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Edited by Kristen Hawkes, University of Utah, Salt Lake City, UT, and approved November 9, 2007 (received for review August 24, 2007)
Abstract
Explanations for the evolution of human pygmies
continue to be a matter of controversy, recently fuelled by the
disagreements surrounding the interpretation of the fossil hominin Homo floresiensis.
Traditional hypotheses assume that the small body size of human pygmies
is an adaptation to special challenges, such as thermoregulation,
locomotion in dense forests, or endurance against starvation. Here, we
present an analysis of stature, growth, and individual fitness for a
large population of Aeta and a smaller one of Batak from the Philippines
and compare it with data on other pygmy groups accumulated by
anthropologists for a century.
The results challenge traditional
explanations of human pygmy body size. We argue that human pygmy
populations and adaptations evolved independently as the result of a
life history tradeoff between the fertility benefits of larger body size
against the costs of late growth cessation, under circumstances of
significant young and adult mortality. Human pygmies do not appear to
have evolved through positive selection for small stature—this was a
by-product of selection for early onset of reproduction.
Human pygmies are defined as populations having an average male height <155 a="" class="xref-bibr" cm="" href="https://www.pnas.org/content/104/51/20216#ref-1" id="xref-ref-1-1">1
There are, however, many populations exhibiting pygmy stature outside
Africa, including ones in the Andaman Islands, Malaysia, Thailand,
Indonesia, the Philippines, Papua New Guinea, Brazil, and Bolivia [ref. 3 and supporting information (SI) Fig. 4].
The small body size of human pygmies has been interpreted as an
adaptation in itself, whether to living in dense tropical forests (4), thermoregulation (1), or endurance against starvation in low productivity environments (5). However, as described by Diamond (5),
none of these explanations account for the worldwide distribution of
human pygmies—some pygmy-sized populations are found outside forests,
and many live in cool and dry areas; furthermore, long-standing poor
nutrition does not necessarily lead to pygmy size, as shown by groups
who, like certain pygmies, experience frequent food shortages (6–8)
and yet are among the tallest populations in the world.
The adaptive
value of pygmy body size remains an unanswered question in human
evolutionary biology, and one thrown into sharp relief by the recent
discovery of a small-bodied fossil hominin population of Flores (9–11).
This article presents the results of the first population-wide study of
the growth, fertility and mortality of two pygmy groups, the Aeta and
Batak from the Philippines (3),
giving unique insights into the life history of these populations and
the fitness associated with variation in their phenotype. The data from
these two groups were compared with those available for African pygmies
to explore three questions—whether short stature is adaptive among
pygmies, whether pygmy growth rates and final stature reflect
nutritional stress, and whether age of onset of reproduction and
cessation of growth correlate with individual fitness.
Results
Pygmy Growth Curves: A Comparative Approach.
In most human populations, a large portion of variance in stature can be accounted for by nutritional status (12).
Nutritional studies worldwide have shown the predictability of the
growth response to stress—societies with very high caloric budgets show
significant secular trends toward earlier growth cessation, faster body
growth, and increased size, whereas populations under nutritional stress
normally reduce growth rates, delay growth cessation, and show smaller
adult body sizes (12).
To test whether the growth pattern of pygmies is characteristic of
nutritionally impaired populations, growth curves were constructed for
the Aeta and compared with those for the Biaka (13) and Agta (14)
pygmies and compared with the lower percentiles of the U.S. growth
distribution, representing undernourished individuals who grow only to
average adult pygmy size (womenHEIGHT = 140 cm, corresponding to the 0.01th percentile of the U.S. distribution) (15). The curves show that pygmies terminate growth at an earlier age than the U.S. under-nourished sample (Fig. 1).
Although the National Center for Health Statistics 0.01th percentile
achieves adult size at age 15, pygmy women grow at higher rates and
achieve a similar adult height at 12–13 years of age. In fact, ages at
growth cessation among the Aeta, Agta, and Biaka are similar to those
observed in the extremely well nourished 95th percentile of the U.S.
distribution, whose adult size exceeds pygmy size by >30 cm. Very
similar results are observed in men (data not shown). Further evidence
that pygmy size is not just a plastic response to nutritional stress is
provided by a comparison with eastern African Pastoralists (16),
such as the Turkana and the Maasai from Kenya, who rank amongst the
tallest traditional human populations (data for women: Turkana = 166 cm,
Maasai = 160 cm; worldwide average male body size of 2,503 ethnographic
populations is 163.9 cm, average female body size of 434 ethnographic
populations is 159.9 cm) [Human Diversity Project, unpublished data
(Leverhulme Centre for Human Evolutionary Studies, Cambridge, U.K.) and SI Fig. 5]. Both the Aeta, Biaka, and eastern African Pastoralists rely on limited caloric budgets (6–8) and therefore grow at slower rates than average western European and U.S. populations (Fig. 1).
Despite dramatic differences in adult body sizes (between a 25- and an
35-cm difference), female pygmies and eastern African Pastoralists show
similar growth deficits from early infancy to age 12 compared with
western European and U.S. populations. Although the Aeta, Agta, and
Biaka growth curves are placed between the percentiles 0.1 and 1,
eastern African Pastoralists compare to the 5th to 10th percentile of
the U.S. distribution. However, from age 12 onwards, there is a clear
divergence in the growth trajectories of the three groups.
Eastern
African Pastoralists continue to grow for 3–4 years after the Aeta,
Agta, and Biaka growth curves level off, moving continuously up from the
7th to the 50th percentile of the U.S. distribution between ages 12 and
22, thereby achieving the average height of well nourished American
adults. In contrast, pygmies do not extend their growth trajectories and
stop growing as early as the U.S. 50th percentile (Fig. 1),
dropping to the percentile 0.01 at adulthood. Thus, the smaller adult
size of pygmies relative to eastern African Pastoralists is mostly
caused by a difference in duration rather than rate of growth, the
opposite of what is observed in cases of nutritionally induced stunting (12).
Fig. 1.
Growth curves for different human populations. Pygmy women [Aeta (black triangles), n = 214; Biaka (13) (gray triangles), n = 157; and Agta (14) (open triangles), n
= 83] grow at rates bellow the 5th U.S. percentile (intermediate solid
line), and their growth curves level off early at ≈13 years old,
reaching an adult body size equivalent to the percentile 0.01 (lower
solid line). African Pastoralists (16) [Massai (open squares) and Turkana (black squares), n
= 228], also grow at slow rates compared with U.S. subjects but extend
their growth trajectories and achieve final height equivalent to the
U.S. 50th percentile (solid upper line).
Pygmy Mortality and Fertility Schedules.
Given these results, we investigated how early
growth cessation correlates with other aspects of life history among
pygmies. The second and perhaps most distinctive feature of known pygmy
populations is their very high adult and preadult mortality rates, more
comparable with values observed in chimpanzees (17) than in other human traditional populations (18–20) (Fig. 2
a). Life expectancy at birth in human pygmy groups is very low [24.2, 16.5, 24.3, 16.6, 15.6, and 16 years in Batak (3), Aeta (3), Agta (21), Aka (1), Mbuti (22), and Efe (3),
respectively, significantly different from eastern African Pastoralists
and other non-pygmy hunter-gatherer populations (34.6, 37.1, and 47.5
years in !Kung (19), Ache (18), and Turkana (20), respectively]. Chances of surviving to adulthood are also markedly reduced in pygmies: whereas only 51% of Batak (3), 33% of Aeta (3), 47% of Agta (21), 40% of Aka (1) and Mbuti (22), and 30% of Efe (3)
children are expected to survive to 15 years of age, in other foragers
and eastern African Pastoralists, those values are 76% (Turkana) (20), 59% (Kung!) (19), and 64% (Ache) (18).
Patterns of both prereproductive and adult mortality separate human
pygmies from these other groups: life expectancy at adulthood (defined
here as age 15 years) is, respectively, 29.5, 27.3, 22.5, 20, and 32.5
years in Batak (3), Aeta (3), Aka (1), Mbuti (22), and Efe (3), against 41.5, 45.8, and 46.6 years in !Kung (19), Ache (18), and Turkana (20),
respectively.
Shortened lifespans also reduce the number of pygmy women
who reach the end of the reproductive period. Age at last reproduction
in the Aeta averages 37.4 years (±7.3, n = 11), but only 13–31%
of women in pygmy populations survive from birth to this age. However,
Turkana women reproduce until as late as 40.3 years (±7, n = 60) (21),
and 63% of women survive to that age. We argue that the precocity of
death in pygmies is the key to the evolution of both pygmy size and life
history. According to life history theory (23),
age at first reproduction is set by natural selection as the result of
two opposite forces. On one hand, extended growth and the resulting
larger adult size engender fertility gains and reduced offspring
mortality, implying a pressure for delayed reproductive onset. On the
other hand, early age at first reproduction is advantageous for
minimizing the likelihood of death before reproduction, and reducing
generation time. Thus, small body size in pygmies can be explained as a
life history tradeoff between extended growth and early reproduction,
with the balance pending toward the latter because of their
exceptionally high mortality rates. This hypothesis is supported by the
third common feature of human pygmy populations: Age-specific fertility
curves (3, 18, 20, 21) are shifted toward earlier ages, showing an earlier peak of fertility when compared with non-pygmy groups (Fig. 2
b).
Fig. 2.
Age-specific survivorship (a) and age-specific fertility (b) for different human pygmies. Pygmy populations: Eastern African Pygmies (3) (gray triangles, dashed line), Western African Pygmies (1) (gray triangles, solid lines), Aeta (3) (black triangles, solid line), Batak (3) (black circles, solid line), and Agta (21) (open triangles, solid lines). Non-pygmy populations: !Kung (19) (gray square, solid line), Ache (18) (cross, dashed line), Turkana (20) (black square, dashed line), and chimpanzees (open circles, solid lines).
Modeling Fitness as a Function of Growth, Fertility, and Mortality Schedules in Human Pygmies.
We have presented empirical evidence supporting
the hypothesis that pygmy body size results from a tradeoff between time
invested in growth and in reproduction. However, because the legitimacy
of adaptive hypotheses can be more properly tested through the
measurement of fitness associated with different phenotypes, we used a
mathematical model to investigate whether optimal or average age at
first reproduction and adult body size can be predicted from the
mortality schedule in one pygmy population (the Aeta from the
Philippines, for which age-specific survivorship, fertility, and growth
curves were constructed).
The model estimates the effect of age at onset
of reproduction on individual fitness of pygmy women by calculating the
parameter r (fitness corrected by the intrinsic rate of population growth) from the Euler–Lotka equation (24), which includes age-specific survivorship (l
x) and age-specific fertility (m
x) as independent variables. We used a binary logistic regression to estimate the effect on fertility (m
x) of age, age squared, and stature (25) instead of body weight (18).
In this analysis, we assumed that observations from the same woman at
different ages were statistically independent. We found a positive
association between size and fertility in the Aeta and the Efe (linear
regression of offspring number on female adult height, controlling by
age; Aeta: r = 0.242, F = 9.34, P < 0.005, n = 154; Efe: r = 0.195, F = 4.34, P < 0.05, n = 110). No significant relationship was found between male fertility and height.
The model closely matches the actual distribution of age at first reproduction in the Aeta (Fig. 3).
Female fitness peaks with an age at first reproduction of 15 years,
much earlier than predicted for three other populations in which
individual fitness was modeled as a function of age and body size, the
Ache (18 years) (18), the !Kung (19.5 years) (19), and rural women in the Gambia (18 years) (25). The modal age at first reproduction in the Aeta pygmies is 16 years (n
= 110), compared with 17 in the Ache, 19 in the !Kung, and 18 in the
Gambian rural women. Our model also predicts higher fitness from very
early ages at first reproduction (12 years, corresponding to the
earliest recorded births in the population), as reflected in the real
distribution of reproductive onset (Fig. 3).
The precocity of reproduction in the pygmies is more evident when they
are compared with the tall and slow-growing Turkana women, who start
reproducing >4 years later than the Aeta (Turkana mean = 22.2 ± 3.3
years, n = 60 (20); Aeta mean = 18.5 ± 3.3 years, n
= 110). Higher fertility at younger ages and increased fitness
associated with an early age at first birth (16 years old) are only
predicted for the well nourished, fast growing, and tall Americans (18)
if they had remained under natural fertility conditions. The model
demonstrates a selective advantage associated with earlier ages at first
reproduction, which exceeds the fertility cost of the smaller adult
size in the Aeta. In other words, although larger women are more fertile
even among pygmies, the age-specific product of fertility and
survivorship is greater in smaller Aeta women.
Fig. 3.
Fitness as a function of size achieved at first reproduction. (Left) estimated relative fitness (r)
as a function of age at first birth for Aeta (solid line). The
histogram shows observed frequencies of first birth in Aeta women; the
dashed vertical line shows the predicted fitness peak (age at first
birth = 15 years). (Right) Models (adapted from refs. 18 and 25) of relative fitness as a function of age and size at first birth for Ache, !Kung (18), and Gambian rural women (25).
Discussion
Based on their high mortality rates, relatively
earlier growth cessation, and early peak of fertility, we postulate
that pygmies occupy the “fast” extreme of life history strategies (26)
among humans, with both longevity and resource availability as limiting
factors. The resulting short stature is only one of the aspects of the
fast pygmy life history package. The taller eastern African Pastoralists
are an example of the opposite “slow” extreme, equally limited from the
nutritional side but less constrained in terms of adult mortality.
Whereas mortality rates were shown to affect rates of growth relative to
adult body size in small-scale societies (27),
here we propose that the small body size of human pygmies evolved as a
by-product of selection for early onset of reproduction.
If our hypothesis is correct, the causes of the
extremely high mortality rates among human pygmies need to be
explained. It is here that the traditional hypotheses explaining the
small body size of pygmies may prove useful. Although the challenges
posed by thermoregulation, locomotion in dense forests, exposure to
tropical diseases, and poor nutrition do not account for the
characteristics of all pygmy populations, as pointed out by Diamond (5),
they may jointly or partially contribute to the similarly high
mortality rates in unrelated pygmy populations. We argue that the small
body size of African and Asian pygmy populations evolved independently
as a case of evolutionary convergence, resulting from a life history
tradeoff between the fertility benefits of larger body size and the
costs of late growth cessation under the circumstance of significant
young and adult mortality.
Finally, the data presented here show that
pygmy body size evolved through earlier cessation of growth, being
therefore the result of changes in late rather than early stages of
growth. This explains why brain growth, which is completed years before
the onset of adolescence (28), is not affected in human pygmies (29). Therefore, if Homo floresiensis is a dwarfed form of Homo erectus, as proposed in ref. 29,
the evolution of small body size on Flores could be understood as the
life history consequence of ecological conditions in islands, such as
increased extrinsic mortality rate and reduced resource availability (30);
however, its small brain size and low encephalisation require the
postulation of different adaptive mechanisms affecting earlier stages of
development.
Materials and Methods
Data Collection.
The new data on the Aeta and Batak Negritos
presented in the article were obtained during two seasons of fieldwork
of four and five months in 2002 and 2003, respectively. Aeta and Batak
individuals were measured to record their variation in body size and
body proportions, and extensive interviews were conducted to record the
genealogies and reproductive history of all adults.
Batak.
The Batak demographic data collected in this
study was added to the data collected by J. Eder (Arizona State
University, Tempe, AZ) in 1980, who kindly made his unpublished data
available for this study. We visited three of five Batak villages and
found 157 Batak. The number of Batak found by Eder in 1980 was 258, of
whom we identified 129 individuals (including living and deceased
people); this number corresponds exactly to 50% of the number of Batak
described by Eder. The other 28 Batak were not in Eder's census because
they were younger than 23 years old. Of the population of 129
individuals from Eder's census who were identified (directly interviewed
or referred to in the genealogies), 41% (53) had died in the 23
year-interval between 1980 and 2003.
Aeta.
We visited 13 of 71 Aeta villages in Zambales; in these, we met 668 Aeta (including children, men, and women of all ages) [see SI Figs. 6 and 7 and
SI Methods
].
Anthropometry.
Growth curves.
A total of 199 Aeta girls and 146 Aeta boys
from 0 to 20 years of age were measured by A.B.M. The Batak were not
included in growth analyses because of the small number of children
existent today. The data for other pygmy and non-pygmy groups are
available in refs. 13, 14, and 16.
Adult body sizes.
A total of 209 Aeta women and 146 Aeta men
older than 21 years of age had their height measured by using a movable
Harpenden Anthropometer. Adult height was not included in any analyses
for Batak population because of the small sample size.
Data on Individual Ages.
Aeta and Batak.
Ages were estimated as described in SI Table 1 and
SI Methods
.
Agta.
Exact ages are known for this population (14, 21).
The growth, fertility, and mortality similarities among Agta, Aeta, and
Batak show that the age estimates for both Aeta and Batak were precise
enough to produce reliable analyses.
Other populations.
The age estimates for individuals of all other
(Efe, Mbuti, etc.) pygmy groups included in the analyses were given by
the researchers who carried out the original studies.
Life Tables.
Aeta and Batak.
Mortality and survivorship rates were estimated from death records only (19) for the Aeta (n = 239) and the Batak (n = 202). Very similar estimates were obtained by fitting data of living individuals to Weiss model life tables (23).
Efe.
From 1928 to 1938, the Efe from the Ituri forest (Eastern African Pygmies) were studied by Schebesta and colleagues (31, 32).
From his data, we estimated average family size (6.6), population
average age (26.6 years), adult average age (34.7 years), and proportion
of the population >50 years of age (16.1%); these data were then fit
to Weiss model life table MT:32.5–30 (22).
Mbuti.
The Mbuti were studied by Turnbull (4). Based on his data, Weiss (22)
calculated average adult age, probability of dying in the first year of
life, and percentage population <15 age="" data="" fit="" life="" mbuti="" model="" mt:20="" of="" p="" table="" the="" to="" years="">
Aka.
Cavalli-Sforza (1) estimated average age among the Aka in 21 years and used this value to identify the Weiss model life table MT: 22.5–40.
Age-Specific Fertility.
Age-specific fertilities were calculated for both the Aeta (n = 191 women) and the Batak (n = 30 women) divided in 5-year intervals, following the methodology described in Hill and Hurtado (18). The data for other pygmy and non-pygmy groups are available in refs. 18, 20, and 21.
Modeling Fitness.
Hill and Hurtado adapted the Euler–Lotka Equation to include the effect of body size (weight) on fertility (ref. 18; see
SI Methods
). In our analysis of the Aeta, the equation was
rewritten to include the effect of height rather than weight on female
fertility as follows:
where l
x is survival from birth to age x, α is age at maturity, and m
x(H
α) is one-half of the expected fertility at age x (i.e., it only includes number of female offspring) as a function of body size at maturity (H
α). Varying α and solving for r determines which age of maturity corresponds to higher fitness (18). We calculated m
x(H
α), or fertility as a function of particular
ages associated with attaining adult (reproductive) body height, using
logistic regressions that examine the hazards of live births by age and
height for parous women (see
SI Methods
), as follows:
Based on the Aeta data, the resulting equation was:
Fertility was then calculated for hypothetical women starting reproduction at different ages [i.e., we calculated m
x(H
α) for values of α from 11 to 39]. Size at
growth cessation was calculated for one year before birth of the
offspring, approximately corresponding to the beginning of pregnancy
(see
SI Methods
). The predicted height (H
α) of hypothetical women stopping growth at
different ages at maturity (α) was estimated through an extension of a
regression of height on age. The regression was calculated for ages 12
(when the first Aeta girls start reproduction) to 17. The predicted
values are shown in SI Table 2. The regression equation is
After calculating m
x(H
α) (see SI Table 3) and survivorship to age x (l
x), we used Eq. 1
to calculate r (fitness) of hypothetical Aeta women beginning reproduction at different ages and heights. Because r
corrects for population growth, it also accounts for the effect of age
at first reproduction on generation length of each phenotype (r calculation in
SI Methods
).
where l
x is survival from birth to age x, α is age at maturity, and m
x(H
α) is one-half of the expected fertility at age x (i.e., it only includes number of female offspring) as a function of body size at maturity (H
α). Varying α and solving for r determines which age of maturity corresponds to higher fitness (18). We calculated m
x(H
α), or fertility as a function of particular
ages associated with attaining adult (reproductive) body height, using
logistic regressions that examine the hazards of live births by age and
height for parous women (see
SI Methods
), as follows:
Based on the Aeta data, the resulting equation was:
Fertility was then calculated for hypothetical women starting reproduction at different ages [i.e., we calculated m
x(H
α) for values of α from 11 to 39]. Size at
growth cessation was calculated for one year before birth of the
offspring, approximately corresponding to the beginning of pregnancy
(see
SI Methods
). The predicted height (H
α) of hypothetical women stopping growth at
different ages at maturity (α) was estimated through an extension of a
regression of height on age. The regression was calculated for ages 12
(when the first Aeta girls start reproduction) to 17. The predicted
values are shown in SI Table 2. The regression equation is
After calculating m
x(H
α) (see SI Table 3) and survivorship to age x (l
x), we used Eq. 1
to calculate r (fitness) of hypothetical Aeta women beginning reproduction at different ages and heights. Because r
corrects for population growth, it also accounts for the effect of age
at first reproduction on generation length of each phenotype (r calculation in
SI Methods
).Acknowledgments
We thank the University of the Philippines, the
Philippines National Commission on Indigenous Peoples, L. Dagsaan, J.
Eder, R. Foley, T. Headland, K. Hill, V. Paz, and C. Paz, J. Stock, and
R. Schlaepfer. We are very grateful to the editor and two anonymous
reviewers for useful comments and suggestions. This work was supported
by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, the
Parkes Foundation, the Evans Fund, the Crowther-Beynon Fund (A.B.M.),
and the Leverhulme Trust.
Footnotes
- *To whom correspondence should be addressed. E-mail: abm25@cam.ac.uk
-
Author contributions: A.B.M. and M.M.L. designed research; A.B.M. performed research; A.B.M., L.V., and M.M.L. analyzed data; and A.B.M., L.V., and M.M.L. wrote the paper.
-
The authors declare no conflict of interest.
-
This article is a PNAS Direct Submission.
-
This article contains supporting information online at www.pnas.org/cgi/content/full/0708024105/DC1.
- © 2007 by The National Academy of Sciences of the USA
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