Upload
others
View
5
Download
0
Embed Size (px)
Citation preview
R EV I EW AR T I C L E
Bioarchaeological evidence for adaptive plasticity andconstraint: Exploring life-history trade-offs in the human past
Daniel H. Temple
Department of Sociology and Anthropology,
George Mason University, Fairfax, Virginia
Correspondence
Daniel H. Temple, Department of Sociology
and Anthropology, George Mason University,
Robinson Hall B, Room 305, MSN-3G5,
Fairfax, VA 22030-4444.
Email: [email protected]
Funding information
National Science Foundation, Grant/Award
Numbers: BCS 104490, 104490); Wenner
Gren Foundation for Anthropological Research,
Grant/Award Numbers: 07318, 07135; Japan
Society for the Promotion of Science, Grant/
Award Number: 07012
AbstractThe Developmental Origins of Health and Disease paradigm evaluates the consequences of
early life stress on health at later stages of life. Interacting with this paradigm represents a pro-
found opportunity to leverage the lifespan and contextual approaches to human skeletal
remains adopted by bioarchaeological research. Teeth and bone provide evidence for stressors
experienced early in life. These events represent evidence for adaptive plasticity as Individuals
survive the events through reallocation of energy to essential physiological functions, which
inhibits enamel and skeletal growth. Age-at-death, adult body size, chronic infection, or child-
hood mortality may be used as covariates to better understand the physiological constraints
operating on individual bodies following survival of early life stress. Contextual evidence from
cemeteries provides clues to the ecological and cultural contingencies that exacerbate or miti-
gate the expression of these trade-offs. Future studies should incorporate newly derived
methods that provide reproducible and precise ways to evaluate early life stress, while incorpo-
rating populations that are often neglected.
KEYWORDS
bioarchaeology, growth and development, linear enamel hypoplasia, stress
1 | INTRODUCTION
The Developmental Origins of Health and Disease (DOHaD) paradigm
has an overarching interest in how early life environments impact the
health and disease of individuals at later stages of the life course. Early
life environment refers to developmental periods that include oocyte,
spermatozoa, zygote, fetal, infancy, and childhood. Clinical and experi-
mental biologists have long documented persistent relationships
between early life adversity and poor health outcomes for adults1–4
and even commented that stress contributing to growth deficits may
have consequences for survival.5,6 For example, survivors of war and
famine frequently express shortened stature, and diminished height is
often associated with mortality risk, cardiovascular disease, and
chronic infection.7–10 Correlations between neonatal mortality, car-
diovascular disease, and respiratory ailments were found in a regional
evaluation of National Census and Survey records that documented
cause of death in more than 20,000 people from the United Kingdom
between 1968 and 1978.11,12 Using records kept by midwife Ethel
Margaret Burnside that included birth weight, placental weight, and
birth length, negative correlations between birth weight and placental
weight with adult systolic and diastolic pressure were found in
449 individuals born between 1935 and 1944.13,14 These results were
used to support the development of the thrifty phenotype hypothesis.
The thrifty phenotype hypothesis predicts that energy sparing behav-
ior by the fetus permits short-term survival in response to nutritional
shortages but results in greater risk of metabolic disorders later in life
due to impaired pancreatic growth.15 As a whole, findings from this
research were used to build a paradigm centered on identifying stress-
ful conditions prior to and immediately after birth, and the long-term
impacts of these factors on adult body size, cardiovascular disease
risk, metabolic syndromes, and mortality risk.16,17
Relationships between early life environment and health at future
stages of the life course should, however, be carefully evaluated. For
example, survivors of the Dutch Winter Famine who experienced
stress early in gestation had a higher glucose tolerance than those
exposed to this environment later in gestation, while no difference in
lipid concentrations was found in survivors of the Siege at Lenin-
grad.18,19 In addition, Polish individuals with low birth weight have
Received: 19 January 2018 Revised: 26 June 2018 Accepted: 28 September 2018
DOI: 10.1002/evan.21754
34 © 2018 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/evan Evol Anthropol. 2019;28:34–46.
improved physiological efficiency in response to workload, while
Jamaicans of low birth weight had lower chronic disease risk than
those with higher birth weight.20,21 Such findings suggest that greater
emphasis on context and method is needed by studies focused on
early life stress. Specifically, these approaches should take into
account cultural and environmental context of birth and future life,
timing of insult, the utility of birth weight as a measure of early life
stress, and the physiological outcomes targeted at later stages of life
(e.g., muscular efficiency, metabolic syndrome, cardiovascular disease,
chronic infection, etc.).
Gluckman and colleagues22 note that these findings did not
undermine the general conceptual framework surrounding earlier
studies and instead prompted a more integrative, mechanistic
approach to these questions, which included the founding of DOHaD
as an academic society. The Third International Congress on DOHaD
grew out of the Second International Congress on Fetal Origins of
Adult Disease in 2003 as an increasingly integrated approach to, “[rec-
ognizing] the broader scope of developmental cues, extending from
the oocyte to the infant and beyond, and the concept that the early
life environment has wide-spread consequences for later health.”23
The concept was adopted by subsequent reviews that set forth the
scope for DOHaD as an epidemiologically descriptive field.23,24 How-
ever, careful evaluation of the Report on the 3rd International Con-
gress on DOHaD portrays an integrative endeavor that sought
insights from evolutionary biology, developmental plasticity, studies
of social hierarchies, and populations in transition.23 Thus, the emer-
gence of DOHaD corresponds with the appropriation of anthropologi-
cal and evolutionary perspectives into this paradigm.
One example of the appropriation of evolutionary insight into
DOHaD includes the predictive adaptive response (PAR) hypothesis.
The PAR hypothesis emphasizes developmental plasticity, evolution-
ary adaptation, and environmental context to explain the relationship
between early life stress and metabolic syndrome.25,26 This hypothe-
sis states that when individuals experience nutritional deprivation dur-
ing fetal or early postnatal development, predictive physiological
responses are built into the organism that help thwart nutritional
dearth through energy sparring.27–29 These physiological cues include
increased insulin resistance, greater propensity to store fat, increased
glucocorticoid receptors in the liver, greater expression of PEPCK
alleles in the liver, and hypomethylation of angiotensinogen.27–29
However, increased risk of metabolic disorders associated with diabe-
tes and cardiovascular disease are found when the birth environment
is a mismatch. Here, the term mismatch refers to a fetal environment
that is deprived of essential nutrients, but a birth environment where
high fat and glucose rich foods are available in abundance.
The PAR hypothesis assumes that fetal bodies use signals from
the mother as predictors of future environments and that this repre-
sents an evolved mechanism generated through natural selection.
Critical responses to the PAR argue that physiological cues received
by the fetus are derived from past maternal and deeper ancestral envi-
ronmental experiences, while birth environments rarely correspond to
those experienced by the fetus diminishing the efficacy of fetal
forecasting.30–32 In addition, the PAR hypothesis fails to account for
the functional mechanisms and trade-offs associated with such a
response and therefore remains a descriptive postulate.33
Worthmann and Kuzara33 provide a useful model to help explain
how individuals survive adverse environments at the earliest stages of
life yet experience increased risk for growth disruption and disease by
contextualizing developmental plasticity and physiological trade-offs
within the endocrinological literature. In life history theory, trade-offs
reference correlations or linkages between two traits that constrain
the simultaneous optimization of both traits in response to natural
selection.34 Physiological trade-offs occur when two or more systems
compete for energy. Under these circumstances, an increase in energy
allocation to one system reduces the allocation of energy to other
systems.35,36 Energetic investments may be allocated to systems
associated with growth, maintenance, and reproduction. Survival of
early life stress is mediated through energy sparring and reallocation
to essential tissue function but reduces investment in other physiolog-
ical systems. The organism invests in short-term survival, while reduc-
ing energetic investments in future growth, maintenance, and
reproduction.
One functional mechanism modulating this process is the
hypothalamic–pituitary–adrenal (HPA) regulation of cortisol levels.
Worthman and Kuzara33 describe cortisol as a master regulator
(or dysregulator) of physiological function, and a number of these
roles are important to briefly highlight. Cortisol is an anti-
inflammatory hormone that speeds the metabolism of fat, protein, and
carbohydrates through glycogenesis in the vascular system to
meet increased metabolic demand while producing short-term immu-
nological and muscular boosts.37 However, cortisol also acts as a
growth and immunological suppressant suggesting phenotypic conse-
quences for short-term investment in survival at later stages of
development.38–49 These consequences suggest that the activation of
the HPA axis in response to early life stress presents a near-term ben-
efit through survival but long-term consequences for growth, mainte-
nance, and survivorship. Overall, this model invokes the concept of
adaptive plasticity and physiological constraint modulated by the HPA
axis as an evolved mechanism for investment in short term survival
with long-term consequences for individual life histories.
Adaptive plasticity may be defined as a, “…reaction norm that
results in the production of a phenotype that is in the same direction
as the optimal value favored by selection in the new environment.”50
These reaction norms have the advantage of maintaining population
stability until selection or biocultural modifications to the environment
reduce the likelihood of mortality or extinction. Within adaptive plas-
ticity, there exist adaptive and nonadaptive reaction norms. Adaptive
reaction norms move the phenotype closer to an adaptive peak, while
nonadaptive reaction norms move the phenotype further from the
adaptive peak.50 In the case of the HPA axis, a strong argument can
be made that this stress response represents an adaptive reaction
norm. For example, in cases of nutritional dearth or infection, the HPA
axis stimulates metabolism and boosts the immune system. This
response moves the phenotype closer to the optimum required to sur-
vive these environmental stressors.51–53 Costs and limits to adaptive
plasticity are also highlighted: costs reduce fitness and limits reference
an inability to express an optimal phenotype.54 One set of costs asso-
ciated with adaptive plasticity includes a series of responses that may
be characterized as physiological constraints. Physiological constraints
reference limits placed on adaptive plasticity through differential
TEMPLE 35
modulation of energy to competing processes.34 Here, physiological
constraint is indicated by reduced energetic investment in growth,
maintenance, and/or reproduction following survival of early life
adversity. The interaction between adaptive plasticity and constraint
remains complex and must be demonstrated by negative correlations
between adaptive change and future consequences, which is challeng-
ing given the long life histories of humans and other primates.34,55,56
Examples of the interplay between adaptive plasticity and physiologi-
cal constraint are found in numerous taxa where survival of early life
stress is associated with faster growth, earlier maturity, reduced
reproductive output, and exacerbated mortality schedules.57–59 In a
broad synthesis, Crespi and Denver60 demonstrate that the tadpole
HPA axis interacts with the thyroid to prompt early metamorphosis to
survive these events and salvage reproductive potential, although
smaller body size and increased mortality risk still occur. A more
recent study found that these prenatal stress responses were highly
conserved along the HPA axis across vertebrate species.61 These find-
ings suggest a role for deep homology in the evolved mechanisms of
adaptive plasticity and physiological constraint in response to adverse
early life environments, although less is known about the interaction
of these mechanisms in the past.
The findings discussed earlier denote the complex, contentious,
and contingent history of DOHaD, and many of these results yield
important conceptual frameworks where bioarchaeological research is
best operationalized. For example, work involving endocrinologically
induced life history trade-offs provide bioarchaeologists with an
understanding of the complex interplay between surviving early life
stress events and the consequences for energetic investment in
growth, maintenance, and reproduction at future stages of develop-
ment. Stress events do not happen in a vacuum, and surviving these
events early in life may deplete energetic resources for investing in
growth and maintenance at later ages resulting in early mortality or
greater risk of chronic infection. Bioarchaeologists may pinpoint evi-
dence for the survival of early life stress events and build on skeletal
and dental indicators of stress and mortality experienced at later
stages of the life course to explore these trade-offs. Results from pre-
vious DOHaD studies also clarify the need for greater context in inter-
pretation. Context includes the timing of early life stress events as
well as the culturally and environmentally contingent nature guiding
the human response to these experiences at later ages. In this sense,
bioarchaeological research may make a substantial contribution to the
study of adaptive plasticity and physiological constraint by exploring
variation in the expression of these trade-offs in human skeletal
remains within environmentally and culturally specific contexts. The
subsequent sections of this article are dedicated to exploring context-
driven bioarchaeological approaches to DOHaD and developing prom-
ising avenues for future inquiry.
2 | BIOARCHAEOLOGICAL APPROACHES
Bioarchaeology is the contextual analysis of human skeletal and dental
remains.62 Bioarchaeology emerged from the application of skeletal
biology to the paradigms of processual archeology and cultural ecol-
ogy.62,63 This historical agency prompted interest in using skeletal
indicators of stress and disease to understand the consequences of
the agricultural transition, urbanization, and contact.64 These studies
relied on a comparative approach that emphasized differences in the
average or prevalence of skeletal indicators of stress and disease
between samples to evaluate the relative health of populations. These
methods were critiqued due to the underlying assumption that the
prevalence of skeletal indicators of stress and disease revealed a
straightforward relationship with health. 62,65,66 The critique empha-
sized that selective mortality and hidden heterogeneity may mask
deeper differences in health between populations and that these dif-
ferences may be obfuscated when uncritically compared. Hidden het-
erogeneity references the idea that all individuals are heterogeneous
in terms of mortality risk and that many of these risk factors may not
appear in the skeleton, while selective mortality emphasizes possibility
that mortality may be exacerbated by these unknown risk factors as
well as the underlying processes contributing to the formation of skel-
etal and dental indicators of stress.66 These observations are sub-
sumed under the appellation, Osteological Paradox, a reference to the
paradoxical relationship associated with the interpretation of health
based on the prevalence of skeletal indicators of stress and disease.
The discussion surrounding this critique has been vociferous, although
there is coalescing agreement around the idea that these problems
must be methodologically addressed by incorporating epidemiological
models that estimate risk of death as a function of skeletal lesions and
morphological variation.67 Importantly, recent syntheses of the osteo-
logical paradox suggest that the models associated with this critique
may be adopted by bioarchaeologists exploring DOHaD related ques-
tions, specifically those exploring the relationship between adverse
early life environments and risks for greater mortality and disease at
later stages of the life cycle.67
The methods associated with the osteological paradox provide a
basic framework for exploring questions related to DOHaD. These
methods include modeling risk of death associated with skeletal and
dental indicators of early life stress; associations between chronic
infection and skeletal and dental indicators of early life stress; risk of
death associated with diminished body size; and modeling survivor-
ship in relation to body size in surviving and nonsurviving elements of
a sample that includes pre-adults and adults. While not explicitly
based on the concept of life history trade-offs, these methods provide
a cutting-edge approach to explore adaptive plasticity and physiologi-
cal constraint in human skeletal remains. Another set of arguments by
the osteological paradox emphasize the need for context and tight
temporal control over samples to account for differences in hidden
heterogeneity. These arguments exist as central tenants to DOHaD,
where environmental context, timing of stress events, and socioeco-
nomic circumstances have figured prominently in interpreting results.
Exploring human life history and DOHaD in bioarchaeological
research has been advocated by numerous comprehensive
reviews.68–72 The use of the term DOHaD in bioarchaeological con-
text does, however, require some semantic fine-tuning. DOHaD is a
comprehensive, quasi-academic discipline united by an interest in the
early life environment, but diversified in approaches to exploring
future life outcomes.23 For example, DOHaD is linked to kidney disor-
ders, cardiovascular disease, endocrine function, mental well-being,
and myriad conditions that do not leave traces on human
36 TEMPLE
remains.14,33,73 The best way forward for bioarchaeologists interacting
with DOHaD may be to evaluate adaptive plasticity and physiological
constraint using skeletal indicators of early life adversity and those
associated with reduced growth and maintenance at later stages of
the life course. The expression of physiological constraints may be fur-
ther probed within the context of the cultural and ecological contin-
gencies acting to accentuate or mitigate these interactions. Thus,
bioarchaeology contributes to a limited, yet important set of questions
affiliated with DOHaD.
It is important to emphasize that human skeletal and dental
remains are only observable at the time of death, and DOHaD studies
are longitudinal evaluations of clinical or experimental samples. How-
ever, careful analysis of the human skeleton and dentition reveal
events that represent exposure to early life adversity where individ-
uals survived through the reallocation of energetic resources along
the HPA axis. Cortisol dysregulates insulin-like growth factor and cal-
cium absorption as well as disrupts the sodium/potassium balance
within ameloblasts and may be implicated in disturbances to the
secretory stage of enamel formation.44–48 In addition, cortisol dysre-
gulates skeletal growth by suppressing growth hormone pulsations
and expression in the growth plate as well as osteoblast differentia-
tion in the periosteal mesenchyme.38–41 Cortisol also inhibits pulsa-
tions of gonadotropin hormones during puberty, which may suppress
the adolescent growth spurt.42,43
Linear enamel hypoplasia (LEH) is a condition characterized by
grooves or furrows of enamel deficiency caused when shortened
enamel prisms are produced during the secretory phase of amelogen-
esis (Figure 1).74,75 Enamel production is stopped earlier than normal
and accentuated striae of Retzius are produced.76 This basic definition
of LEH has been intensively referenced by bioarchaeological research
that envisions LEH as an indicator of developmental damage. The pro-
cess contributing to LEH is, however, mostly transitory as the gradual
return to prismatic shape of enamel rods is reported in the cervical
walls of defects.77 LEH may, therefore, be seen as evidence for adap-
tive plasticity—an event that is certainly associated with physiological
damage, but one where the individual survived and the LEH formed as
a response to the physiological mechanisms promoting survival
(i.e., physiological trade-offs). Similarly, growth differences in height
and weight during infancy and childhood are often expressed in adult-
hood and attributed to the energetic cost of investment in survival.78
This suggests that subadult and adult body size may be used as evi-
dence for the survival of early life adversity. Vertebral body height
and neural canal dimensions are also potential indicators of early life
stress. Vertebral body height increases between birth and 5 years of
age, then remains dormant until the adolescent growth spurt between
10 and 13 years of age.79 Fusion of the spinous process occurs
around 1–2 years of age, while the neural arch fuses to the vertebral
body at 5 years.79 Measurements of the transverse and anteroposter-
ior diameter of the neural canal provide evidence for disruptions to
this process.80 Taken as a whole, the human skeleton and dentition
preserve evidence of stress events experienced early in life, although
the production of these defects may be seen as a deeper physiological
strategy associated with survival as the event was preserved in the tis-
sues of an individual that continued to live.
Negative correlations with future physiological outcomes in life
must be demonstrated to adequately support arguments in favor of
physiological constraint.34,55,56 Maintenance references the capacity to
preserve existing tissues and physiological capabilities, and energy
invested in surviving adversity early in life competes with energy
invested in maintenance.49 Long-term consequences of early life stress
to the capacity for maintenance include damage to the immune system.
Cortisol inhibits the production and function of lymphocytic cells, while
also dysregulating antibody producing cells, white blood cells, immuno-
globulins, and T-lymphocytes.49 The human skeleton and dentition pre-
serve evidence for chronic disease and age-at-death suggesting that
bioarchaeological research may evaluate correlations/risk associated
with early life stress and disease/mortality at later ages. For example,
risk of chronic infection may be compared between individuals with
and without skeletal and dental evidence for early life adversity using
specific and nonspecific skeletal indicators of infection. Alternately, sus-
ceptibility to growth disruption may be explored by estimating the num-
ber or periodicity of LEH following early life stress.81,82 Age-at-death
may also be used to evaluate the ultimate trade-off with surviving early
life stress, exacerbated mortality schedules. Finally, the context laden
approach of bioarchaeological research has the capacity to demonstrate
how social and ecological contexts may accentuate or mitigate physio-
logical constraints following the survival of early life stress events. That
is, increased risk of death and disease may not be predetermined out-
comes of surviving early life adversity, and the contextual approach of
bioarchaeological research helps reveal the environmental and cultural
contingencies that contribute to this variation.
2.1 | Adult body size
Adult stature and mortality were correlated in colonial-era Andaman
Island groups.83 Plasticity in growth response was the primary driver
of this variation: faster maturation lead to an earlier cessation of
FIGURE 1 Accentuated perikymata help identify the presence and
timing of linear enamel hypopolasia formation. This imagedemonstrates accentuated perikymata in an early adolescent malefrom the Yoshigo site, ca. 3,300–2,800 BP. Numbers are placed onperikymata associated with the occlusal wall of the defect, the regionassociated with disrupted enamel formation
TEMPLE 37
growth. These findings were interpreted within the broader sphere of
adaptive plasticity and constraint as faster maturation likely permitted
earlier reproduction, but this process was associated with elevated
mortality. The impact of early life stress on survivorship in the wake
of infectious disease epidemics is also illustrated in historic cemeteries
used as repositories for victims of bubonic plague.84 Individuals with
shorter stature had a greater risk of dying from the bubonic plague in
historic London, although this association is not repeated under condi-
tions of normal mortality. Epidemic disease appears to have acted as a
mortality driver among individuals who survived growth disruptions
early in development. In another instance, short stature was associ-
ated with elevated mortality risk in only high status females in an eco-
nomically diverse sample from Industrial London.85 These results are
somewhat surprising given that economic wealth is often assumed to
buffer against mortality elicited by early life stressors. However, the
frailest individuals in the poor sample died before adulthood due to
interactions between diet and infectious disease suggesting that
(a) skeletal indicators of stress are not always straightforward in
expression (i.e., the shortest may not always die youngest) and
(b) local environmental conditions greatly influence the expression of
life history trade-offs following early life stress events.
Additional studies use factors such as the timing of stress events
or evidence for developmental stability as measures of exposure to
early life stress and the resultant consequences on life history. Trans-
verse diameter of the vertebral neural canal was associated with adult
mortality in low status males and high/middle status females in Medi-
eval and Historic London, while no mortality risk was found in high
status males and low status females.86 The results suggest variation in
the physiological constraints following early life adversity may occur
according to economic status or gendered identities. Another study
compared cause of death and fluctuating asymmetry of the craniofa-
cial skeleton in a documented skeletal sample from Portugal.87 These
researchers found higher rates of facial asymmetry in individuals who
died due to degenerative (cardiovascular and metabolic disorders)
compared to infectious conditions, providing some support for rela-
tionships between early life environment and cardiovascular disease
observed in living populations. Studies of hunter-gatherers (prehistoric
and contemporary) found no association between the presence of
LEH and adult height.88,89 However, individuals with comparatively
earlier forming LEH had shorter stature.88 This suggests that contex-
tual information such as age-at-defect formation also helps reveal cir-
cumstances under which individuals may be vulnerable to morbidity
and mortality hazards at later ages.
2.2 | Skeletal growth and maturation
Life history trade-offs may also be explored through skeletal growth
in surviving and non-surviving contingents of a sample 66,90 Some of
this work has focused on the Tirup cemetery in Denmark, dated
between 900 and 700 BP. Estimated stature of nonsurviving sub-
adults from Tirup cemetery, New World agriculturalists, and hunter-
gatherers were compared to living samples derived from the World
Health Organization and to adults from the respective samples.91,92
The remains represent individuals who lived in a small village during
this brief window of time. New World agricultural samples were
derived from the Irene Mound, Georgia Coast (900–400 BP), San Cris-
tobal, New Mexico (700–380 BP), and Chiribaya, Peru sites
(1,000–640 BP). The hunter-gatherer samples were derived from sites
affiliated with persistent landscape occupations in Siberia
(8,000–4,000 BP), Japan (3,000–2,300 BP), and Alaska (800–400 BP).
In all cases, nonsurviving subadults fell near or below the 5th percen-
tile for growth established by the World Health Organization, and in
the case of Tirup and the New World agricultural samples, height
reached an endpoint substantially below adult counterparts. In con-
trast, estimated height for the hunter-gatherer subadults reached an
end point that fell within the range of adult body size. These results
hint at the environmentally contingent nature of body size and sub-
adult survivorship: subadults who experienced growth disturbances
often do not survive this period, while in other cases individuals who
do not survive this period lack evidence for growth disturbances, and
this appears to be tethered to a subsistence economy.
Bioarchaeology may also be used to explore hypotheses related
to life history strategies and maturation. Where subadult mortality is
high, maturation is comparatively slow and age-at-first-reproduction
is later to allow for energetic investment in growth and mainte-
nance.55 Where subadult mortality is low and adult mortality is high,
maturation is comparatively fast as energetic investments in survival
and growth are diminished.55 Changes in these strategies are
observed across vertebrate populations when predators who increase
subadult or adult mortality are introduced.93 Earlier age-at-menarche
combined with earlier attainment of adult body size is found in con-
temporary hunter-gatherers with high adult mortality.94–96 Bioarch-
aeological research may explore these trade-offs with mortality
through the evaluation of earlier or later age of adult body size attain-
ment. Here, the ages where individuals reach adult height may be
associated with growth cessation and sexual maturity.
One such study explored the evolution of small body size in
hunter-gatherers from South Africa to understand whether this mor-
photype was attributable to an earlier achievement of adult body
size.97 Adult body size in the South African sample was achieved close
to age of sexual maturation in living populations with higher levels of
subadult mortality. The result did not fit the prediction that high adult
mortality in these samples drove earlier age at sexual maturation and
smaller body size. In prehistoric Japan, Late/Final (4000–2,300 BP)
Jomon period hunter-gatherers are smaller than subsequent wet-rice
farmers, despite similar rates of growth.98 Cubic regression lines fit to
Late/Final Jomon period subadult statures predict achievement of
adult stature around 16.0 years of age (Figure 2). This result is similar
to those reported in South Africa and suggests that early maturation
did not contribute to smaller size in the Jomon sample. Comparisons
of juvenile and adult mortality and growth rates in Yayoi period skele-
tal remains are required to more completely support this argument,
but the results hint at ways in which skeletal growth and maturation
may be used to further elucidate life history trade-offs in the past.
2.3 | Linear enamel hypoplasia
The relationship between LEH and mortality elucidates the complex
manifestations of physiological constraints in response to early life
stress events. Individuals with LEH have significantly lower average
38 TEMPLE
ages-at-death than those without LEH99,100 and more frequently
express other skeletal indicators of disease.101,102 Some of the best evi-
dence for this trend can be found in the deciduous teeth of American
Indians from Illinois, where infant and childhood survival is impaired in
association with defects that form in the prenatal and perinatal environ-
ment.103,104 Individuals with LEH were at greater risk of death from
infectious disease epidemics such as bubonic plague compared to indi-
viduals without LEH, although individuals with LEH from attritional
cemeteries had an even greater risk of death suggesting that wide-
spread mortality during epidemics may mask the expression of life his-
tory trade-offs.105 In another instance, individuals with LEH had an
increased mortality risk during medieval famine in London.106 LEH was
associated with decreased survivorship in prehistoric dental remains
from the Illinois Valley, and differences in survivorship between individ-
uals with LEH were found between time periods, with diminished sur-
vival found among samples dated to periods of environmental
deterioration.107 These findings suggest that early life stressors reduce
the capacity to survive future stress events, particularly during periods
of ecological catastrophe. That said, Amoroso and colleagues108 report
significant relationships between the presence of LEH and risk of death
in a sample of individuals of known occupation and age from 19th Cen-
tury Portugal. Interestingly, however, significance was reduced when
adding year of birth, socioeconomic status, and cause of death to the
regression model indicating that the physiological constraints associated
with surviving early life stress are environmentally and culturally
contingent—that is, long-term consequences of early life stress may be
muted by cultural buffering systems associated with individual identity.
Taken as a whole, the findings of these studies provide tantalizing evi-
dence for interactions between early life stress with cultural and eco-
logical contingencies, specifically those associated with environmental
deterioration, epidemic disease, famine, and socioeconomic inequality.
Many studies rely on LEH presence as an indicator of early life
stress. The critical predictions of life history models focus on the canali-
zation of energy budgets via physiological trade-offs due to stresses
experienced early in life. The presence of LEH is highly variable in terms
of age-at-defect formation as imbricational enamel forms between
approximately 1.1 and 6.2 years on anterior permanent teeth.109,110
Studies focused on LEH presence point out a relationship between
stress and susceptibility to mortality but do not provide evidence
regarding vulnerability of surviving stress during specific developmental
periods.68 Elevated risks of mortality when “strong” accentuated striae
of Retzius occurred before 7.0 years of age, but no risk when “weak”
accentuated striae of Retzius occurred during the same ages in a sample
from medieval Denmark.111 Interestingly, “strong” accentuated striae of
Retzius between ages 2.0 and 4.0 were not associated with a higher
mortality risk. In addition, Temple112 found that risk of death and future
growth disruptions were associated with the age-at-first-defect forma-
tion: individuals with comparatively earlier ages-at first-defect formation
had exacerbated mortality schedules and greater numbers of LEH. How-
ever, these findings were limited to a small sample of Late/Final Jomon
period hunter-gatherers from the Japanese archipelago. Wilson bands
are accentuated striae of Retzius produced when a broader than normal
band of ameloblasts cease enamel production. These lines were identi-
fied histologically in permanent molars and found to have a modal
occurrence around 5.0 months of age.113 Individuals with Wilson bands
had an earlier mean age at death than those without the lesion suggest-
ing that those who survived early life stress events were more suscepti-
ble to mortality. As a whole, the microstructural approach to LEH helps
further reveal details surrounding ages where stress events may produce
greater vulnerability to physiological constraints and thus adds impor-
tant contextual information to the study of surviving early life adversity
and the expression of physiological constraints at later ages (See Box 1).
2.4 | Crypt fenestration enamel defects
An emerging way to explore early life stress in human skeletal and dental
remains is localized hypoplasia of the primary canine, more recently
called crypt fenestration enamel defects (CFEDs). CFEDs are circular
hypoplastic enamel patches approximately 1–2 mm in diameter
(Figure 5). The lesion was originally attributed to stress experiences in
late fetal and perinatal infants, but later studies found no distinction
across socioeconomic boundaries and indicate more etiological research
is needed.114 Associations between tooth size and CFEDs suggest that
the lesion may be caused by alveolar crypt fenestration.115,116 Experi-
mental studies report that nutritional insufficiency produces osteopenia
in the alveolus and subsequent mastication induces trauma to the tooth
that disrupts amelogenesis.117 Comparing prevalence of these lesions is
common in bioarchaeological research and suggest that maternal stress
and dietary quality are implicated in the production of CFEDs.118,119
When compared to LEH, CFED presence is associated with earlier mor-
tality in samples of enslaved and free African Americans.120 Lukacs and
colleagues121 found relationships between CFED and growth stunting in
some but not all samples of subadults from rural and urban India. The
authors state that this inconsistent result was contextually driven: socio-
economic status, urban versus rural environments, and severity of stress
associated with the duration and chronology of these events. Increased
mortality risks were not found in infants and children with CFEDs from
the Eten and Mórrope sites in protohistoric Peru, although there were
differences in mortality associated CFED between sites.122 Individuals
without CFED from Eten had greater survivorship than those
FIGURE 2 Percentages of achieved growth for late/final Jomon
period hunter-gatherers. The line cubic line was fit to the data usingmethods of forward selection. The polynomial line of best fit suggestsan achievement of adult stature around 16 years of age, which isbelow the average age-at-first-birth for traditional populations
TEMPLE 39
BOX 1. Measuring life history using incremental microstructures of enamel
Anthropologists are piecing together individual life histories using incremental microstructures of enamel using measuring microscopes
(Figure 3). Striae of Retzius are time-dependent structures associated with lateral enamel formation and are associated with eight to
12 daily cross striations. The modal periodicity of striae of Retzius in human populations is 7–8 days.97,98 These structures along with
knowledge of cusp formation and crown initiation times provide anthropologists with a developmental clock of tooth formation. Impor-
tantly, striae of Retzius outcrop onto the labial surface of teeth as perikymata. Perikymata are important to the reconstruction of stress
using teeth because these structures have accentuated spacing following the production of linear enamel hypoplasia (LEH) (see Figure 1).
Anthropologists measure the spacing between perikymata and the depth of the enamel surface to identify LEH. Accentuated perikymata
area associated with LEH. Using known variables regarding cuspal enamel and crown initiation timing, it is possible to place LEH into a
detailed chronological context using these constants and the modal periodicity of perikymata in relation to the location of an LEH. This is
one way that stress experiences in the early life environment may be reconstructed using state-of-the-art methods. Figure 4 shows a
perikymata spacing and enamel surface profile of one adult male hunter-gatherer, who lived approximately 3,000 years ago in prehistoric
Japan. LEH were identified using z-scores of perikymata spacing and are indicated in the figure with arrows and letters. These LEH were
matched at the same developmental stage (within one tenth of a year) on other teeth. In this case, the earliest evidence for LEH appears
at approximately 1.2 years of age and the latest evidence for LEH appears at approximately 3.9 years of-age.
FIGURE 3 Engineer's measuring microscope in the author's former laboratory at University of North CarolinaWilmington. Themicroscope pro-
vides 5x, 10x, and 25x magnification of objects, and the vision gauge software program allows for measurements in the x, y, and z coordinates.
The z-coordinate is a depth measurement that is collected from the position of a digital stylus attached to the left side of the microscope (pic-
tured here) and provides a depiction of the enamel surface. This measurement is taken at beginning of each perikymata or about every 60 μm
movement along the labial surface of the tooth. The y-coordinate is measured between perikymata and provides a perikymata spacing profile
FIGURE 4 This image depicts an enamel surface profile from individual 194, an adult male from the Takasago site located in Hokkaido Japan.
The light bars are measurements of the enamel surface profile or depth collected from the z-coordinate measurements. The dark bars are the
perikymata spacing profile associated with the y-coordinate measurements. LEH are depicted with arrows and letters. Each LEH corresponds
to a depression in the enamel surface and accentuated perikymata spacing
40 TEMPLE
with and without CFED from Mórrope, while individuals with
CFED from Eten had greater survivorship than individuals with
the defect from Mórrope. Mórrope was an ecologically and cul-
turally isolated community and this led to a more pronounced
disease experience in response to European colonization.123
Greater survivorship in response to CFED formation in the Eten
compared to Mórrope sample suggests that mortality associated
with CFED may be driven by deeper contexts associated with
disease and mortality. CFEDs are a promising lesion for docu-
menting early life stress experiences. Future studies should com-
pare survivorship and CFED between epidemic and attritional
cemeteries to understand if surviving the experience early in life
elicits physiological constraints under known cultural and environ-
mental conditions.
2.5 | Stable isotopic approaches
Stable isotope analysis of the human dentition and skeleton provide
insight into early life stress and diet, particularly when isotope samples
are derived from tissues that form in incremental layers of bones
teeth.124 Sandberg et al.125 explored the relationship between LEH and
isotopically derived estimates of the cessation of breastfeeding. The
work found that the majority of LEH occur at the time leading up to
the cessation of breastfeeding suggesting that the process of physiolog-
ical and social separation contributes a greater level of stress than mal-
nutrition or infection following this event. Importantly, the work
demonstrates a consistent pattern of early age-at-breastfeeding-
cessation in survivors, while nonsurvivors consumed breast milk for a
greater period of time. This result does not suggest that cessation of
breastfeeding at earlier ages is optimal, but instead argues that the iso-
topic signal for extended breastfeeding fits into a socioecological con-
text where food shortages may have been offset by weaning practices.
These results have received some support. Later studies compared car-
bon and nitrogen values obtained from adult dentine and bone collagen
from post-weaning subadults and found a higher quality diet in the
early life of individuals who survived to adulthood.126 Stable isotope
analysis of diet in the early life environment is beginning to shed light
on how these contexts may produce challenges to survival and elicit
physiological constraints at later ages.
3 | THE FUTURE
Bioarchaeological explorations of DOHaD are best realized through
approaches to human life histories, specifically the exploration of adap-
tive plasticity and physiological constraint. Early life experiences are var-
ied and there are many contingencies acting to promote or reduce early
life stress experiences as well as the expression of physiological con-
straints. Many of these experiences revolve around socioeconomic
inequality, while others still reflect constraints promoted by the local
environment. Within this range of context, the psycho-social experience
of individuals requires consideration. For example, recent studies of LEH
confirm that psychological trauma at the earliest stages of development
may produce these lesions. In one instance, a gorilla with a documented
life history expresses a deep LEH that is histologically estimated to the
time of capture.127 In other instances, shortened DNA telomeres (end
sequences of DNA that promote cell division by acting as disposable
units during replication) are found in cases of war and social upheaval
suggesting that psycho-social experiences leave imprints on bodies that
have far reaching consequences across the human life cycle.8,128 Some-
times the psychological weight of surviving social hardship is enough
and elicits the production of lesions while impairing future survival.
Bioarchaeologists should pursue research questions that acknowledge
this complexity in the evaluation of early life adversity and include
psycho-social stressors as an important component of future research.
It is also possible for bioarchaeological research to contextualize
lives and lifestyles as deeply entangled or integrated events, with
intergenerational consequences.71 Gestational conditions as well as
environments experienced by earlier matrilines may alter DNA seg-
ments through placental interactions or direct inheritance30,32, and
these experiences discriminatorily kill people of color.129–131 Bioarch-
aeological research documents skeletal evidence for the embodied
consequences of colonization, dispossession, racism, and slavery in the
United States. 120,132–135 Furthermore, genetic studies aim to demon-
strate how stress may promote resilience when couched within the
context of individual agency.136 The incorporation of skeletal evidence
for early life stress and physiological constraint, documentation of the
intergenerational consequences, and analysis of survivorship would
augment the vast sociopolitical networks seeking to offset institutional
racism in the United States by legitimizing the trauma of these experi-
ences and demonstrating resilience through agency. This begins with
training a diverse group of scholars for future generations who will be
equipped to address these questions from an experiential and empirical
standpoint.137,138
Bioarchaeological research may also build on studies of infant/
maternal life history as embodied, integrated events139: it is a truism,
for example, that Late/Final Jomon people who experienced stress at
a comparatively early age express greater evidence for growth disrup-
tion and mortality.112 However, it is equally true that these individuals
experienced stress at ages where deeply embodied relationships
between maternal and infant organisms were formed, and these
events acted to disentangle the socially and physiologically embodied
FIGURE 5 Crypt fenestration enamel defect in the left mandibular
deciduous canine of a child from the Eten site, Lambayeque Valley,Peru. Photo courtesy of Haagen Klaus
TEMPLE 41
relationships between mother and offspring.140 This result emphasizes
the likelihood that physiological constraints may be more profoundly
expressed when disruptions between entwined bodies occur. In addi-
tion, studies of carbon and nitrogen isotopes derived from molar den-
tine and bone collagen track maternal diet in individuals who survive
and do not survive childhood.141 Reconstruction of maternal diet is
based on (a) findings that reveal bone collagen of fetal/neonatal indi-
viduals may actually be a record of maternal diet due to faster rates of
turnover in the fetus/infant and (b) early increments of dentine in
deciduous and permanent molars contain collagen formed in utero.
These are possible to compare to average female nitrogen values
derived from bone collagen to gain a sense of maternal diet in fetal or
perinatal individuals. Individuals surviving childhood had dentine nitro-
gen values within 1 standard deviation of the female mean, and those
failing to survive childhood recorded values well above or below this
mean combined with bone values that represent dramatic deviations
from fetal/perinatal nitrogen levels. These results demonstrate how
bioarchaeological research may be used to evaluate the transmission
of stressors across multiple generations. The context-laden approach
valued by bioarchaeologists should be incorporated into the develop-
ment of these methods and look squarely at the socioeconomic, cul-
tural, and ecological contingencies that produce and reproduce stress
experience and physiological constraints.
Finally, isotopic analysis of human dentine provides system-specific
signatures of early life stress events that are possible to time based on
the incremental nature of dentine formation.142 Isotopic analysis of bar-
ium relative to calcium may, for example, identify disruptions to growth
in body weight. In the same sample, heat shock protein HSP70 levels
were targeted. The expression of this protein helps reveal stress events
associated with oxidation, temperature increases, and heavy metal
exposure. Approximately 88% of the observed spikes in HSP70 coin-
cide with elemental signatures associated with accentuated lines. These
findings offer a promising way to uncover early life stress events using
an objective method that provides time-specific signatures of stress
from identifiable physiological systems.
4 | PENULTIMATE NOTE: SOCIAL AGENCY
One oft whispered critique of life history theory is that this approach
ignores the primacy of social agency [emphasis mine]. In bioarchaeology,
this critique is derived from the writings of Bourdieu143 and Foucalt144
that see the body as principally shaped by individual practices, beliefs,
and habits, which are attributes of social organization. Bourdieu143 liter-
ally sees bodies as endowed with habitus (dispositions attained through
practice), while Foucalt144 emphasizes the ways in which social institu-
tions shape bodies through control. Here, bodies express almost a limit-
less plasticity and are constantly shaped and reshaped by the
dispositions, habits, and perceptions of the individual and the system
which creates and reinforces these perceptions. This approach is impor-
tant for understanding the formation of skeletal diversity within social
and ecological systems but does not guide the capacity to explain the
cumulative results of these experiences when an individual is observed
in the context of death. In evaluating behavioral and biological variation,
Ingold145 notes that bodies are associated with the accumulation of
social and ecological interactions, a process of developmental learning.
This concept builds on earlier explorations of hunter-gatherers that
argue for the cumulative nature of ecologically and socially mediated
experiences in building perceptions, habits, and action.146 This life
course approach moves closer to life history theory by contextualizing
bodies within the aegis of cumulative experience. However, stopping at
this point is atemporal [sic] when applied to bioarchaeological contexts.
Bodies break, and bodies die. By focusing only on the factors that shape
the living body, bioarchaeological research ignores the crucial fact that
the locus of study is an individual at the time of death. It is, therefore,
incumbent on any scholar of social agency to understand the cumulative
experiences that facilitate the context for death, or at least acknowledge
that the biological body has limits and that these limits often manifest
through physiological constraints. Taken as a whole, this critique of life
history theory represents an unintentionally decontextualized view of
bioarchaeology—one that fails to see that bodily limits may be buffered
or exceeded based on social and ecological contingencies and that the
contextualized approach of bioarchaeological research has an integral
role in teasing apart these factors. More specifically, because bioarch-
aeology is the contextual study of human remains, bioarchaeological
research has the capacity to understand how social and ecological con-
texts interact with the body to accentuate or inhibit the physiological
constraints attached to surviving early life stress. Thus, instead of ignor-
ing the primacy of social agency, a contextualized bioarchaeological
approach to life history theory relies heavily on social and ecological
agencies as a mechanisms for explaining diversity in these strategies.
5 | CONCLUSIONS
DOHaD is a comprehensive paradigm that incorporates a lifespan
approach to health and well-being. This represents a novel approach
to understanding health in adults as a process rooted in early life
experience and one tethered to the cultural and economic contingen-
cies that produce and reproduce those experiences across the life-
span. Critical approaches to DOHaD argue that the reciprocal
relationships between early life environments and future life history
outcomes should be placed within evolutionary context, specifically
one that acknowledges the functional basis for these relationships
and physiological constraints imposed on adaptive evolution. Survival
of early life adversity invokes adaptive plasticity through the capacity
physiological reallocations of energy that emphasize short-term sur-
vival. In contrast, physiological constraint references the limited
capacity for energetic investment in competing processes following
survival of these events. This life history approach is particularly well-
suited to bioarchaeological research. Bioarchaeologists work with tis-
sues that reveal evidence for early life stress events and evidence for
chronic disease and death at later stages of the life cycle. The contex-
tual approach of bioarchaeology may also be leveraged so that the
ecologically and culturally contingent interplay between adaptive plas-
ticity and physiological constraint may be further revealed. As such,
bioarchaeologists are in a unique position to explore the contextual
expression of adaptive plasticity and physiological constraint as an
indispensable component of DOHaD. These works should continue to
emphasize vectors of inequality that perpetuate stress and mortality
42 TEMPLE
over multiple generations, while highlighting the essential role of oft
neglected individuals in building the human story.
Glossary
Angiotensinogen Peptide hormone that increases bloodpressure (hypertension) throughvasoconstriction and sodium retention bythe kidneys.
Adaptive plasticity The capacity to produce multiplephenotypes in response to environmentalconditions that increase organismalfitness. Put differently, phenotypicflexibility that moves the organismtoward an adaptive peak throughoptimization of function. Differentiatedfrom developmental plasticity byincreased fitness.
Crypt fenestrationenamel defect(CFED)
Deciduous defects of enamel that areproduced due to osteopenia in the earlydeveloping alveolus. Osteopenia exposesthe tooth to external pressures andtrauma. The result is a circular or notchshaped section of missing enamel(Figure 4).
Hidden heterogeneity Individuals experience myriad(heterogeneous) mortality risks over thelife course, and many of these risks maynot be observable (hidden) in humanskeletal remains.
Hypomethylation Loss of a methyl group from DNA that altersthe expression of an allele.
Metabolic syndrome Pathological condition associated withcentral obesity combined with any two ofthe following: elevated triglycerides,reduced high density lipoprotein, raisedfasting plasma glucose, and/orhypertension. The combination ofdisorders associated with metabolicsyndrome predisposes individuals to typeII diabetes and cardiovascular disease.
Methylation Addition of a methyl group to DNA thatmodifies the expression of an allele.
PEPCK alleles Mitochondrial enzymes involved in the earlystages of glycolysis. PEPCK enzymes arechief catalysts of gluconeogenesis, theprocess where cells synthesize glucosefrom substrates such as amino acids,glycerol, and lactase. Damage to PEPCKalleles may result in hypoglycemia byinhibiting this initial sequence ofglycolysis.
Perikymata Outcroppings of the Striae of Retzius thatare visible on the labial surface of thetooth. Perikymata follow the sameperiodicity as the Striae of Retzius. Thesestructures may, therefore, be reproducedusing high resolution silicone and resin toidentify the presence and timing of linearenamel hypoplasia.
Physiological constraint Limits on the capacity for natural selectionto optimize phenotypes due to the finitenature of energy availability. Naturalselection may, for example, favor largesized offspring at the expense of numberof offspring due to energetic limits on thecapacity to produce multiple largeoffspring under circumstances wheregreater body size provides a selectiveadvantage.
(Continues)
Selective mortality The process where disadvantagedindividuals die earlier than their peers.Disadvantages or frailty may be definedby comparing mortality risks betweendifferent groups of a sample.Bioarchaeologists often evaluate selectivemortality in terms of lesion presence,specifically to understand whetherindividuals with skeletal or dentalindicators of stress and disease had anincreased risk of mortality whencompared to individuals without theselesions.
Striae of Retzius Dark lines of enamel moving from thedentino-enamel junction to the surface ofthe tooth. These lines are often describedas forming over an approximately 7-dayperiodicity, although the humanperiodicity range is between 6 and12 days.
ACKNOWLEDGMENTS
The author would like to thank Sharon DeWitte and Jason Kamilar for
the invitation to contribute this article to Evolutionary Anthropology.
Original research by the author was funded by the National Science
Foundation (BCS 104490), Japan Society for the Promotion of Science
(07012), and Wenner Gren Foundation for Anthropological Research
(07135). Access to the Late/Final Jomon period collections featured in
this article was permitted by M. Nakatsukasa, H. Matsumura, G. Suwa,
Y. Kaifu, and R. Kono. Comments from Haagen Klaus, Laurie Reitsema,
Jane Buikstra, and Jaclyn Thomas were helpful in developing the ideas
expressed in this article. The editor, associate editor, and three anony-
mous reviewers provided comments that significantly improved this
manuscript.
CONFLICT OF INTEREST
The author declares no conflict of interest.
ORCID
Daniel H. Temple https://orcid.org/0000-0003-4582-3978
REFERENCES
[1] Banning C. 1946. Food shortage and public health, first half of 1945.
Ann Am Acad Pol Soc Sci 245:93–110.[2] Kimura K, Kitano S. 1959. Growth of the Japanese physiques in four
successive decades after world war II. J Anthropol Soc Nippon 67:
37–46.[3] Riesenfield AC. 1973. The effect of starvation and extreme tempera-
tures on the body proportions of the rat. Am J Phys Anthropol 39:
427–459.[4] Forsdahl A. 1977. Are poor living conditions in childhood and ado-
lescence an important risk factor for arteriosclerotic heart disease?
Br J Prev Med 31:91–95.[5] Boas F. 1930. Observations on the growth of children. Science 72:
44–48.[6] Seyle H. 1936. A syndrome produced by general nocuous agents.
Nature 138:32.
TEMPLE 43
[7] Painter RC, Osmond C, Gluckman P, et al. 2008. Transgenerationaleffects of prenatal exposure to the Dutch famine on neonatal adi-posity and health in later life. BJOG 115:1243–1249.
[8] Rodney NC, Mulligan CJ. 2014. A biocultural study of the effects ofmaternal stress on mother and newborn health in the DemocraticRepublic of Congo. Am J Phys Anthropol 155:200–209.
[9] Thayer Z, Barbosa-Leiker C, McDonell M, et al. 2017. Early lifetrauma, post-traumatic stress disorder, and allostatic load in a sam-ple of American Indian adults. Am J Hum Biol 29:e22943.
[10] Eriksson M, Raikkonen K, Eriksson JG. 2014. Early life stress andlater health outcomes—Findings from the Helsinki birth cohortstudy. Am J Hum Biol 26:111–116.
[11] Barker DJP, Osmond C. 1986. Infant mortality, childhood, nutrition,and ischaemic heart disease in England and Wales. Lancet 8489:1077–1081.
[12] Barker DJP, Osmond C, Law CM. 1989. The intrauterine and earlypostnatal origins of cardiovascular disease and chronic bronchitis.J Epidemiol Commun Health 259-262(43):237–240.
[13] Barker DJ, Bull AR, Osmond C, et al. 1990. Fetal and placental sizeand risk of hypertension in adult life. Brit Med J 6746:259–262.
[14] Barker DJ. 1992. Fetal and infant origins of adult disease, London:Tavistock.
[15] Hales CN, Barker DJP. 2001. The thrifty phenotype hypothesis. BrMed Bull 60:5–20.
[16] Barker DJP. 1990. The fetal origins of adult health and disease: Thewomb may be more important than the home. Brit Med J 301:111.
[17] Almond D, Currie J. 2011. Killing me softly: The fetal origins hypoth-esis. J Econ Perspect 25:153–172.
[18] Ravelli AC, Van der Meulen JHP, Michels RPJ, et al. 1998. Glucosetolerance in adults after prenatal exposure to famine. Lancet 351:173–177.
[19] Stanner SA, Bulmer K, Andrés C, et al. 1997. Does malnutrition inutero determine diabetes and coronary heart disease in adulthood?Results from the Leningrad siege study, a cross-sectional study.BMJ 315:1342–1348.
[20] Ellison PT, Jasienska G. 2007. Constraint, adaptation, and pathology:How do we tell them apart? Am J Hum Biol 19:622–630.
[21] Forrester TE, Badaloo AV, Boyne MS, et al. 2012. Prenatal factorscontribute to emergence of kwashiorkor or maramsmus in responseto severe undernutrition: Evidence for the predictive adaptationmodel. PLoS One 7:e35907.
[22] Gluckman PD, Buklijas T, Hanson MA. 2016. The developmental ori-gins of health and disease (DOHaD) concept: Past, present, andfuture. In: Rosenfield CS, editor. The epigenome and developmentalorigins of health and disease, New York, NY: Elsevier. p 1–15.
[23] Gillman MW, Barker D, Bier D, et al. 2007. Meeting report on the3rd international congress on developmental origins of health anddisease (DOHaD). Ped Res 61:625–629.
[24] Gillman MW. 2005. The developmental origins of health and dis-ease. N Engl J Med 353:1848–1850.
[25] Bateson P. 2001. Fetal experience and good adult design. Int J Epi-demiol 30:928–934.
[26] Bateson P, Barker D, Clutton-Brock T, et al. 2004. Developmentalplasticity and human health. Nature 430:419–421.
[27] Gluckman PD, Hanson MA, Morton SMB, et al. 2005. Life-longechoes—A critical analysis of the developmental origins of adult dis-ease model. Biol Neonate 87:127–139.
[28] Gluckman PD, Hanson MA, Spencer HG. 2005. Predictive adaptiveresponses and human evolution. Trends Ecol Evol 20:527–533.
[29] Gluckman PD, Hanson MA, Beedle AS. 2007. Early life events andtheir consequences for later disease: A life history and evolutionaryperspective. Am J Hum Biol 19:1–19.
[30] Kuzawa CW. 2005. Fetal origins of developmental plasticity: Arefetal cues reliable predictors of future nutritional environments?Am J Hum Biol 17:5–21.
[31] Wells JCK. 2007. Flaws in the theory of predictive adaptiveresponses. Trends Ecol Metabol 18:331–337.
[32] Wells JCK. 2011. The thrifty phenotype: An adaptation in growth ormetabolism? Am J Hum Biol 23:65–76.
[33] Worthman CM, Kuzara J. 2005. Life history and the early origins ofhealth differentials. Am J Hum Biol 17:95–112.
[34] Stearns SC. 1992. The evolution of life histories, Oxford: Oxford
University Press.[35] Levins R. 1968. Evolution in changing environments, Princeton:
Princeton University Press.[36] Sibly RM, Calow P. 1989. A life cycle theory for responses to stress.
Biol J Linn Soc 37:101–116.[37] Sapolsky RM. 1998. Why zebras Don't get ulcers: An updated guide
to stress, stress related diseases, and coping, New York, NY: W.F.
Freeman.[38] Chyun YS, Kream BE, Raisz LG. 1984. Cortisol decreases bone for-
mation by inhibiting periosteal cell proliferation. Endocrinology 114:
477–480.[39] Martinelli CE Jr, Moreira AC. 1994. Relation between growth hor-
mone and cortisol spontaneous secretion in children. Clin Endocrinol
41:117–121.[40] Macrae VE, Ahmed SF, Mushtaq T, et al. 2007. IGF-I signalling in
bone growth: Inhibitory actions of dexamethasone and IL-1beta.
Growth Horm IGF Res 17:435–439.[41] Fernandez-Cancio M, Esteban C, Carrascosa A, et al. 2008. IGF-I
and not IGF-II expression is regulated by glucocorticoids in human
fetal epiphyseal chondrocytes. Growth Horm IGF Res 18:497–505.[42] Rees L, Greene SA, Adlard P, et al. 1988. Growth and endocrine function
in steroid sensitive nephrotic syndrome. ArchDis Child 63:484–490.[43] Seeman E. 2001. Clinical review 137: Sexual dimorphism in skeletal
size, density and strength. J Clin Endocrinol Metab 86:4576–4584.[44] Kreshover SJ. 1960. Metabolic disturbances in tooth formation. Ann
NY Acad Sci 85:161–167.[45] Sasaki T, Garant PR. 1987. Mitochondrial migration and CA-ATPase
modulation in secretory ameloblasts of fasted calcium-loaded rats.
Am J Anat 179:116–130.[46] Joseph BK, Savage NW, Young WG, et al. 1994. Insulin-like growth
factor-I receptor in the cell biology of the ameloblast: An immuno-
histochemical study on the rat incisor. Epithelial Cell Biol 3:47–53.[47] Sasaki T, Takagi M, Yanagisawa T. 1997. Structure and function of
ameloblasts in enamel formation. Ciba Found Sympos 205:32–46.[48] Yamamoto T, Oida S, Inage T. 2006. Gene expression and localiza-
tion of insulin-like growth factors and their receptors throughout
amelogenesis in rat incisors. J Histochem Cytochem 54:243–252.[49] McDade TW. 2003. Life history and the immune system: Steps toward
a human ecological immunology. Yrbk Phys Anthropol 46:100–125.[50] Ghalambor CK, McKay JK, Carroll SP, et al. 2007. Adaptive versus
non-adaptive phenotypic plasticity and the potential for contempo-
rary adaptation in new environments. Funct Ecol 21:394–407.[51] Seyle H. 1971. Hormones and resistance, New York, NY: Springer-
Verlag.[52] McEwan BS, Stellar E. 1993. Stress and the individual mechanisms
leading to disease. Arch Intern Med 153:2093–2101.[53] McEwan BS. 1998. Stress, adaptation, and disease: Allostasis and
allostatic load. Ann NY Acad Sci 840:33–44.[54] DeWitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic
plasticity. Trends Ecol Evol 13:77–81.[55] Charnov EL. 1993. Life history invariants: Some explorations of
symmetry in evolutionary ecology, Oxford, UK: Oxford University
Press.[56] Futuyma DJ. 1998. Evolutionary Biology. , Sunderland: Sinauer and
Associates.[57] Sultan SE. 2003. Phenotypic plasticity in plants: A case study in eco-
logical development. Evol Dev 5:25–33.[58] Suryan RM, Saba VS, Wallace BP, et al. 2009. Environmental forcing
on life history strategies: Evidence for multi-trophic level responses
on ocean basin scales. Prog Oceangr 81:214–222.[59] Denver RJ, Mirhadi N, Phillips M. 1998. Adaptive plasticity in
amphibian metamorphosis: Response of Scaphius hammondii tad-
poles to habitat dessication. Ecology 79:1859–1872.[60] Crespi EJ, Denver RJ. 2005. Ancient origins of human developmen-
tal plasticity. Am J Hum Biol 17:44–54.[61] Thayer ZM, Wilson MA, Kim AW, et al. 2018. Impact of prenatal
stress on offspring glucocorticoid levels: A phylogenetic meta-
analysis across 14 vertebrate species. Nature Sci Rep 8:4942.
44 TEMPLE
[62] Buikstra JE. 1977. Biocultural dimensions of archaeological study: Aregional perspective. In: Blakely RL, editor. Biocultural adaptation inprehistoric America, Athens: University of Georgia Press. p 67–84.
[63] Armelagos GJ. 2003. Bioarchaeology as anthropology. ArchaeolPapers Am Anthropol Assoc 13:27–41.
[64] Larsen CS. 2015. Bioarchaeology: Interpreting behavior from thehuman skeleton, 2nd ed. Cambridge, UK: Cambridge UniversityPress.
[65] Ortner DJ. 1991. Theoretical and methodological issues in paleopa-thology. In: Ortner DJ, Aufderheide AC, editors. Paleopathology:Current synthesis and future options, Washington: SmithsonianInstitution Press. p 5–11.
[66] Wood JW, Milner GR, Harpending HC, et al. 1992. The osteologicalparadox: Problems of inferring health from skeletal samples. CurrAnthropol 33:343–370.
[67] DeWitte SN, Stojanowski CM. 2015. The osteological paradox20 years later: Past perspectives and future directions. J ArchaeolRes 23:397–450.
[68] Armelagos GJ, Goodman AH, Harper KN, et al. 2009. Enamel hypo-plasia and early mortality: Bioarchaeological support for the barkerhypothesis. Evol Anthropol 18:261–271.
[69] Temple DH, Goodman AH. 2014. Bioarchaeology has a “health”problem: Conceptualizing “stress” and “health” in bioarchaeologicalresearch. Am J Phys Anthropol 151:186–191.
[70] Klaus HD. 2014. Frontiers in the bioarchaeology of stress and dis-ease: Cross-discplinary perspectives from pathophysiology, humanbiology, and epidemiology. Am J Phys Anthropol 155:294–308.
[71] Gowland RL. 2015. Entangled lives: Implications of the developmen-tal origins of health and disease hypothesis for bioarchaeology andthe life course. Am J Phys Anthropol 158:530–540.
[72] Agarwal SC. 2016. Bone morphologies and life history. Yrbk PhysAnthropol 61:130–149.
[73] Malinovskaya NA, Morgun AV, Lopatina OL, et al. 2018. Early lifestress: Consequences for the development of the brain. NeurosciBehav Physiol 48:233–250.
[74] Goodman AH, Rose JC. 1990. Assessment of systemic physiologicalperturbations from dental enamel hypoplasias and associated histo-logical structures. Yrbk Phys Anthropol 33:59–110.
[75] Goodman AH, Rose JC. 1991. Dental enamel hypoplasias as indica-tors of nutritional status. In: Kelley MA, Larsen CS, editors.Advances in dental anthropology, New York, NY: Wiley-Liss. p279–293.
[76] Hillson SW. 2014. Tooth development in human evolution andbioarchaeology, Cambridge: Cambridge University Press.
[77] Hillson S, Bond J. 1997. The relationship of enamel hypoplasia totooth crown growth: A discussion. Am J Phys Anthropol 104:89–103.
[78] Hochberg Z. 2012. Evo-Devo of child growth. New Jersey, Hoboken:Wiley-Blackwell.
[79] Newman SL, Gowland RL. 2015. The use of non-adult vertebraldimensions as indicators of growth disruption and non-specific healthstress in skeletal populations. Am J Phys Anthropol 158:155–164.
[80] Clark GA, Hall NR, Armelagos GJ, et al. 1986. Poor early growthprior to childhood: Decreased health and life-span in the adult.Am J Phys Anthropol 70:145160.
[81] Littleton J. 2005. Invisible impacts but long-term consequences:Hypoplasia and contact in Central Australia. Am J Phys Anthropol126:295–304.
[82] Macho GA, Leakey MG, Williamson DK, et al. 2003. Paleoenviron-mental reconstruction: Evidence for seasonality at Allia bay, Kenya,at 3.9 million years. Paleogeogr Paleogeol Paleoclimatol 199:17–30.
[83] Stock JT, Migliano AB. 2009. Stature, mortality, and life historyamong the indigenous populations of the Andaman Islands,1871-1986. Curr Anthropol 50:713–725.
[84] DeWitte SN, Hughes-Morey G. 2012. Stature and frailty during theblack death: The effect of stature on risks of epidemic mortality.J Archaeol Sci 39:1412–1419.
[85] Hughes-Morey G. 2016. Interpreting stature in industrial London.Am J Phys Anthropol 159:126–134.
[86] Watts R. 2015. The long term impact of developmental stress. Evi-dence from late medieval and post-medieval London(AD 1117-1853). Am J Phys Anthropol 158:569–580.
[87] Weisensee KE. 2013. Assessing the relationship between fluctuat-ing asymmetry and cause of death in skeletal remains: A test of thedevelopmental origins of health and disease hypothesis. Am J HumBiol 25:411–417.
[88] Floyd B, Littleton J. 2006. Linear enamel hypoplasia and growth inan Australian aboriginal community: Not so small, but not so healthyeither. Ann Hum Biol 33:424–443.
[89] Temple DH. 2008. What can stature variation reveal about environ-mental differences between prehistoric Jomon foragers? Under-standing the impact of systemic stress on developmental stability.Am J Hum Biol 20:431–439.
[90] Saunders SR, Hoppa RD. 1994. Growth deficit in survivors and non-survivors: Biological and mortality bias in subadult skeletal samples.Yrbk Phys Anthropol 36:127–151.
[91] Usher B. 2016. Short bones, short life. Subadult selective mortalityat Tirup. Am J Phys Anthropol S62:320.
[92] Violaris C, Usher B, Temple DH. 2018. Do the short die young? Acomparative study of agricultural and hunter-gatherer children'sgrowth patterns. Am J Phys Anthropol S64:289.
[93] Reznick D, Byrga H, Endler JE. 1990. Experimentally induced life-history evolution in a natural population. Nature 346:357–359.
[94] Migliano AB. 2005. Why are pygmies small? Ontogenetic implica-tions of life history evolution. Ph.D. dissertation, CambridgeUniversity.
[95] Migliano AB, Vinicius L, Lahr MM. 2007. Life-history trade-offsexplain the evolution of human pygmies. Proc Natl Acad Sci 104:20216–20219.
[96] Walker RS, Hamilton MJ. 2008. Life history consequences of den-sity dependence and the evolution of human body size. CurrAnthropol 49:115–122.
[97] Pfeiffer S, Harrington L. 2011. Bioarchaeological evidence for thebasis of small adult stature in southern Africa. Curr Anthropol 52:449–461.
[98] Okazaki K. 2004. A morphological study on the growth patterns ofancient people in the northern Kyushu-Yamaguchi region, Japan.Anthropol Sci 112:219–234.
[99] Goodman AH, Armelagos GJ. 1988. Childhood stress and decreasedlongevity in prehistoric populations. Am Anthropol 90:936–944.
[100] Goodman AH. 1996. Early life stresses and adult health: Insightsfrom dental enamel development. In: Henry CJK, Ulijaszek SJ, edi-tors. Long-term consequences of early environment: Growth, devel-opment, and the lifespan developmental perspective, New York,NY: Cambridge University Press. p 163–182.
[101] Stodder ALW. 1997. Subadult stress, morbidity, and longevity inlatte period populations on Guam, Mariana Islands. Am J PhysAnthropol 104:363–380.
[102] Sciulli PW, Oberly J. 2002. Native Americans in eastern NorthAmerica: The southern Great Lakes and upper Ohio Valley. In:Steckel RH, Rose JC, editors. The backbone of history: Health andnutrition in the Western hemisphere, Cambridge, UK: CambridgeUniversity Press. p 440–480.
[103] Cook DC, Buikstra JE. 1979. Health and survival in prehistoricpopulations: Prenatal defects. Am J Phys Anthropol 51:649–664.
[104] Blakey ML, Armelagos GJ. 1985. Deciduous defects in prehistoricAmericans from Dickson mounds: Prenatal and postnatal stress.Am J Phys Anthropol 66:371–380.
[105] DeWitte SN, Wood JW. 2008. Selectivity of black death mortalitywith respect to pre-existing health. Proc Natl Acad Sci 105:1436–1441.
[106] Yaussy SL, DeWitte SN, Redfern RC. 2016. Frailty and famine: Pat-terns of mortality and physiological stress among victims of faminein medieval London. Am J Phys Anthropol 160:272–283.
[107] Wilson JJ. 2014. Paradox and promise: Research on the role ofrecent advances in paleodemography and paleoepidemiology to thestudy of “health” in pre-Columbian societies. Am J Phys Anthropol155:268–280.
[108] Amoroso A, Garcia SJ, Cardoso HFV. 2014. Age at death and linearenamel hypoplasias: Testing the effects of childhood stress andadult socioeconomic circumstances in premature mortality.Am J Hum Biol 26:461–468.
TEMPLE 45
[109] Reid DJ, Dean MC. 2006. Variation in modern human enamel for-mation times. J Hum Evol 50:329–346.
[110] Reid DJ, Beynon AD, Ramirez Rozzi F. 1998. Histological recon-struction of dental development in four individuals from a medievalsite in Picardie, France. J Hum Evol 35:463–479.
[111] Thomas RF. 2003. Enamel defects, well-being, and mortality in amedieval Danish village. Ph.D. dissertation, Pennsylvania State Uni-versity, University Park, Pennsylvania.
[112] Temple DH. 2014. Plasticity and constraint in response to early-lifestressors among late/final Jomon period foragers from Japan: Evi-dence for life history trade-offs from incremental microstructures ofenamel. Am J Phys Anthropol 155:537–545.
[113] Garland CJ, Turner BL, Klaus HD. 2016. Biocultural consequencesof Spanish contact in Lambayeque Valley region of northern Peru:Internal enamel micro-defects as indicators of early life stress. Int JOsteoarchaeol 26:947–958.
[114] Lukacs JR. 1991. Localized enamel hypoplasia of the deciduouscanine teeth in rural Pakistan. Hum Biol 63:513–522.
[115] Skinner MF, Newell EA. 2003. Localised hypoplasia of the primarycanine in bonobos, orangutans and gorillas. Am J Phys Anthropol120:61–72.
[116] Lukacs JR. 2009. Markers of stress in juvenile bonobos (Pan panis-cus): Are enamel hypoplasia, skeletal development, and tooth sizeinterrelated? Am J Phys Anthropol 110:351–363.
[117] Skinner MF, Rodrigues AT, Byra C. 2014. Developing a pig modelfor crypt fenestration-induced localized hypoplastic defects inhumans. Am J Phys Anthropol 154:239–250.
[118] Halcrow SE, Tayles N. 2008. Stress near the start of life? Localisedhypoplasia of the primary canine in late prehistoric mainland South-east Asia. J Archaeol Sci 35:2215–2222.
[119] Stojanowski CM, Carver MJ. 2011. Influence of emergent cattlepastoralism in the southern Sahara desert based on localized hypo-plasia of the primary canine. Int J Paleopathol 1:89–97.
[120] Blakey ML, Leslie TE, Reidy JP. 1994. Frequency and chronologicaldistribution of dental enamel hypoplasia in enslaved African Ameri-cans: A test of the weaning hypothesis. Am J Phys Anthropol 95:371–383.
[121] Lukacs JR, Walimbe SR, Floyd B. 2001. Epidemiology of enamelhypoplasia in deciduous teeth: Explaining variation in prevalence inwestern India. Am J Hum Biol 13:788–807.
[122] Thomas JA, Temple DH, Klaus HD. In review. Perinatal stress andsurvivorship in protohistoric Peru: Evidence for contingencies ininfant and child life histories. Am J Phys Anthropol. .
[123] Klaus HD, Alvarez-Calderon R. 2017. Escaping conquest? A first lookat regional cultural and biological variation in postcontact Eten, Peru.In: Murphy MS, Klaus HD, editors. Colonized bodies, worlds trans-formed: toward a global bioarchaeology of contact and colonialism.Gainesville, FL: University Press of Florida. p 95–128.
[124] King CL, Millard AR, Gröcke DR, et al. 2018. A comparison of usingbulk and incremental isotopic analyses to establish weaning prac-tices in the past. STAR: Sci, Technol, Archaeol Res 3:126–134.https://doi.org/10.1080/20548923.2018.1443548.
[125] Sandberg PA, Sponheimer M, Lee-Thorp J, et al. 2014. Intra-toothstable isotope analysis of dentine: A step towards addressing selec-tive mortality in the reconstruction of life history in the archaeologi-cal record. Am J Phys Anthropol 155:281–293.
[126] Reitsema L, Vercellotti V, Boano R. 2016. Subadult dietary variationat medieval Trino Vercellese, Italy and its relationship to adult dietand mortality. Am J Phys Anthropol 160:653–664.
[127] McGrath K, El-Zaatari S, Guatelli-Steinberg D, et al. 2018. Quantify-ing linear enamel hypoplasia in Virunga mountain gorillas and othergreat apes. Am J Phys Anthropol. 166:337–352.
[128] Unternaehrer E, Luers P, Dempster E, et al. 2012. Dynamic changesin DNA methylation of stress associated genes (OXTR, BDNF) afteracute psychosocial stress. Transl Psych 2:e150.
[129] Barcelona de Mendoza V, Huang Y, Crusto C, et al. 2017. Perceivedracial discrimination and DNA methylation among African Americanwomen in the InterGEN study. Biol Res Nurs 20:1–8.
[130] Kuzawa CW, Sweet E. 2009. Epigenetics and the embodiment ofrace: Developmental origins of US racial disparities in cardiovascularhealth. Am J Hum Biol 21:2–15.
[131] Benyshek DC, Martin JF, Johnston CF. 2001. A reconsideration of theorigins of the type 2 diabetes epidemic among native Americans andthe implications for intervention policy.Med Anthropol 20:25–64.
[132] Rankin-Hill L. 1997. A biohistory of 19th century afro-Americans: Theburial remains of a Philadelphia cemetery,Westport: Berin andGarvey.
[133] de la Cova C. 2011. Race, health, and disease in 19th century bornmales. Am J Phys Anthropol 144:526–537.
[134] de la Cova C. 2014. The biological effects of urbanization and in-migration on 19th-century-born African Americans and EuropeanAmericans of low socioeconomic status: An anthropological and his-torical approach. In: Zuckermann MK, editor. Are modern environ-ments bad for health? Revisiting the second epidemiologicaltransition, New York, NY: Wiley Blackwell. p 243–264.
[135] Larsen CS, Milner GR. 1994. In the wake of contact: Biologicalresponses to conquest, New York, NY: Wiley.
[136] Jackson FLC. 2016. Resilience through research and publication.Backbone 2:1–2.
[137] Jackson FLC, Cross C. 2015. Applying next generation researchstandards in the cobb research laboratory. Backbone 1:1–3.
[138] Gomez M. 2015. Using the contents of the cobb research laboratoryto understand today's health disparities. Backbone 1:1–3.
[139] Halcrow SE, Gowland RS. in press. The mother-infant nexus in anthro-pology: Small beginnings, significant outcomes, NewYork, NY: Springer.
[140] Temple DH. In review. The maternal-infant nexus revealed by linearenamel hypoplasia: Chronological and contextual evaluation ofdevelopmental stress using incremental microstructures of enamelin late/final Jomon period hunter-gatherers. In: Halcrow S,Gowland R, editors. The mother-infant nexus in anthropology: Smallbeginnings, significant outcomes, New York, NY: Springer.
[141] Beaumont J, Montgomery J, Buckberry J, Jay M. 2015. Infant mor-tality and isotopic complexity: New approaches to stress, maternalhealth, and weaning. Am J Phys Anthropol 157:441–457.
[142] Austin C, Smith TM, Farhani RMZ, et al. 2016. Uncovering system-specific stress signatures in primate teeth with multimodal imaging.Nature Sci Rep 6:18802.
[143] Bourdieu P. 1971. Outline of a theory of practice, Cambridge: Cam-bridge University Press.
[144] Foucalt M. 1975. Discipline and punish: The birth of the prison,New York, NY: Pantheon Books.
[145] Ingold T. 1998. The perception of the environment: Essays on liveli-hood, dwelling, and skill, London: Routledge.
[146] Laughlin WS. 1968. Hunting: An integrating biobehavioral systemand its evolutionary importance. In: Lee RB, DeVore I, editors. Manthe hunter, Chicago: Aldine Publishing Company. p 304–320.
AUTHOR BIOGRAPHY
DANIEL H. TEMPLE is an associate professor in the Department of Soci-
ology and Anthropology at George Mason University. His primary
research interests include skeletal and dental biology, developmental
stress, life history evolution, evolutionary morphology, ontology and
memory, resilience and adaptation, and hunter-gatherer mortuary
practices. He is currently investigating individual life histories, socioe-
cological and cultural resilience, and construction of persistent places
in hunter-gatherers from Northeast Asia, North America, and Eurasia.
His research has been funded by the Wenner Gren Foundation,
National Geographic Society, National Science Foundation, Japan
Society for the Promotion of Science, and Social Sciences and Human-
ities Research Council of Canada.
How to cite this article: Temple DH. Bioarchaeological evi-
dence for adaptive plasticity and constraint: Exploring life-
history trade-offs in the human past. Evol Anthropol. 2019;28:
34–46. https://doi.org/10.1002/evan.21754
46 TEMPLE