2 The Study of Human Adaptation

A. Roberto Frisancho

INTRODUCTION systems of organs, to entire organisms. For example, the

lungs provide oxygen to the extracellular fluid to conti-
Ever since hominids left Africa, they have expanded nually replenish the oxygen that is being used by the cells,
throughout the world and have adapted to diverse the kidneys maintain constant ion concentrations, and
environments, and acquired specific biological and the gastrointestinal system provides nutrients.
cultural traits that have enabled them to survive in a Humans living in hot or cold climates must undergo
given area. The conceptual framework of research in additional functional adjustments to maintain thermal
biological anthropology is that evolutionary selection balance; these may comprise adjustments to the rate
processes have produced the human species and that of metabolism, avenues of heat loss, heat conservation,
these processes have produced a set of genetic charac- respiration, blood circulation, fluid and electrolyte
teristics, which adapted our evolving species to their transport, and exchange. In the same manner, persons
environment. Current investigations have demonstrated exposed to high altitudes must adjust through physio-
that the phenotype measured morphologically, physio- logical, chemical, and morphological mechanisms, such
logically, or biochemically is the product of genetic as increase in ventilation, increase in the oxygen-carrying
plasticity operating during development. Within this capacity of the blood resulting from an increased concen-
framework, it is assumed that some of the biological tration of red blood cells, and increased ability of
adjustments or adaptations people made to their natural tissues to utilize oxygen at low pressures. Failure to
and social environments have also modified how they activate the functional adaptive processes may result in
adjusted to subsequent environments. The adjustments failure to restore homeostasis; which in turn results in
we have made to improve our adaptations to a given the maladaptation of the organism and eventual incap-
environment have produced a new environment to acitation of the individual. Therefore homeostasis is a
which we, in turn, adapt in an ongoing process of new part and function of survival. The continued existence
stress and new adaptation. of a biological system implies that the system possesses
mechanisms that enable it to maintain its identity,
despite the endless pressures of environmental stresses
HOMEOSTASIS AND ENVIRONMENTAL (Proser, 1964). The complementary concepts of homeo-
STRESS stasis and adaptation are valid at all levels of biological
organization; they apply to social groups as well as to
Central to the study of adaptation is the concept of unicellular or multicellular organisms (Proser, 1964).
homeostasis and environmental stress. Environmental Homeostasis is a function of a dynamic interaction
stress is defined as any condition that disturbs the normal of feedback mechanisms whereby a given stimulus
functioning of the organism. Such interference eventu- elicits a response aimed at restoring the original equi-
ally causes a disturbance of internal homeostasis. librium. Several mathematical models of homeostasis
Homeostasis means the ability of the organism to main- have been proposed. In general, they show (as schema-
tain a stable internal environment despite diverse, disrup- tized in Figure 2.1) that when a primary stress disturbs
tive, external environmental influence (Proser, 1964). the homeostasis that exists between the organism and
On a functional level, all adaptive responses of the the environment the organism must resort either
organism or the individual are made to restore internal to biological or cultural-technological responses in
homeostasis. These controls operate in a hierarchy at order to function normally. For example, when faced
all levels of biological organization, from a single with heat stress, the organism may simply reduce its
biochemical pathway, to the mitochondria of a cell, to metabolic activity so all heat-producing processes
cells organized into tissues, tissues into organs and are slowed down, or may increase the activity of the

Human Evolutionary Biology, ed. Michael P. Muehlenbein. Published by Cambridge University Press. # Cambridge University Press 2010.

17
 18 A. Roberto Frisancho

Lifetime:
habituation
Primary acclimation
stress acclimatization
Biological
responses Restores
Disturbs homeostasis
homeostasis Growth: between
between developmental organism
organism acclimatization and
and environment
environment Cultural– Decrease
technological environmental
responses stress

2.1. Schematization of adaptation process and mechanisms that enable individual or population
to maintain homeostasis in the face of primary environmental disturbing stress. From Frisancho (1993).

heat-loss mechanisms. In either case, the organism processes that enable them to function and to be adapted
may maintain homeostasis, but the physiological to their environment.
processes will occur at a different set point. The attain- Not all responses made by the organism can be
ment of full homeostasis or full functional adaptation, considered adaptive. Although a given response might
depending on the nature of the stress, may require not be adaptive per se, through its effect on another
short-term responses, such as those acquired during structure or function it may prove beneficial to the
acclimation or acclimatization, or may require expos- organism’s function. Conversely, a given adaptive
ure during the period of growth and development as in response may aid the organism in one function, but
developmental acclimatization. actually have negative effects on other functions or
In theory, the respective contributions of genetic and structures. Thus, within all areas of human endeavor
environmental factors vary with the developmental stage a given trait is considered adaptive when its beneficial
of the organism–the earlier the stage, the greater the effects outweigh the negative ones. In theory, this is a
influence of the environment and the greater the valid assumption, but in practice, due to the relative
plasticity of the organism (Proser, 1964; Timiras, 1972; nature of adaptation, it is quite difficult to determine
Frisancho, 1975, 1993). However, as will be shown, the the true adaptive value of a given response. Every
principle does not apply to all biological parameters; response must be considered in the context of the
it depends on the nature of the stress, the developmental environmental conditions in which the response was
stage of the organism, the type of organism, and the measured and within the perspective of the length of
particular functional process that is affected. For time of the study and the subject population.
example, an adult individual exposed to high-altitude
hypoxia through prolonged residence may attain a level
of adaptation that permits normal functioning in all ADAPTIVE PROCESSES
daily activities and as such we may consider him
adapted. However, when exposed to stress that requires The term adaptation is used in the broad generic sense
increased energy, such as strenuous exercise, this of functional adaptation, and it is applied to all levels of
individual may not prove to be fully adapted. On the other biological organization from individuals to populations.
hand, through cultural and technological adaptation, A basic premise of this approach is that adaptation is a
humans may actually modify and thus decrease the process whereby the organism has attained a beneficial
nature of the environmental stresses so that a new adjustment to the environment (Mayr, 1963; Lewontin,
microenvironment is created to which the organism 1957; Proser, 1964; Dubos, 1965; Baker, 1966; Lasker,
does not need to make any physiological responses. 1969; Mazess, 1973; Frisancho, 1975, 1993). This adjust-
For example, cultural and technological responses permit ment can be either temporary or permanent, acquired
humans to live under extreme conditions of cold stress either through short-term or lifetime processes, and may
with the result that some of the physiological processes involve physiological, structural, behavioral, or cultural
are not altered. However, on rare occasions, humans changes aimed at improving the organism’s functional
have been able to completely avoid an environmental performance in the face of environmental stresses.
stress. Witness the fact that the Eskimos, despite their If environmental stresses are conducive to differential
advanced technological adaptation to cold in their mortality and fertility, then adaptive changes may
everyday hunting activities, are exposed to periods of cold become established in the population through changes
stress and in response have developed biological in genetic composition and thus attain a level of
The Study of Human Adaptation 19

genetic adaptation. In this context, functional adapta- ACCLIMATIZATION

tion, along with cultural and genetic adaptation, is
viewed as part of a continuum in an adaptive process Acclimatization refers to changes occurring within
that enables individuals and populations to maintain the lifetime of an organism that reduce the strain
both internal and external environmental homeostasis. caused by stressful changes in the natural climate or
Therefore the concept of adaptation is applicable to all by complex environmental stresses (Eagan, 1963;
levels of biological organization from unicellular organ- Bligh and Johnson, 1973; Folk, 1974). If the adaptive
isms to the largest mammals and from individuals traits are acquired during the growth period of
to populations. This broad use of the concept of adapta- the organism, the process is referred to as either
tion is justified not only in theory but also because it developmental adaptation or developmental acclima-
is currently applied to all areas of human endeavor tization (Timiras, 1972; Frisancho, 1975, 1993). Stud-
so that no discipline can claim priority or exclusivity in ies on acclimatization are done with reference to both
the use of the term (Dubos, 1965). Functional adaptation major environmental stresses and several related
involves changes in organ system function, histology, secondary stresses. For example, any difference in
morphology, biochemical composition, anatomical the physiological and structural characteristics of
relationships, and body composition; either independ- subjects prior to and after residence in a tropical
ently or integrated in the organism as a whole. These environment is interpreted as a result of acclimatiza-
changes can occur through acclimation, habituation, tion to heat stress. In addition, because tropical
acclimatization or genetic adaptation. climates are also associated with nutritional and
disease stresses, individual or population differences
in function and structure may also be related to these
ACCLIMATION factors. On the other hand, in studies of acclimation
any possible differences are easily attributed to the
Acclimation refers to the adaptive biological changes major stress to which the experimental subject has
that occur in response to a single experimentally been exposed in the laboratory. For understanding
induced stress (Eagan, 1963; Folk, 1974) rather than to the basic physiological processes of adaptation, stud-
multiple stresses as occurring in acclimatization. As with ies on acclimation are certainly better than those of
acclimatization, changes occurring during the process acclimatization. However, since all organisms are
of growth may also be referred to as developmental never exposed to a single stress, but instead to
acclimation (Timiras, 1972; Frisancho, 1975, 1993). multiple stresses, a more realistic approach is that of
studying acclimatization responses. Thus, studies on
both acclimation and acclimatization are essential for
HABITUATION understanding the processes whereby the organism
adapts to a given environmental condition. This
Habituation implies a gradual reduction of responses rationale becomes even more important when the
to, or perception of, repeated stimulation (Eagan, aim is to understand the mechanisms whereby
1963; Folk, 1974). By extension, habituation refers to humans adapt to a given climatic area, since humans
the diminution of normal neural responses, for in a given area are not only exposed to diverse stresses
example, the decrease of sensations such as pain. Such but have also modified the nature and intensity of
changes can be generalized for the whole organism these stresses, as well as created new stresses for
(general habituation) or can be specific for a given part themselves and for generations to come.
of the organism (specific habituation). Habituation
necessarily depends on learning and conditioning;
which enable the organism to transfer an existing DEVELOPMENTAL ACCLIMATIZATION
response to a new stimulus. A common confusion is
that habituation can lead to adaptation. However, the The concept of developmental acclimatization (also
extent to which these physiological responses are referred to as developmental adaptation) is based
important in maintaining homeostasis depends on upon the fact that the organism’s plasticity and suscep-
the severity of environmental stress. For example, with tibility to environmental influence is inversely related
severe cold stress or low oxygen availability, failure to to developmental states of the organism, so that the
respond physiologically may endanger the well-being younger the individual the greater is the influence
and survival of the organism. Likewise, getting used to of the environment and the greater the organism’s
tolerating high levels of noise implies ignoring the plasticity (Frisancho, 1975, 1993; Frisancho and
stress, which eventually can lead to deafness. In other Schechter, 1997). Hence, variability in physiological
words, habituation is a process that in the long run traits can be traced to the developmental history of
produces negative side effects. the individual.
 20 A. Roberto Frisancho

ACCOMMODATION AND ADAPTATION is an important mechanism that facilitates human

biological adaptation (Thomas, 1975; Rappaport, 1976;
The term accommodation is used to describe responses Moran, 1979). It may be said that cultural adaptation
to environmental stresses that are not wholly success- during both contemporary times and in an evolutionary
ful because, even though they favor survival of the perspective, represents humanity’s most important tool.
individual, they also result in significant losses in some It is through cultural adaptation that humans have
important functions (Waterlow, 1990). For example, been able to survive and colonize far into the zones
subjects when exposed to a low intake of leucine for of extreme environmental conditions. Humans have
three weeks can achieve body leucine balance at the adapted to cold environments by inventing fire and
expense of reducing protein synthesis and protein clothing, building houses, and harnessing new sources
turnover (Young and Marchini, 1990). Since low of energy. The construction of houses, use of clothing in
protein synthesis and protein turnover diminishes the diverse climates, certain behavioral patterns, and work
individual’s capacity to successfully withstand major habits, represent biological and cultural adaptations to
stresses, such as infectious diseases (Frenk, 1986), climatic stress. The development of medicine, from its
under conditions of low-dietary protein intake achiev- primitive manifestations to its high levels in the present
ing body leucine balance represents only a temporary era, and the increase of energy production associated
accommodation, which in the long run is not adaptive. with agricultural and industrial revolutions are represen-
In other words, accommodation is a stopgap that tative of human cultural adaptation to the physical
ultimately produces negative side effects. environment.
Culture and technology have facilitated biological
adaptation, yet they have also created, and continue to
INDIVIDUALS VERSUS POPULATIONS
create, new stressful conditions that require new adap-
tive responses. A modification of one environmental
Whatever the method employed, geographical or experi-
condition may result in the change of another, and
mental research in human adaptation is concerned with
such a change may eventually result in the creation of
populations, not with individuals; although the research
a new stressful condition. Advances in the medical
itself is based on individuals. There are two related
sciences have successfully reduced infant and adult
reasons for this.
mortality to the extent that the world population is
The first is a practical consideration. Studying all
growing at an explosive rate, and unless world food
members of a given population, unless its size is small
resources are increased, the twenty-first century will
enough, is too difficult to be attempted by any research
witness a world famine. Western technology, although
team. Therefore, according to the objectives of the
upgrading living standards, has also created a polluted
investigation, the research centers on a sample that is
environment that may become unfit for good health
considered representative of the entire population.
and life. If this process continues unchecked,
Based on these studies, the researchers present a
environmental pollution will eventually become
picture of the population as a whole, with respect to
another selective force to which humans must adapt
the problem being investigated.
through biological or cultural processes, or else face
The second reason is a theoretical one. In the study
extinction. Likewise, cultural and technological adap-
of adaptation, we usually focus on populations rather
tation has resulted in the rapid increase of energy
than on individuals because it is the population that
availability and has decreased energy expenditure;
survives and perpetuates itself. In the investigation
causing a disproportionate increase in the develop-
of biological evolution, the relevant population is the
ment of degenerative diseases associated with meta-
breeding population because it is a vehicle for the
bolic syndrome. This mismatch between biology and
gene pool, which is the means for change and hence
lifestyle threatens our survival as human species
evolution. The study of an individual phenomenon
(Eaton et al., 2002). Therefore, adaptation to the world
is only a means to understand the process. The adapta-
of today may be incompatible with survival in the
tion of any individual or individuals merely reflects the
world of tomorrow unless humans learn to adjust their
adaptation that has been achieved by the population of
cultural and biological capacities.
which he is a member.

CULTURAL AND TECHNOLOGICAL GENETIC ADAPTATION AND ADAPTABILITY

ADAPTATION
Genetic adaptation refers to specific heritable charac-
Cultural adaptation refers to the nonbiological responses teristics that favor tolerance and survival of an
of the individual or population to modify or ameliorate individual or a population in a particular total envir-
an environmental stress. As such, cultural adaptation onment. A given biological trait is considered genetic
The Study of Human Adaptation 21

when it is unique to the individual or population and

Environmental influences
when it can be shown that it is acquired through during growth and development
biological inheritance. A genetic adaptation becomes have a high influence and
established through the action of natural selection elicit a high morphological
(Neel, 1962; Livingstone, 1958; Neel et al., 1998; Mayr, response
1997). Natural selection refers to the mechanisms
whereby the genotypes of those individuals showing
the greatest adaptation or “fitness” (leaving the most Morphological
Genetic Genetic
descendents through reduced mortality and increased phenotypic
trait mediation
fertility) will be perpetuated, and those less adapted to response
the environment will contribute fewer genes to the
population gene pool. Natural selection favors the
features of an organism that bring it into a more Environmental influences
efficient relationship with its environment. Those during adulthood
gene combinations fostering the best-adapted pheno- have a low influence and
types will be “selected for,” and inferior genotypes will elicit a low morphological
response
be eliminated.
The selective forces for humans, as for other 2.2. Schematization of interaction of genetic and environment
mammals, include the sum total of factors in the nat- and the phenotypic morphological outcome. Morphological and
ural environment. All the natural conditions, such as physiological diversity reflects the responses and adaptations
that the organism makes to particular environment during and
hot and cold climates and oxygen-poor environments,
development. From Frisancho (1993).
are potential selective forces. Food is a selective force
by its own abundance, eliminating those susceptible to
obesity and cardiac failures, or by its very scarcity, and individual flexibility. Extinct populations are those
favoring smaller size and slower growth. In the same which were unable to meet the challenges of new
manner, disease is a powerful selective agent, favoring conditions. Thus, contemporary fitness requires both
in each generation those with better immunity. The genetic uniformity and genetic variability.
natural world is full of forces that make some individ- Contemporary adaptation of human beings is both
uals, and by inference some populations, better the result of their past and their present adaptability
adapted than others because no two individuals or (Lasker, 1969; Frisancho, 1993). It is this capacity to
populations have the same capacity of adaptation. adapt that enables them to be in a dynamic equilibrium
The maladapted population will tend to have lower in their biological niche. It is the nature of the living
fertility and/or higher mortality than that of the organism to be part of an ecosystem whereby it modifies
adapted population. the environment and, in turn, is also affected by
The capacity for adaptation (adaptability) to envir- such modification. The maintenance of this dynamic
onmental stress varies between populations and even equilibrium represents homeostasis; which, in essence,
between individuals. The fitness of an individual or reflects the ability to survive in varying environments
population is determined by its total adaptation to the (Dubos, 1965; Proser, 1964). The ecosystem is the
environment – genetic, physiological, and behavioral fundamental biological entity – the living individual
(or cultural). Fitness, in genetic terms, includes more satisfying its needs in a dynamic relation to its habitat.
than just the ability to survive and reproduce in a given In Darwinian terms, the ecosystem is the setting for
environment; it must include the capacity for future the struggle for existence, efficiency and survival are
survival in future environments. The long-range fitness the measures of fitness, and natural selection is the
of a population depends on its genetic stability and process underlying all products (Proser, 1964).
variability. The greater the adaptation, the longer the In general, the morphological and functional features
individual or population will survive, and the greater reflect the adaptability or capacity of the organism to
the advantage in leaving progeny resembling the respond and adapt to a particular environment
parents. In a fixed environment, all characteristics (Figure 2.2). The effect and responses to a given environ-
could be under rigid genetic control with maximum mental condition are directly related to the developmental
adaptation to the environment. On the other hand, in stage of organism; so that the younger the age, the
a changing environment a certain amount of variabil- greater the effect and the greater the flexibility to respond
ity is necessary to ensure that the population will and adapt. Conversely, the later the age and, especially
survive environmental change. This requirement for during adulthood, the effect of the environment is less
variability can be fulfilled either genetically or pheno- likely to be permanent and the capacity to respond and
typically or both. In most populations a compromise adapt is also diminished when compared to a developing
exists between the production of a variety of genotypes organism.
 22 A. Roberto Frisancho

MULTILEVEL SELECTION AND EVOLUTION single defector (Traulsen and Nowawk, 2006). Hence,
OF CO-OPERATION this simple condition ensures that selection favors
co-operators and opposes defectors.
Ever since Darwin (1871) indicated that the competi- The concept of group selection has been a major
tion between groups can lead to selection of co-opera- tenet of behavioral ecology. The major premise of
tive behavior, the concept of multilevel selection has behavioral evolutionary ecology is that genetic and
been developed. He stated that, “there can be no doubt behavioral traits are two distinct expressions of a
that a tribe including many members who were single evolutionary process. (Trivers, 1971; Cronk,
always ready to give aid to each other and to sacrifice 1991; Strier, 2000; Silk, 2001). In behavioral ecology,
themselves for the common good, would be victorious behaviors are treated like any other biological trait
over other tribes; and this would be natural selection” and are potentially subject to natural selection. The
(Darwin, 1871, p. 166). Over many years, Wilson and processes involved in behavioral evolution are
colleagues have been the main proponent of the idea of equivalent to those in genetic evolution: natural selec-
group selection (Wilson, 1975; Sober and Wilson, 1998; tion influences the frequency of a trait transmitted
Traulsen and Nowak, 2006). It is assumed that group from parent to offspring through differential fertility
selection is an important organizing principle that and mortality. In the evolutionary perspective, bio-
permeates evolutionary processes from the emergence logical structures have been custom tailored to motiv-
of the first cells to development of nations. According ate behaviors that are likely to enhance individual
to multilevel selection, groups consist of genetically fitness. Therefore, behavioral variants with a high
unrelated individuals, and successful groups attract fitness have been favored and these perpetuate the
new individuals, which learn the strategies of others evolutionary origin of fitness-enhancing biological
in the same group. A population can be subdivided traits. It follows then, that the behavioral traits that
into groups, and the individuals interact with other enhance fitness also accentuate biological fitness.
members of the group, and depending on their repro- In other words, a change occurring in one system
ductive fitness, individuals can lead to larger groups entails a change in the fitness governing evolution in
that split more often. In other words, higher-level or the other system. Therefore, both genetic and behav-
group selection emerges as a by-product of individual ioral selection tend to favor those existing variants
reproduction. whose net effect is to increase the average fitness
A fundamental condition for the success of the of the individual and population to the prevailing
group, therefore, must be co-operation among indi- conditions. Studies of primates indicate that they
viduals, and thus group selection favors co-operative use a diversity of behaviors that increase the likeli-
altruistic behavior and opposes defectors. The fitness hood of gaining access to mates and guarantee the
of an individual, and the group at large, also depends survival of their offspring; which, in turn, insures the
on the altruistic behavior of nonrelatives. When an passing of their traits to the next generation. In this
altruist gives an alarm call, it benefits not only his or context, behavioral actions that lead to a higher
her relatives, but also other unrelated members of reproductive success will become adaptive and the
the group because a primate troop does not only genes associated with such behavior will be trans-
include relatives. Thus, altruism can be selected ferred to the next generation faster than those that
if these nonrelated individuals can be counted on to are less adaptive. Therefore, the differences in fitness
reciprocate the favor when the need arises. between individuals and populations will determine
A recipient of an altruistic behavior who fails to recip- the behavioral pattern of a given primate group.
rocate is a cheater. Studies of nonhuman primates In other words, a specific behavioral strategy that
indicate that a cheater may gain in the short run by contributes to the survival and reproductive fitness
receiving aid without any costs to their own fitness of the individual – and eventually the population –
(Strier, 2000). However, reciprocity is necessary becomes part of the genetic milieu of the species.
for future support in the long run because the In summary, co-operation and altruism evolve by
cheater’s fitness is lower when compared to the group selection or multilevel selection. Human behav-
individual who reciprocated. In view of the fact that ioral ecology rests upon a foundation of evolutionary
primates constantly need to protect themselves from theory, which include sexual selection, whereby indi-
neighboring communities and predators, one can viduals within one sex secure mates and produce
assume that reciprocal altruism must have been offspring at the expense of other individuals within
selected for because it enhanced their fitness, not the same sex, which can cause changes in gene
because the animals are conscious of their motives frequency across generations that are driven at least
or the reproductive consequences of their behavior. in part by interactions between related individuals
Mathematical models indicate that a single co- referred to as kin selection, and be expressed as the
operator has a greater fixation probability than a sum of an individual’s own reproductive success.
The Study of Human Adaptation 23

CURRENT DIRECTIONS IN ADAPTATION mellitus was a quick insulin trigger. Insulin’s main func-
RESEARCH tion is to assist in the homeostasis of glucose in the
blood. Specifically, when blood glucose levels are too
In the 1970s I postulated the hypothesis of develop- high, the pancreas releases insulin to increase tissue
mental adaptation to explain the enlarged lung volume uptake of glucose, thus reducing blood glucose levels.
and enhanced aerobic capacity that characterize the Conversely, when blood glucose levels are low, the
Andean high altitude natives. According to the organism secretes glucagon and growth hormone, which
developmental adaptation hypothesis, “adult biological in turn, induce the release of stored glucose and fatty
traits are the result of the effects of the environment acids into the blood stream raising serum glucose levels.
and the physiological responses that the organism The insulin response is to activate an uptake of glucose
makes during the developmental state” (Frisancho, into the muscle cells for storage, and in liver cells it
1970, 1975, 1977). This concept is based upon the fact influences the conversion of glucose to fatty acids for
that the organism’s plasticity and susceptibility to envir- storage in fat (adipose) tissue. This response was an
onmental influence is inversely related to developmen- asset during times of abundance because it would allow
tal states of the organism, so that the younger the an individual to build-up energy reserves more quickly
individual the greater is the influence of the environ- and thus better survive times of food scarcity. Under
ment and the greater the organism’s plasticity these conditions, the thrifty gene was selected to regulate
(Frisancho, 1975, 1977, 1993). Hence, variability in efficient intake and utilization of fuel stores. In other
physiological traits can be traced to the developmental words, during periods of food shortage and famine,
history of the individual (Figure 2.2). Currently this those with the thrifty genotype would have a selective
concept has been applied to explain the variability in advantage because they relied on larger, previously
adult behavioral traits such as in learning and crime and stored energy to maintain homeostasis; whereas those
delinquency (Yueh-Au Chien, 1994; Sroufe et al., 2005; without “thrifty” genotypes would be at a disadvantage
Kruger et al., 2008), in sensory inputs and auditory and less likely to survive and reproduce. However, under
spatial processing (Martin and Martin, 2002), in toler- modern conditions of abundant food and sedentary
ance to surgical intervention (Faury et al., 2003), in lifestyle, this genotype becomes perversely disadvanta-
variability in oxygen consumption and mitochondrial geous. With a constant abundance of food, insulin levels
membrane potential in energy metabolism of rat remain high, resulting in tissues becoming less sensitive
cortical neurons (Schuchmann et al., 2005), and in to the effects of insulin. This reduced sensitivity to the
variability in increased risk of adult obesity and cardio- effects of insulin results in chronically elevated blood
vascular problems associated with the metabolic glucose levels type II diabetes and related chronic health
syndrome (Barker, 1994). A common denominator of problems (e.g., obesity).
all these studies is that humans and many other A test of the genetic predisposition to type II
organisms are conditioned by experiences during devel- diabetes involved a comparative study of the Pima
opment and as developmental experiences is an import- Indians of southern Arizona and the Pima Indians of
ant contributor to variability in adult phenotypic the Sierra Madre mountains of northern Mexico
behavioral and biological traits. (Knowler et al., 1990; Price et al., 1992). These two
In this section I will summarize the evidence groups, which were separated 700 1000 years ago,
supporting the applicability of the concept of develop- differ in their life style. The Arizona Pima live under
mental adaptation to account for the origins of the high conditions of access to a high fat, highly refined diet
risk of the adult metabolic syndrome incorporating and low energy expenditure. In contrast, the Mexican
information derived from thrifty gene, thrifty pheno- Pima still pursue a much more traditional lifestyle
type, and epigenetics. The evolution of the metabolic and have a diet based on the occasional intake of
syndrome is also discussed at length in Chapter 30 of lamb and poultry, but mainly on beans, corn, and
this volume. potatoes, grown by traditional, and physically very
energy-demanding, techniques. These two groups
differ significantly in the frequency of obesity and
DEVELOPMENTAL ADAPTATION AND THE diabetes. The Arizona Pima adults have a body mass
THRIFTY GENOTYPE index (BMI) of 33.4 kg/m2; compared to a BMI of 24.9
kg/m2 in the Mexican Pima (Ravussin et al., 1994).
Neel and colleagues (Neel, 1962; Neel et al., 1998) Likewise, in the Arizona Pima 37% of men and 54%
attempted to explain the epidemic proportions of of women were diabetic, while in the Mexican Pima
diabetes in Native American populations, such as the only 2 of 19 women and 1 of 16 men were diabetic
Pima Native Americans, by postulating the existence of (Knowler et al., 1990; Price et al., 1992). In other
a “thrifty gene” that increased the risk of type II diabetes. words, although the Mexican Pima share the “thrifty
According to this hypothesis, the basic defect in diabetes gene” with Arizona Pima, their increased frequency of
 24 A. Roberto Frisancho

obesity and diabetes is more evidence that an abun- Poor maternal nutrition
dance of fatty foods and modern sedentary lifestyles associated with fetal
undernutrition
are the real culprits. Thus, it is not the presence of a
“thrifty gene” alone that results in increased rates of
diabetes, but rather the interaction with modern diet- Fetal programing: Cellular,
ary and lifestyle conditions the results in increased physiological, and metabolic
rates of the chronic health problems. compensatory responses
resulting in energy conservation
In summary, the thrifty genotype hypothesis has
been used to explain the epidemic levels of obesity
and diabetes among non-Western populations, such Adult poor Adult good
postnatal postnatal
as South Pacific Islanders, sub-Saharan Africans,
nutrition and high nutrition and low
Native Americans in the southwestern United States, energy energy
Inuit, Australian aborigines, etc. (Eaton et al., 1988; expenditure expenditure
O’Dea, 1991); all of whom were newly introduced to
industrialized diets and environments. The fact that
the frequency of type II diabetes has recently increased Nondiabetic Type II diabetic
and good health and polor health
among Europeans that were not subjected to periodic
famines cannot be attributed to the action of a 2.3. The thrifty phenotype. The risk of type II diabetes and
so-called “thrifty” gene. metabolic syndrome in adulthood is associated with prenatal
undernutrition resulting in efficient physiological adaptation that
becomes detrimental when food is abundant and energy
expenditure is low.
DEVELOPMENTAL ADAPTATION AND
THE THRIFTY PHENOTYPE
the Dutch famine of World War II were found to have
Recently, Barker and colleagues (Barker, 2007; Hales impaired glucose tolerance and increased adiposity
and Barker, 1992) have reported an inverse relationship in adulthood (Stein et al., 1975, 2007).
between birthweight and the risk of hypertension,
cardiovascular disease, and type II diabetes in adulthood
when the individual is well nourished postnatally. DEVELOPMENTAL ADAPTATION AND
To account for these observations, Barker and colleagues EPIGENETICS
proposed that adverse effects in utero induce cellular,
physiological, and metabolic compensatory responses, Epigenetics refers to the transmission of phenotypic
such as insulin resistance, high blood plasma levels of traits from one generation to the next that do not
fatty acids, which result in energy conservation and depend on differences in DNA sequence (Waddington,
reduced somatic growth that enable the fetus to survive 1952; Jablonka, 2004; Holliday, 2006). During the last
undernutrition. This response is referred to as the thrifty two decades, there has been an accumulation of obser-
phenotype hypothesis (Armitage et al., 2005). These vations indicating that the expression of DNA traits can
responses that were adaptive under poor prenatal condi- be affected by environmental factors acting during
tions become a problem if food becomes abundant. development. Specifically, experimental studies
In this view, thrifty physiological mechanisms are showed that identical twin mice differ in the color of
adaptive in nutritionally poor environments, but in rich fur; one has brown fur and will grow up to be lean and
environments are maladaptive. That is, what was positive healthy, while the other has yellow fur and becomes
under reduced availability of nutrients, particularly obese and prone to cardiovascular disease. The differ-
during periods of rapid development, becomes negative ent phenotypes are due to the addition of a methyl
in rich environments because it facilitates nutrient group (-CH3); which is referred to as methylation.
absorption and hence increases the risk of adult obesity
and the suite of risk factors for cardiovascular disease
Methylation
known as the metabolic syndrome (Figure 2.3).
In summary, it appears that nutrition and other Methylation refers to the altering of the genetic envir-
environmental factors during prenatal and early post- onment through the addition of a methyl group (-CH3)
natal development influence cellular plasticity; thereby to the fifth position of cytosine, which is largely
altering susceptibility to adult cardiovascular disease, confined to CpG dinucleotides. This addition, by modi-
type II diabetes, obesity, and other chronic diseases fying the CpG islands, prevents signaling molecules
referred as the adult metabolic syndrome. This hypoth- from reaching the promoter site to turn the gene on
esis is supported by the finding that the offspring of and prevent the expression of the dark coat color.
women who were starved and became pregnant during In other words, the additional methyl group attaches
The Study of Human Adaptation 25

to and shuts off the gene that controls dark fur color the organism; so that the younger the individual, the
and allows the yellow color to be expressed. Thus, the greater the epigenetic marks, including CpG methyla-
process of methylation works as a kind epigenome that tion. Despite the great interest in molecular genetics,
dictates which genes in the genome are turned on and there is scant incontrovertible evidence indicating
which are not. This process can differ even between epigenetic effects in humans. Considering society’s
identical twins. increased concern about environmental pollutants, this
Recently, experimental studies indicate that area of research should a good direction for human
bisphenol A (BPA) can alter gene expression and biologists.
affect adult phenotype by modifying CpG methylation
at critical epigenetically labile genomic regions (Water-
land and Jirtle, 2004). Bisphenol A is used in the produc- OVERVIEW
tion of polycarbonate and plastic containers and in
the organism acts like the body’s own hormones. Thus, The term adaptation encompasses the physiological,
there is concern that long-term exposure to BPA may cultural, and genetic adaptations that permit individ-
induce chronic toxicity in humans (vom Saal and uals and populations to adjust to the environment in
Hughes, 2005). Fortunately, the effects of methylation which they live. These adjustments are complex, and
are not permanent but reversible, as shown by the fact the concept of adaptation cannot be reduced to a simple
that the yellow agouti (Avy), whose diet was supple- rigid definition without oversimplification. The func-
mented with folic acid, vitamin B12, choline, betaine, tional approach in using the adaptation concept permits
and zinc, counteracted the DNA methylation and its application to all levels of biological organization
changed coat color from yellow to dark brown coat from unicellular to multicellular organisms, from early
(Dolinoy and Jirtle, 2008), which is associated with a embryonic to adult stages, and from individuals to popu-
low risk of cardiovascular disease. lations. In this context, human biological responses to
environmental stress can be considered as part of a
continuous process whereby past adaptations are modi-
Transgenerational epigenetic effects
fied and developed to permit the organism to function
It has been suggested that the epigenetic modifications and maintain equilibrium within the environment to
brought about by parental conditions may be which it is daily exposed.
expressed even in grandchildren. Extensive records of The mechanisms for attaining full functional adap-
a population in Overkalix cohorts, northern Sweden, tation include acclimation, acclimatization, habitu-
found that an association between grandparental ation, and accommodation. The role played by each
prepubertal slow growth periods (SGP) or rapid of these processes depends on the nature of the stress
growth periods (RGP), and parental periods of low or or stresses, the organ system involved, and the devel-
high food availability, with grandchildren’s mortality opmental stage of the organism. It is emphasized that
and disease risk (Kaati et al., 2007). If the SGP of the the goal of the organism’s responses to a given stress is
grandparent was a period of high food availability, to maintain homeostasis within an acceptable normal
then the male grandchild had reduced longevity but range with itself and with respect to other organisms
an increased mortality. The extent to which these and the environment (as schematized in Figure 2.1).
associations represent multigenerational epigenetic Such adaptations are usually reversible, but the revers-
effects is unwarranted, in part because ruling out ibility depends on the developmental stage of the
genetic and societal confounders, and in the absence organism at which the adaptive response occurs and
of molecular evidence, is extremely difficult. Hence, the nature of the environmental stress. This character-
future research must be focused on long-term transge- istic allows organisms to adapt to a wide range of
nerational studies whereby many birth cohorts are environmental conditions. Furthermore, an adaptation
studied using intensive prenatal and perinatal genotyp- is always a compromise between positive and negative
ing across generations. Only then can variability in the effects. Every adaptation involves a cost. The process
expression of phenotypic traits can be attributed to of adaptation is always positively beneficial; without
epigenetic changes. which the organism would be worse off, however the
In summary, epigenetic effects exist that are not organism has to pay a price for the benefit. The benefit
necessarily adaptive, and in many of these cases, the derived from a given response depends on the circum-
inherited phenotype is actually detrimental to the organ- stances and the conditions where it occurs. As recently
ism. Environmental exposure to nutritional, chemical, pointed out (Young and Marchini, 1990), every adap-
and physical factors can alter gene expression and affect tation involves a choice. For example, a man has
adult phenotype: a process known as epigenetics. In all 6 hours in which to walk 11 km. If he walks slowly,
of these studies, the extent of DNA methylation depends he saves energy expenditure, and therefore it may be
on and is inversely related to the developmental state of adaptive if the energy resources are limited; however
 26 A. Roberto Frisancho

he has no time left to do anything else. On the other 7. Compare developmental and adult adaptation.
hand, if he walks fast, he saves time at the cost of using Which is more likely to be reversible and why?
more energy. Thus, the adaptive importance of given 8. Discuss the applicability of the concept of develop-
type of response depends on the conditions. mental adaptation to the hypothesis thrifty geno-
The concept of developmental adaptation has type and thrifty phenotype that account for the
become a major focus for studying the origins of human increased frequency of the adult metabolic syn-
diversity (Figure 2.2). The applicability of this research drome among native and nonnative populations.
strategy is based upon the premise that human biological 9. Discuss the relationship of the concept of develop-
responses to environmental stress represent a continu- mental adaptation to the field of epigenetics.
ous process whereby past adaptations are modified and
developed to permit the organism to function and main-
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