respects from that of living apes(Bogin 1988, 1997, 2006; Bogin and Smith 1996; Robson et al. 2006; Schultz 1960;Watts 1986). In general, nonhuman primates are considered to have four major life-history stages: infancy, the juvenile period, a short adolescent period, and the adultstage (see discussion below). However, modern humans have inserted anadditional stage: early childhood, which falls before the juvenile period, and they

Hum Nat (2011) 22:249280DOI 10.1007/s12110-011-9119-3

J. L. Thompson (*)Department of Anthropology, University of Nevada, Las Vegas, 4505 Maryland Parkway, Las Vegas,NV 89154-5003, USAe-mail: jennifer.thompson@unlv.edu

A. J. NelsonDepartment of Anthropology, The University of Western Ontario, London, ON N6A 5C2, Canada

have greatly elongated their adolescent stage (Bogin 1999, 2006) (Fig. 1). Thismeans that sexual and physical maturation is substantially delayed to the last stage ofthe growth periodadolescenceand the whole growth period is extended, takingalmost twice as long as that seen in extant apes (Bogin 1999; Schultz 1960).

The focus of this special issue is on the middle childhood stage of growth anddevelopment (a term used by developmental psychologists, who recognize early,middle, and late childhood). In broad comparative ethological terms, the middlechildhood stage starts after brain growth is complete and during which individualsare not completely dependent on their parents but have not yet reached puberty(Bogin and Smith 1996; Leigh 2004; Pereira and Altmann 1985). In thecomparative, primatological literature this stage is generally called the juvenilestage (as used in the previous paragraph) (e.g., Bogin 2003). Higher primates,particularly apes, are differentiated from other mammals by having a prolongedjuvenile period, which is thought to have evolved by means of natural selection,allowing more time for social learning and cognitive development (Bogin 2006;Kaplan and Robson 2002; Kaplan et al. 2000; Pagel and Harvey 1993; Pereira andAltmann 1985). Thus, apes and modern humans share the trait of a long juvenileperiod, but the addition of the early childhood stage and the elongation of theadolescent stage of the program of human growth and development have changedhow the middle childhood period relates to the infancy and adult periods. The goalof this paper is to explore the evolution of the modern human pattern of growth anddevelopment, with a focus on the period of middle childhood in Homo erectus andmore recent hominins. A secondary goal of this paper is to review how closely theoverall pattern of Neandertal growth and development, including the early childhoodand adolescent stages, matches that of modern humans to assess when the modernpattern of growth and development evolved.

Fig. 1 Length of life history stages in apes and modern humans. Note that apes lack an early childhoodstage. (modified from Bogin 2003)

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Definitions of the Stages of Growth and Development

As outlined above, the pattern of growth and development in modern humans differsfrom that of higher primates principally by possessing an early childhood stage andan elongated adolescent stage, resulting in a longer period of preadult growth,combined with high rates of postnatal brain growth (Bogin 1999). Before we canexplore the evolution of these stages in detail, we must clearly define what the stagesare. As Dean and Smith (2009:102) note, mammalian life stages can be defined in anumber of different ways. We choose to follow Bogin (2006:205) in dividing humanlife history into five stages because they are biologically definable and meaningfuland because each stage encompasses a set of biological and behavioral traits thatdefine them. Such an approach does not ignore life history events like age atmaturation, birth rates, interbirth intervals, and age at death (Leigh and Blomquist2007). Furthermore, Bogins stages can be cross-referenced to skeletal/dentallandmarks, thereby providing a starting point for organizing and analyzing theimmature fossil record that consists of bones and teeth. Finally, it also allows us toexamine the nature of the juvenile stage (or middle childhood) by assessing thosestages that precede and follow it and to explore evolutionary explanations for anydifferences (e.g., embodied capital model, grandmother hypothesis; Hawkes andPaine 2006). That being said, it is still extremely challenging to develop precisedescriptions of the different stages of growth and development in modern humansbecause different scholars use different landmarks, leading to differing opinions onwhen the different stages start and stop. The task of developing precise definitions ofeach stage of growth is made even more complicated when one attempts to mapthese stages onto our closest primate relatives, the African apes, in order to developmodels of how the patterns of growth and development may have evolved from thecommon ancestor we share with the chimpanzee and gorilla. However, suchdefinitions are a critical starting point prior to assessing the fossil record. Theobjective of this section is to develop a consensus stage model to form the basis forthe consideration of the evolutionary changes that occurred over the past severalmillion years.

Infancy in all mammals is described as the postnatal period during which the offspringis wholly dependent on the parents, usually the lactating mother, for food and protection(Bogin 1999). In modern humans, a neonatal period lasting for the first 28 days of lifeis sometimes identified, and rapid prenatal brain growth rates are maintained for thefirst year of life (Dienske 1986; Rosenberg 1992; Smith and Tompkins 1995). Theextension of fetal brain growth rates allows modern human females to give birth toinfants with relatively small brains (compared with the adult outcome) as an adaptationto locomotor and gestation length constraints, and the high postnatal growth ratesenable us to develop our large brain (Leigh 2004; but see Robson et al. 2006).

The key trait marking the end of the infancy period for both apes and humans isweaning. In apes weaning takes place at about 4 years of age (Robson and Wood2008) and in humans (worldwide average) at about 3 years of age (Bogin 2003;Robson and Wood 2008). In apes, weaning coincides with the achievement of 90%of brain growth and with the eruption of the first permanent molar, although theseevents are further delayed in modern humans (Bogin 2003; Robson and Wood 2008).

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Early Childhood Following infancy, modern humans experience the childhood stage(called early childhood here to differentiate it from middle childhood) not seen inapes. During early childhood, high rates of brain growth are maintained but onlymoderate somatic growth occurs (Bogin 2003, 2006). During this stage, the humanchild is dependent on its parents for extensive food supplementation not only tosupport the high rate of brain growth but because the digestive system and dentitionare not yet mature enough to process adult foods (Bogin 1999, 2006; Leonard andRobertson 1994, 1997; Sellen 2006).

Middle Childhood The end of the early childhood phase, and hence the beginning ofthe juvenile, or middle childhood, stage, is the subject of some debate. One markeroften used is the cessation of brain growth (in weight), which, Bogin (2003) hasargued, occurs by about 7 years of age. However, while this age certainly marks theattainment of the majority of brain growth, growth actually continues slowly into theteenage years (Robson and Wood 2008). Hence, some scholars argue that a bettermarker is the achievement of 90% of adult brain growth, which occurs by about5 years of age (Robson and Wood 2008). Another marker is the eruption of the firstpermanent molar (which coincides with the end of infancy and the beginning of thejuvenile stage in apes), which occurs between 4.7 and 7 years of age in humans(Robson and Wood 2008). Finally, much of the anthropological/psychologicalliterature cites the ages of 5 or 6 as the beginning of the middle childhood stage (e.g.,White 1996). Thus, a range of estimates for the beginning of middle childhoodwould be from 5 to 7 years of age. Given the lack of consistency in these markers,using a compromise estimate of about 6 years to mark the beginning of the middlechildhood/juvenile stage is a useful starting point for assessing fossil material.

The juvenile, or middle childhood, stage starts directly after weaning in apes, andafter the early childhood stage in modern humans. By the beginning of the middlechildhood stage, in both apes and modern humans, brain growth is mostly complete,the first molars have erupted, and individuals are not completely dependent on theirparents but they have not yet reached puberty (Bogin and Smith 1996; Leigh 2004;Pereira and Altmann 1985). Higher primates, particularly apes and modern humans,are differentiated from other mammals by having a prolonged juvenile period, whichis thought to have evolved by means of natural selection, allowing more time forsocial learning and cognitive development (Bogin 2006; Campbell 2006; Kaplan andRobson 2002; Kaplan et al. 2000, 2003; Pagel and Harvey 1993; Pereira andAltmann 1985; but see Blurton Jones 2006). In modern humans the middlechildhood stage can be described as the entry into the age of reasoning (White1996:17), during which important cognitive developments occur and new behaviorsemerge (Hochberg 2008; White 1996).

The end of the juvenile period is generally considered to be the onset ofsexual maturation, which is most obviously marked by the onset of menarche infemales (e.g., Bogin 2003; Pereira and Altmann 1985). Sexual maturation occursat around 11 or 12 years of age in modern humans (Bogin 2003) and between theages of 7 and 11 for the different species of African apes (Leigh 1996; Strier 2007).Thus, the middle childhood/juvenile period lasts between 5 and 6 years in modernhumans, and between 3 and 7 years for the African apes, with a midpoint of about5 years.

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Adolescence One of several definitions of the adolescent stage that is commonlyused is the period of life beginning with sexual maturity and ending with thecessation of somatic growth and the attainment of adult size (e.g., Watts 1985).Bogins (1999, 2003) definition explicitly includes a growth spurt. AlthoughAfrican apes do demonstrate a growth spurt in body mass (e.g., Leigh 1996),Bogin appears to feel that this body mass spurt is insufficient to identify theadolescent stage in our primate relatives (see Bogin 2003: Figure 2.7). However,there is definitely a delay between menarche and the cessation of somatic growthin African apes, leading other researchers to argue that the adolescent stage shouldbe recognized (e.g., Leigh 1996; Pereira and Altmann 1985; Watts 1985). In thispaper we will follow the consensus opinion that the adolescent stage should berecognized in African apes, although we agree that adolescence in modern humansis distinct because it is delayed and of longer duration than in the great apes (Bogin1988; Smith 1993; Tanner 1990; Watts 1985) and involves a consequent delay inreproductive maturity. The adolescent stage is also notable in modern humansbecause they also undergo a very pronounced and delayed growth spurt (Leigh1996:455). The adolescent growth spurt is apparently unique to humans in that itinvolves a rapid increase in the rate of growth soon after the eruption of the secondmolar, resulting in an increase in linear dimensions of most of the skeleton,including the face (Bogin 2003). Although both human and nonhuman primatesdemonstrate some sort of acceleration in growth velocity during adolescence(Laird 1967; Leigh 1996), this long absolute delay in the initiation of the humangrowth spurt (Leigh 1996:455) as well as the magnitude and late timing of thehuman growth spurt (and thus the nature of adolescence) appear to be unique tomodern humans (Bogin 2003). Somatic growth in African apes terminates atbetween 10 and 12 years of age, making their adolescence approximately 2 yearslong. In modern humans, adolescence begins about 1012 years of age and ends atabout age 1820, lasting about 8 years (Robson and Wood 2008; see alsoRosenfeld and Nicodemus 2003).

Adulthood is the period between the cessation of growth and attainment ofreproductive maturity and the death of the individual. African apes are known tohave a maximum lifespan of between 50 and 54 years, whereas the maximum life span ofnonindustrialized groups of modern humans is about 85 years (Robson andWood 2008).

This paper will review the available fossil evidence to assess when ourmodern pattern of growth evolved. It will focus on the genus Homo (erectus,neanderthalensis, sapiens). Studies of Plio-Pleistocene hominins (the australopi-thecines and habilines) have demonstrated that early hominins followed an apelikerate and pattern of growth and development, with the implication being that laterhominins became more similar to modern humans over the course of evolution(Anemone et al. 1996; Beynon and Dean 1988, 1991; Bromage and Dean 1985;Dean 1989; Dean et al. 2001; Moggi-Cecchi 2001; Smith 1986, 1989, 1991, 1992).Thus, H. habilis and rudolfensis will be excluded since their dental developmentand body proportions are more australopithecine- than humanlike (Ruff 2009;Skinner and Wood 2006; Wood and Collard 1999). In fact, Wood and Collard(1999) have argued that the habilines should be completely excluded from thegenus Homo.

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Recognizing Life History Stages in the Fossil Record

Although scholars who study stages of growth and development in modern humansand other living organisms can readily observe physical and behavioral traits andeasily assess the age of their study subjects, evolutionary biologists must identifyanatomical correlates that can be used to identify the stages and rely on dental/skeletal criteria in order to determine the developmental age of a fossil.

Infancy The age of weaning is particularly difficult to establish in the fossil record.However, the increasing use of isotopic analysis, particularly of N values, holds somepromise in this regard (e.g., Bocherens et al. 2001). Allometry can be used to makepredictions for weaning age on the basis of its association with body size (Harvey andClutton-Brock 1985), and patterns of lesions generally associated with systemic stressthat accompanies weaning (such as linear enamel hypoplastic lesions) can beexamined on the skeleton (Dean and Smith 2009; Katzenberg et al. 1996).

Early Childhood The pause in somatic growth experienced in early childhood may beindicated by alterations in the pattern of dental development (Mann et al. 1996), whilean increase in the final size of the adult brain is likely to be the product of high rates ofbrain growth that occur during this period (Bogin 2003) and the absolute extension ofthe time for brain growth (ca. 4 years in apes and ca. 6 years in modern humans). If itis possible to determine the age of weaning, the continuation of brain growth after theage of weaning would also be evidence for the early childhood stage.

Middle Childhood is somewhat difficult to accurately identify in the fossil record.Apart from the eruption of M1, which marks the beginning of the middle childhood/juvenile stage, perhaps the best method is by exclusion: individuals in this stage willnot demonstrate evidence of the brain growth that is characteristic of infancy andearly childhood, nor will they show evidence of the adolescent growth spurt. It ispossible that they will demonstrate evidence of stress and/or pathological/traumaticlesions that are associated with the initial adoption of adultlike behaviors.

Adolescence The key feature of adolescence, the growth spurt, is recognized on theskeleton in a variety of ways. One is the plotting of long bone growth on dental agefor samples of individuals (Nelson and Thompson 2005). Another is the relationshipbetween bone size and epiphyseal fusion (Smith 1993) and the proportionalrelationships among different skeletal elements (Anton and Leigh 2003).

Adulthood The cessation of growth and shift into the adult stage is recognizedskeletally by the movement of the third molars into occlusion and the closure of theepiphyses of the major long bones (Buikstra and Ubelaker 1994).

An important aspect of the analysis of any hominin fossil is the determination ofits age at death. However, age determination is not necessarily a straightforwardexercise. Standards exist for dental eruption and skeletal maturation in modernhumans and in African apes, but we must be very careful in the simple application ofthese standards to fossil forms. Furthermore, ever more sophisticated agingtechniques are being developed, forcing us to reconsider earlier hypotheses.

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Adaptive factors that changed during the course of human evolution and that wouldhave had profound effects on patterns of growth and development include (1) body size(see Ruff et al. 1997), (2) brain size (Ruff et al. 1997), (3) evolutionary cost/benefittrade-offs associated with delaying or extending the growth period (Bock and Sellen2002; Brumbach et al. 2009; Hawkes and Paine 2006; Leigh 2001), (4) dietaryrequirements (Gurven and Walker 2006), (5) increased emphasis on time available forlearning complex tasks (Bogin 2003; Kaplan et al. 2003), and (6) mortality rates(Migliano et al. 2007; Stearns and Koella 1986; Walker et al. 2006).

The Fossil Record

Homo erectus

The origin of H. erectus heralded the appearance of an adult morphology which wasmuch more reminiscent of modern humans than any previous hominin. H. erectuswas very close to, and possibly larger than, modern humans in terms of body size(Kappelman 1996; Ruff et al. 1997) and stature (McHenry 1991). The upper end ofthe range of cranial capacity recorded for this taxon (691 to 1,231 ml; Aiello andDean 1990; Spoor et al. 2007) reaches into the lower end of the range of variationfor modern humans (Aiello and Dean 1990:193). Overall limb proportions appear tolie within the modern human range of variation (McHenry 1978; Ruff 2003, 2008;Walker and Leakey 1993).

It is difficult to ascertain much about the infancy of H. erectus. Analysis of the1.8-million-year-old Mojokerto child (see Table 1 for a listing of the subadult fossilsdiscussed in the text), who died at about 1 year of age, reveals that its cranialcapacity was 7284% of that of an average adult H. erectus (Coqueugniot et al.2004; but see Leigh 2006 for further discussion). This evidence suggests a pattern ofrelative brain growth resembling that of living apes rather than modern humans(Coqueugniot et al. 2004). A recent discovery of a 1.2-million-year-old adult femalepelvis from Gona, Ethiopia, indicates that H. erectus females hips were wider thanthose of modern human females, suggesting that H. erectus infants were born withheads about 30% larger than previously calculated (Walker and Ruff 1993). Simpsonet al. (2008:1090) concluded that such infants would have experienced a rate ofpostnatal brain growth that was intermediate between modern humans andchimpanzees. However, since the Gona pelvis may belong to Paranthropus boisei(Ruff 2010), these results must be interpreted with caution. Also, several authors(Leigh 2004; Robson et al. 2006) challenge the idea that human brain growth ininfancy is distinct from that of apes.

Enamel defects on the canine teeth of the Nariokotome boy occurred when he wasas young as 3.3 or as old as 4.2 years of age (depending on aging method) and maycoincide with weaning (Dean and Smith 2009). If so, this may mean a longer infancyin H. erectus, falling between that seen in chimpanzees (4.5 years) and humans(2.8 years) (Robson et al. 2006; see also Skinner 1997).

Bogin (2006) argues that childhood evolved by about two million years ago insome early member of the genus Homo. We would argue that this is unlikely, given

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Table1

Importantsubadultfossilspecimenscitedin

thisstudy

Specimen

Taxonomicidentification

Place

ofdiscovery

Geologicalage

Chronologicalageof

individual

Key

references

Modjokerto

H.erectus

Java

1.8mya

ca.1yr

Coqueugniot

etal.2004

Nariokotome

(KNM-W

T15000)

Herectus

Kenya

1.5mya

rangefrom

7.6to

15yrs

WalkerandRuff1993;Tardieu1998;

DeanandSmith

2009

GranDolina1,2,3

H.an

tecessor

Spain

800kya

1=adolescent

Bermdez

deCastroetal.1999

2=earlychildhood

3=adolescent

Simade

losHuesos18

H.heidelbergensis

Spain

300kya

912

yrs

Bermdez

deCastroandRosas

2001

andBermdez

deCastroetal.2003

Scladina

H.nean

dertha

lensis

Belgium

160kya

8yrs

Smith

etal.2007

LeMoustier1

H.nean

dertha

lensis

France

45kya

rangefrom

7to

15.5

yrs

Thompson

andNelson2005a;

Ullrich2005a

LaChaise

H.nean

dertha

lensis

France

160125kya

8.7yrs

Macchiarelli

etal.2006

Roc

deMarsal1

H.nean

dertha

lensis

France

7564kya

2.53yrs

Bayleetal.2009a

Lakonis

H.nean

dertha

lensis

Greece