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REVIEW Evo–devo of child growth II: human life history and transition between its phases Ze’ev Hochberg Meyer Children’s Hospital, Rambam Medical Center, and Technion-Israel Institute of Technology, PO Box9602, Haifa 31096, Israel (Correspondence should be addressed to Z Hochberg; Email: [email protected]) Abstract This review attempts to use evolutionary life-history theory in understanding child growth in a broad evolutionary perspective. It uses the data and theory of evolutionary predictive adaptive strategies for transition from one life-history phase to the next, and the inherent adaptive plasticity in the timing of such transitions. Humans evolved to withstand energy crises by decreasing their body size, and evolutionary short-term adaptations to energy crises utilize a plasticity that modifies the timing of transition from infancy into childhood, culminating in short stature at the time of an energy crisis. Transition to juvenility is part of a strategy of conversion from a period of total dependence on the familyand tribe for provision and security to self-supply, and a degree of adaptive plasticity is provided and determines body composition. Transition to adolescence entails plasticity in adapting to energy resources, other environmental cues, and the social needs of the maturing adolescent to determine lifespan and the period of fecundity and fertility. Conclusion: Life-history transitions are the times when the child adaptively responds to environmental cues in order to enhance growth–body composition–lifespan–fecundity schedules and behavioral strategies that yield the highest fitness in a given environment. European Journal of Endocrinology 160 135–141 Introduction Life-history evolutionary theory is considered here as part of evolutionary development biology (evo–devo) (1) as it addresses factors that produce variation in life histories, which are found both among and within species. Here, it is taken into the realm of clinical medicine and child growth, following the first article in this ‘evo–devo’ series (2). In the case of humans, life-history evolutionary theory is best understood in the context of biological rationale and cultural expressions as a solution to an ecological problem posed by the environment and subject to constraints intrinsic to the organism (3). Among the questions posed are: why are organisms small or large? Why do they mature early or late? Why do they have few or many offspring? Why do they have a short or a long lifespan? Why must they grow old and die? Several reviews on this topic include (2, 4–7). The transition from one life-history phase to the next requires a mechanism for the onset of the latter. Thus, the transition from infancy to childhood is associated with the setting in of the dominance of the GH–insulin-like growth factor 1 (IGF1) axis. The transition into juvenility requires the development of androgen-generating adrenal reticularis. The beginning of adolescent-related puberty is a function of the hypothalamic–pituitary–gonadal (HPG) axis maturation. This review presents the data and theory of evolutionary predictive adaptive strategies for transition from one life-history phase to the next and the inherent adaptive plasticity in the timing of such transitions in order to match not only energy supply, but also other environmental cues. Child growth and the theory of life history Life history has been defined as the strategic allocation of an organism’s energy toward growth, maintenance, reproduction, raising offspring to independence, and avoiding death (3, 7). For a mammal, it is, among others, the strategy of when to be born, when to be weaned, when to stop growing, when to reproduce, and when to die in the best way as to increase its fitness (8). Life-history phases During the evolution of the hominin, childhood and adolescence have been added as new life-history phases (Fig. 1, Table 1) (3). Thus, Homo sapiens have four prolonged and pronounced postnatal pre-adult life- history phases: infancy, which lasts for 30–36 months European Journal of Endocrinology (2009) 160 135–141 ISSN 0804-4643 q 2009 European Society of Endocrinology DOI: 10.1530/EJE-08-0445 Online version via www.eje-online.org

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European Journal of Endocrinology (2009) 160 135–141 ISSN 0804-4643

REVIEW

Evo–devo of child growth II: human life history and transitionbetween its phasesZe’ev HochbergMeyer Children’s Hospital, Rambam Medical Center, and Technion-Israel Institute of Technology, PO Box 9602, Haifa 31096, Israel

(Correspondence should be addressed to Z Hochberg; Email: [email protected])

q 2009 European Society of E

Abstract

This review attempts to use evolutionary life-history theory in understanding child growth in a broadevolutionary perspective. It uses the data and theory of evolutionary predictive adaptive strategies fortransition from one life-history phase to the next, and the inherent adaptive plasticity in the timing ofsuch transitions. Humans evolved to withstand energy crises by decreasing their body size, andevolutionary short-term adaptations to energy crises utilize a plasticity that modifies the timing oftransition from infancy into childhood, culminating in short stature at the time of an energy crisis.Transition to juvenility is part of a strategy of conversion from a period of total dependence on thefamily and tribe for provision and security to self-supply, and a degree of adaptive plasticity is providedand determines body composition. Transition to adolescence entails plasticity in adapting to energyresources, other environmental cues, and the social needs of the maturing adolescent to determinelifespan and the period of fecundity and fertility.Conclusion: Life-history transitions are the times when the child adaptively responds to environmentalcues in order to enhance growth–body composition–lifespan–fecundity schedules and behavioralstrategies that yield the highest fitness in a given environment.

European Journal of Endocrinology 160 135–141

Introduction

Life-history evolutionary theory is considered here as partof evolutionary development biology (evo–devo) (1) as itaddresses factors that produce variation in life histories,which are found both among and within species. Here, it istaken into the realm of clinical medicine and child growth,following the first article in this ‘evo–devo’ series (2). Inthe case of humans, life-history evolutionary theory is bestunderstood in the context of biological rationale andcultural expressions as a solution to an ecological problemposed by the environment and subject to constraintsintrinsic to the organism (3). Among the questions posedare: why are organisms small or large? Why do theymature early or late? Why do they have few or manyoffspring? Why do they have a short or a long lifespan?Why must they grow old and die? Several reviews on thistopic include (2, 4–7).

The transition from one life-history phase to thenext requires a mechanism for the onset of the latter.Thus, the transition from infancy to childhood isassociated with the setting in of the dominance of theGH–insulin-like growth factor 1 (IGF1) axis. Thetransition into juvenility requires the development ofandrogen-generating adrenal reticularis. The beginningof adolescent-related puberty is a function of thehypothalamic–pituitary–gonadal (HPG) axis maturation.

ndocrinology

This review presents the data and theory ofevolutionary predictive adaptive strategies for transitionfrom one life-history phase to the next and the inherentadaptive plasticity in the timing of such transitions inorder to match not only energy supply, but also otherenvironmental cues.

Child growth and the theory of lifehistory

Life history has been defined as the strategic allocationof an organism’s energy toward growth, maintenance,reproduction, raising offspring to independence, andavoiding death (3, 7). For a mammal, it is, amongothers, the strategy of when to be born, when to beweaned, when to stop growing, when to reproduce, andwhen to die in the best way as to increase its fitness (8).

Life-history phases

During the evolution of the hominin, childhood andadolescence have been added as new life-history phases(Fig. 1, Table 1) (3). Thus, Homo sapiens have fourprolonged and pronounced postnatal pre-adult life-history phases: infancy, which lasts for 30–36 months

DOI: 10.1530/EJE-08-0445

Online version via www.eje-online.org

Figure 1 Pre-adult life history for boys and girls. Childhood andadolescence are relatively late development in human evolution.The first molar tooth (M) erupts in other apes at the end of infancyand in humans at the end of childhood.

136 Z Hochberg EUROPEAN JOURNAL OF ENDOCRINOLOGY (2009) 160

and ends with weaning from breast feeding intraditional societies; childhood, which lasts for anadditional 2–4 years, culminating in a degree ofindependence for protection and food provision; ajuvenile stage of 3–4 years that concludes with thereadiness for a sexual maturation process (9); andadolescence, which lasts for 3–5 years, culminating infertility at an average age of 18 (10).

By reconstruction and without certitude, it has beensuggested that some 3 000 000–4 000 000 years agothe early hominin Australopithecus afarensis had merelytwo postnatal, pre-adult life-history phases: infancy andjuvenility (7, 11). He had a long infancy of about 6 years(as compared with 5 years of the chimpanzee), but acomparatively short lifespan, and his first molar tootherupted in mid-infancy (Fig. 1). With a marked growthof his brain size, 1 900 000 years ago Homo habilis hadto be born less mature to fit into a narrow bipedalmaternal pelvis. He had a shorter period of infancy anddeveloped a new strategic life-history phase: childhood,defined by weaning from breast feeding, slowing andstabilization of growth velocity, dependence on olderpeople for food provision and protection, with the firstmolar erupting at the transition from infancy tochildhood. While the brain size steadily grew, andhence newborns had to be born less mature to fit into

Table 1 Life-history phases, growth milestones, and social function.

Approximate age Characteristics of life-history phases

0–30 months Infancy: breast-feedingFeeding by maternal lactation. Rapid and

More than 50% of resting metabolic ra2–6 years Childhood: dependence for food and pro

Slowing and stabilization of the growth rarebound. Dependence on family for fo

6–11 years Juvenility: initial independenceAdrenarche. Finding much of own food.

rate. Competing with adults for food an11–15 years Adolescence: preparation for adulthood,

Dimorphic secondary sexual characterististill pre-adult size. Learn and practice

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the narrow birth canal, infancy grew shorter andchildhood has been thriving and extending, with thefirst molar progressively deferred in H. sapiens into thetransition from childhood to juvenility. Adolescence, asreconstructions suggest, came about as late as 100 000years ago as a distinct life-history phase, with the typicalpubertal growth spurt and rapid sexual puberty,deferring the assumption of adulthood in a speciesthat lives longer. The entire assemblage has beenextremely successful, and the resulting overpopulationof humans is, for better or for worse, the consequence ofthat winning strategy.

Transitions between life-history phases

Staging has retained a central place in evolutionary life-history theory and in endocrine deliberation, andrightly so. In defining a life phase for evolutionary,physiological, social, or endocrine inquiries, oneinevitably needs to define the stage’s beginning andend. Onsets are a key concept of that narrative, whereasoffsets remain even more intricately difficult to charac-terize. Offsets of life-history phases may not really exist.

Multiple hormone mechanisms have evolved toactivate both physiological and behavioral traits at theright time and in the correct context as the child transitsfrom infancy to childhood, then to juvenility, and laterto adolescence and adulthood. As the child transits frominfancy to childhood, the GH–IGF1 sets in and newbehavioral traits develop, but the metabolic forces thatdrive infantile growth remain as active and the infantilemental achievement develop further, although someinfantile manners recede while the child ceases to feedon mother’s milk. At adrenarche, androgens come intoplay for the first time, and behaviors change, but theGH–IGF1 axis remains as imperative, while the juvenilejoins adults in their daily activities. Adolescence isassociated with the onset of the hypothalamic–pitu-itary–gonadal axis, while both adrenal androgens andthe GH–IGF1 axis do not set off secretion.

Endocrine mechanisms are available to set off any ofthese means in adjusting to environmental signals:malnutrition will slow the GH–IGF1 axis, anorexia

decelerating growth. Rapid growth of the brain. Deciduous dentition.te is devoted to brain growth and functiontectionte. Immature dentition. Extended family and tribal care. Adiposity

od and security. Immature motor control. Cognitive advancement

Avoiding predators. Mid-childhood transition, then slowing growthd space. Joining society functions/elementary schoolnon-fertilecs. Growth acceleration. Peer-grouping. Stature and muscularity areadult skills while still infertile

Evo–devo of child growth II 137EUROPEAN JOURNAL OF ENDOCRINOLOGY (2009) 160

nervosa will block adrenal androgen secretion, andphysical exertion will slow the HGP axis, to name justthree possibilities.

Phenotypic plasticity and adaptation

Humans live under a variety of environmental con-ditions unprecedented in nature, including the entirerange of geographical latitudes and altitudes, as well asextremely diverse weather conditions. Whereas theabove vary slowly, nutritional conditions may changemore rapidly, and evolution has provided for mech-anisms to adapt to these extremes, and socio-culturaladjustments filled the remaining gaps when changeswere faster than the evolutionary time scale. Thesecular trend in child growth and puberty is a dazzlingexample of such an adaptation.

As a consequence of life conditions under changingenvironment, children may be stunted for short orlonger periods, be underweight or overweight, and be atrisk for disease. In the endocrine jargon, this has beenlabeled ‘developmental programming.’ The evolution-ary language for the same is ‘predictive adaptiveresponse’ (12). A life-history theory analysis rephrasesthese to the concept of ‘trade-offs’ (5). Under adverseconditions, Bogin et al. argue, trade-offs result inreduced survival, poor growth, constraints on physicalactivity, and poor reproductive outcomes (5).

Whereas programming implies permanent maladap-tive effects that place people at risk for disease, predictiveadaptation considers the phenotypic changes as adap-tive, and at two levels: i) short-term adaptive responsesfor immediate survival and ii) predictive responsesrequired to ensure postnatal survival to reproductiveage (fitness). Organismal size, including child growth, isprobably the supreme case in point of the paradigm.Franz Boas (1858–1942) introduced the evolutionaryconcept of developmental plasticity early in the 1900s;this was expanded in the 1960 by Lasker (13), andGluckman and Hanson suggested the concept ofpredictive adaptive response (12, 14), postulating thatit is the mismatch between intrauterine stunting andearly infantile catching up that results in the ensuingmetabolic morbidity. Predictive adaptive responsesrequire trade-offs, such as reduced fetal growth infavor of survival, or early puberty with lower qualityoffspring against slow maturation and later firstpregnancy with higher quality offspring. A givengenotype can generate multiple phenotypes dependingon the environmental conditions experienced by theorganism during development (15).

Infancy–childhood transition:determination of adult stature

As recently reviewed, it is the transition from infantileto childhood growth that determines ultimate adult

height (2). Based on the predictive adaptive responsetheory, the expected response to a secure environmentincludes the investment in large body size, whereasthe expected responses to a threatening environmentwill include a reduction in body size.

For the infancy–childhood growth transition tooccur, the child must have a positive energy balance.The infancy–childhood growth transition age isinfluenced and delayed by disease, when energyconsumption increases rapidly (2), and by under-nutrition, gastrointestinal infection, and socioeconomicimpediments, when energy supplies are scarce (16, 17).

There seems to be sufficient indirect evidence topropose that a delay in the infancy–childhood growthtransition is a predictive strategy in adapting to anenergy crisis during infancy. Yet, the contemporarycrisis of Western societies is energy saturation ratherthan shortage, and the transition from infancy tochildhood is also the age of shifting dietary saturation inaffluent societies. In children with delayed infancy–childhood transition (DICT) (2), mismatching of thepredictive adaptive response and otherwise overfeedingresults in the unwanted permutation of obesity withshort stature (18). This is well documented for migrantsfrom developing to richer countries, who are shorter butat higher risk for overweight and obesity (19). Thetrade-off approach would explain these intergenera-tional effects: physical and social abuse lead topathology rather than adaptation.

Unlike the large volume of experimental dataavailable for intrauterine programming for adult disease(20), the infancy–childhood growth transition cannotbe investigated in experimental animals; as mentioned,H. sapiens is the only remaining hominin to have achildhood. Further investigation on this topic will haveto rely on clinical research.

Childhood to juvenility transition:determination of body composition

As recently reviewed, it is difficult to decide when to setthe transition age to juvenility, as some parts of thejuvenile package may start early, and others a year ortwo later (9). Transition into juvenility may be definedby adrenarche, for the onset of adrenal androgenproduction at age 5–6 years, by tooth eruption, growthpattern, and the adiposity rebound.

For the paleoanthropologist, the transition fromchildhood to juvenility is associated with the eruptionof permanent molars at age 6 years. A comparativestudy across 21 primate species found the age of firstmolar eruption to be highly associated with brainweight (rZ0.98) and a host of other life-historyvariables (21). The study concluded that the mean ageof tooth eruption is a good overall measure of thematuration rate of a species, and in the context ofthe present discussion – the transition from childhood

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138 Z Hochberg EUROPEAN JOURNAL OF ENDOCRINOLOGY (2009) 160

to juvenility. If this is the case, then data for dentaleruption in 1837, which showed similar eruption agesto those known today (22), seem to indicate that theonset of juvenility has not changed much over the last170 years. At a time of a marked worldwide upwardtrend for height, there has been little change in thetiming of tooth eruption (23).

Another possible definition of transition to juvenilityderives from the growth curves (Fig. 2). After a period ofconstant growth rate, the peak of the ‘mid-childhoodspurt’ (greater for girls than boys) signifies a transitioninto a new growth decelerating phase at age 4.5 yearsfor girls and 5.5 years for boys. One possible conse-quence of this aspect of the transition is that laterjuvenility onset allows for a longer period of childhood,with its relative stable and high growth rate beforethe typical juvenile slow down. A year of boys’ CJtransition delay contributes to their final height anaverage of 6 cm. Thus, every month of delay injuvenility onset will advance boys’ final height by0.5 cm and girls’ by close to 0.6 cm.

Adiposity rebound is another indicator for thetransition to juveniles’ body composition. The adiposityrebound corresponds to the second rise in the age-related body mass index curve that occurs between ages4 and 6 years. Its sexual dimorphism corresponds verywell to that observed in the second derivative growthcurves, with mean boys’ rebound at age 68 months, as

Figure 2 Mean growth velocity (upper panel), and growthacceleration (cm/y2, lower panel) for boys (solid lines) and girls(soft lines). The first and second derivatives were calculated from(37). I, infancy; C, childhood; J, juvenility and A, adolescence.

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compared with girls with a mean adiposity rebound 6months earlier.

Adiposity rebound may be the first clinical sign ofjuvenility, or it may be the signal that turns thetransition on. It is interesting to note that even leangirls with precocious adrenarche have higher levels ofIGF1, IGFBP3, and leptin (24) than control, asmechanisms that may transmit the signal of adequateenergy readiness.

Transition from juvenility to adolescence

The onset of puberty has been the topic of muchresearch and many review articles. This will bementioned here only briefly, with respect to life-historyevolutionary perspective and the context of thetransition from juvenility to adolescence as a period ofadaptive plasticity. Using the paradigm of this review, Ispeak of a transition from juvenility to adolescencerather that an onset. This semantic matter entails twoaspects that are introduced here. Whereas ‘onset’implies an event that has happened at once, transitionis rather a course of actions that starts during juvenility,progressively gaining power as the child enters a full-scale adolescence. The second non-semantic matter isthat the child transits into adolescence, and hypo-thalamic–pituitary–gonadal maturation with its bio-logical effects is but one aspect of the package known asadolescence. Adaptation of adolescence to the environ-ment and the consequences of early or late transitioninvolve the many facets of adolescence.

Even during childhood and juvenility, girls havehigher estrogen levels than boys (25). The onset ofpuberty in girls is mostly considered to take place whenbreast buds erupt. However, it is now recognized thatthis is not the first sign of maturation of the femalehypothalamic–pituitary–gonadal axis. Very much likeboys, who exhibit their gonads for direct palpation andshow testicular growth, the ovaries start to growdiscretely about 2 years before breast buds appear. Thesame is true for estradiol levels, which show a rise about2 years before thelarche (26), and growth accelerates atleast 6 months before breast buds are evident. Boysshow a similar pattern of gradual maturation of thehypothalamic–pituitary–gonadal axis. Testosteronelevels start to gradually rise at a mean age of 9, longbefore gonadal growth – the so called gonadarche (26).

Just as much as the secular trend in human size hasbeen an adaptive phenomenon for an encouragingenvironment, the receding age of adolescence andpubertal development has been an adaptive responseto positive environmental cues in terms of energybalance. The ever-younger age of girls’ thelarche andmenarche may have more than a single justification. Inthe last decade, the popular explanation has been thatthis phenomenon results from environmental exposureto endocrine disruptors, thus accelerating hypothalamic

Evo–devo of child growth II 139EUROPEAN JOURNAL OF ENDOCRINOLOGY (2009) 160

maturation. Whereas it may have a bearing on theearlier age of thelarche, which is a recent trend, it canhardly explain the secular trend in the age of menarcheover the last 170 years. An evolutionary perspective onthis worldwide trend has been proposed by Gluckmanand Hanson (27). They have challenged the conceptthat this has been pathological, and suggested thatreproductive and life-history strategies might bereflected in the more frequent presentation of femaleswith early onset adolescence.

With respect to puberty, women face a trade-offbetween spending a long time accumulating resourcesthrough childhood growth, thereby improving the oddsfor successful pregnancy, against beginning reproduc-tion and increasing the number of reproductive cycles. Itturns out that a later first birth allows for a longer periodof adolescent weight gain, and that heavier women intraditional societies are more fertile, both correlatingwith higher birth rates. This trade-off has been used tomodel the optimal age at first birth. The optimal age atfirst birth under such models is 18 years, near theobserved mean of 17.5 years in such societies (28).

The environmental cues for the transition intoadolescence vary with species and gender, and it maybe related to altitude, temperature, humidity, andlighting, but mostly it relates to energy balance. Sensorsin the hypothalamus and hindbrain monitor thesesignals and permit high-frequency GNRH1 releasewhen the signals reach appropriate levels (29). Theconsequences of puberty and adulthood that follow,such as the defense of territory or mate, pregnancy, andcare of young, are energetically expensive. Theindividual must sense whether he/she has grownsufficiently (through metabolic cues), what his/herrelationship is to other individuals (through socialcues), and whether conditions are optimal to beginthe reproductive process (through environmental cues)(30). Metabolic fuel availability, insulin, glucose, andleptin in females serve as important signals for theattainment of somatic growth sufficient to supportpregnancy (31).

Consumption of more nutritious foods, such as thosederived from animal protein, increased by w2 600 000

years ago when an early hominin displayed animportant behavioral shift relative to ancestral forms:the recognition that a carcass represented a new andvaluable food source. The shift in the hominin ‘preyimage’ to the carcass and the use of tools for butcheryincreased the amount of protein and calories available,irrespective of the local landscape. Life-history theoryclaims that 2 600 000 years ago was before homininhad an adolescent stage, and a childhood stage had juststarted to evolve (7, 8); the age range of 3–5 years wasthat of childhood, and in the absence of adolescence, thetransition to juvenility might have determined the ageof fertility.

In the past few decades, we have been facing a uniquejuvenility–adolescence transition where puberty hasadvanced but psychosocial adolescence has beendelayed. Physical growth and the hypothalamic–pituitary–gonadal axis start their transit into matu-ration at the end of the first decade of life, but as late asthe second and early third decades of life, adolescentsare not mature enough to assume adult roles (27).Biological maturation has come to precede psychosocialmaturation significantly for the first time in ourevolutionary history, and this ‘developmental mis-match,’ as Gluckman and Hanson described it, hasconsiderable societal implications. This remains beyondthe scope of this review, which focuses on aspects ofchild growth.

The juvenile–adolescence transitional slowinggrowth rate has been suggested to be a predictiveadaptive period, and the response has to do withlongevity in a negative relationship with nutritionduring this transition (32); poor food supply results inlonger life. Moreover, food supply during this transitionhad an effect that lasted for at least the children andgrandchildren generation, and interestingly enough, itwas inherited from fathers to their sons and daughter(32). Using the Northern Sweden Overkalix cohorts of1890, 1905, and 1920, this study analyzed food supplyeffects on offspring and grandchild mortality relativerisk, using 303 probands and their 1818 parents andgrandparents. Paternal grandfather’s food supply waslinked to the mortality relative risk of grandsons, while

Figure 3 Periods of adaptiveplasticity in the transition betweenlife-history phases (double arrows).Transition from infancy to childhoodendows with a predictive adaptiveresponse that determines adultheight. Transition from childhood tojuvenility bestows a predictiveadaptive response that resolvesadult body composition and meta-bolic consequences. The transitionfrom juvenility to adolescenceestablishes longevity and the age offecundity and reproduction.

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140 Z Hochberg EUROPEAN JOURNAL OF ENDOCRINOLOGY (2009) 160

paternal grandmother’s food supply was associatedwith the granddaughters’ mortality. These transgenera-tional effects were observed with exposure during thejuvenility–adolescence transition (both grandparents)or fetal/infant life (grandmothers), but not during eithergrandparent’s puberty. This mode of inheritancesuggests that the transgenerational transmissions aremediated by the sex chromosomes, X and Y.

Transgenerational inheritance of phasetransition

Prematurity, an obvious change in transition from onelife phase to another, is a familial trait (33). Thistransition period is not dealt with in this treatise.Likewise, the transition into adolescence is a well-known familial trait without a genetic background, or,at least, such genes have not yet been discovered. I darespeculate that they never will be. The genes expressplasticity/changeability but not the plastic changes. Wehave some unpublished observations that DICT is also afamilial trait, and the same is true for the transition intojuvenility (34) and precocious pubarche.

These transgenerational traits are adaptive responsesto environment circumstances, which used to lastlonger than a single generation. In any event, modernlifestyles, with rapid changes in world climate andmassive rapid population shifts over long distancesmight have changed the rules, leading to a mismatchbetween the environment and the phenotype orbetween several phenotypic phenomena of the life-phase package (12).

Low birth weight is common in developing countries.However, migrant mothers also give birth to smallerinfants despite improved healthcare (35), demonstrat-ing the transgenerational influence of their ancestorenvironment. In a study in rural Guatemala, pregnantwomen and their offspring received one of two types ofnutritional supplements (36). One was a drink called‘atole,’ which was enhanced with protein and calories;the other was a drink called ‘fresco,’ which wasenhanced with calories, but less than the calories inthe atole drink. The infants and children of the originalstudy received these nutritional supplements until age7. In the 1990s, women who were part of the originalstudy as children were asked to be part of a follow-upanalysis to investigate the transgenerational influencesof the original intervention (5, 36). The mothers hadbeen measured repeatedly from their birth until age 3,as were their children. The report shows that thecurrent generation of infants grew faster than theirmothers did. Thirty years after the initial intervention,infants of women who as babies received the protein-energy drink atole grew faster than infants of motherswho received fresco (calorie-rich only).

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Conclusions

Like other organisms, humans evolved to withstandenvironmental hardships like energy crises by respond-ing in ways that would maintain some evolutionaryfitness, even if sub-maximal. The means to do this is aseries of predictive adaptive responses that utilize thesensitive times of transitions from one to its next life-history phase, each assigned with its own domain(Fig. 3).

The transition from infancy to childhood is assignedwith predictive adaptation to the environment of bodysize. Short-term adaptations to energy crises utilize aplasticity that postpones the timing of transition toreduce height and advances timing to enhance size.

The transition from childhood to juvenility is part of astrategy in the transition from a period of totaldependence on the family and tribe for provision andsecurity into self-supply; it is assigned with a predictiveadaptive response of body composition and energymetabolism.

The transition from juvenility to adolescence isassigned with lifespan and the age and length offecundity. It entails plasticity in adapting to energyresources, other environmental cues, the social needs ofadolescence, and their maturation to determine fitnessdirectly.

Declaration of interest

The author declares no conflict of interest.

Funding

This research did not receive any specific grant from any fundingagency in the public, commercial or not-for-profit sector.

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Received 15 October 2008

Accepted 10 November 2008

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