PERSPECTIVES
killing was within or between groups is tricky
to ascertain (especially from archaeological
data) and varies among sites, but on average,
14% of adult deaths appear to have been due
to warfare. The extent of prehistoric genetic
differentiation is also difficult to estimate, but
based on genetic studies of extant huntergatherers, the model shows that a realistic
level of inbreeding within groups allows
10.1126/science.1175874
group benefits to offset fitness costs of
roughly 3% associated with being an “altruistic warrior” relative to nonaltruists. Ironically,
ANTHROPOLOGY
lethal hostility toward other groups could
thus underpin cooperation and support
within human communities.
The model does not account for
sex
differences, which might matter,
Ruth Mace
because females did not fight in wars,
Human social evolution is determined by demography.
were likely to join and reproduce with
the victorious group after conflict
nlike other animals, humans cooperate evolutionary outcomes not
[they may well have been the objective
with nonrelatives in coordinated act- seen in other animals (4).
of the conflict in the first place (6)],
ions, decorate their bodies, build comPerhaps the central differand were more likely, even in peaceplex artefacts (useful or otherwise), talk, and ence between genetic and cultime, to migrate out of their natal
divide themselves into linguistic groups. To tural transmission is that we
group to breed. The inheritance of the
understand the evolutionary basis of such can change our cultural phealtruistic traits is assumed to be vertibehaviors, anthropologists must consider not notype during our lives—for
cal and asexual, so the model could
only issues connected to social evolution in ani- example, to conform to group
work for a cultural trait (possibly even
mals, but also the implications of the possible norms. Cultural differences
better than for a genetic one). It is also
coevolution of genes and culture. Two articles between groups might be
possible that the measures of inbreedin this issue examine aspects of human social easier to maintain than are geing observed are maintained by culevolution: On page 1293, Bowles (1) investi- netic ones, due to processes
tural processes, such as language difgates the origins of altruism toward one’s own such as conformist social learnferences between groups. Nonethesocial group, while on page 1298, Powell et al. ing and punishment; several
less, Bowles suggests that the model
(2) study the emergence of cultural complexity. models show that if these procould theoretically apply to other socBased on empirical evidence and modeling, cesses occur, cultural group
ial animals. Zoologists, whose limited
both studies suggest that the demographic selection could explain the
tolerance of group selection rarely
structure of our ancestral populations deter- evolution of prosocial or altru- Technological and cul- extends beyond the human species,
tural complexity. So- will find this statement controversial;
mined how social evolution proceeded.
istic behavior (5).
phisticated tools such as
If, like me, you were brought up on The
Bowles now makes a more
but it is certainly not without the
these harpoons began
Selfish Gene (3), you learned that selection acts radical claim: that the demo- to emerge in the upper bounds of scientific possibility to test.
on individuals or genes, and you are trained to graphic structure of hunter- Paleolithic (between ca
Powell et al. address the evolube wary of group selectionist explanations for gatherer populations allowed 40,000 and 10,000 years tion of technological and cultural
behavior. Group selection is generally rejected group-selected genetic traits ago).
complexity—human behaviors that
as unimportant because even a tiny amount of to evolve in humans. He arhave left clear traces in the archaeomigration between groups quickly destroys the gues that lethal warfare was endemic and logical record. Traits such as the creation of
genetic differences needed for group selection that altruistic, group-beneficial behaviors abstract art, improvements in stone and
to act. But recent literature on social evolution that hurt the survival chances of individuals other tools, long-distance “trading,” and the
has reopened the debate, arguing that in some but improved the likelihood for groups to manufacture of musical instruments mark
circumstances group selection might be impor- win conflicts could emerge by group selec- the emergence of modern humans who
tant, especially in a cultural species like hu- tion. This argument was originally espoused behaved much as we do (see the figure).
mans. Genetic and cultural traits are both heri- by Darwin, but few formal tests of it have These material expressions of the modern
table and subject to evolutionary processes, been done.
condition emerged much later than did
but cultural traits are not transmitted in a
In his model, Bowles identifies two key anatomically modern humans. Some asMendelian way; they can be inherited from determinants of whether group selection can pects of behavioral modernity first apalmost anyone, including people who may not favor altruistic behavior: the individual and peared in southern Africa, possibly as early
share your genetic interests. This could lead to group costs and benefits of altruism in warfare, as 90,000 years ago, only to disappear again
and the extent of genetic differentiation among and reappear in Eurasia ~45,000 years ago.
groups. An array of ethnographic and archaeo- The timing of these events makes a biologiDepartment of Anthropology, University College London,
logical evidence shows that hunter-gatherers cal change in cognitive capacity a someTaviton Street, London WC1H 0BW, UK. E-mail: r.mace@
certainly did kill each other. How much of this what unlikely explanation.
ucl.ac.uk
References and Notes
1. C. Cecconi, E. A. Shank, C. Bustamante, S. Marqusee,
Science 309, 2057 (2005).
2. E. M. Puchner et al., Proc. Natl. Acad. Sci. U.S.A. 105,
13385 (2008).
3. J. P. Junker, F. Ziegler, M. Rief, Science 323, 633 (2009).
4. A. del Rio et al., Science 323, 638 (2009).
5. X. Zhang et al., Science 324, 1330 (2009).
6. J. E. Sadler, Annu. Rev. Biochem. 67, 395 (1998).
7. S. W. Schneider et al., Proc. Natl. Acad. Sci. U.S.A. 104,
7899 (2007).
8. G. G. Levy et al., Nature 413, 488 (2001).
9. H. M. Tsai, Blood 87, 4235 (1996).
10. C. P. Johnson, H. Y. Tang, C. Carag, D. W. Speicher, D. E.
Discher, Science 317, 663 (2007).
11. A. J. Engler, S. Sen, H. L. Sweeney, D. E. Discher, Cell
126, 677 (2006).
12. We thank A. Bausch and R. Netz for helpful comments on
the manuscript. We acknowledge funding through
Deutsche Forschungsgemeinschaft grant SFB 486 B9.
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CREDIT: THE LONDON ART ARCHIVE/ALAMY
U
PERSPECTIVES
ical evidence (8) that depopulation may have
occurred at the relevant time (around 70,000
to 60,000 years ago).
The model of Powell et al. only includes
selection on cultural traits, not on individuals
or populations. In the model, skills are
assumed to be transmitted because they are
beneficial. It is therefore possible that the
advantages of cultural skill acquisition caused
population density to increase, rather than
emerged as a response to it. This is an area for
further modeling. And, of course, Powell et al.
argue that the cognitive ability to learn these
skills was already present in all. Researchers
seeking genes involved in cognitive ability
would thus be unwise to base their evidence
on correlating geographic patterns of candidate genes with geographic patterns of the
emergence of culturally acquired skills—at
least not without paying careful attention to
demographic differences.
The two models (1, 2) paint rather different pictures of Pleistocene life. Were early
modern humans in frequent contact with
neighboring groups to exchange cultural
innovations, or were they inward looking,
unwilling to travel, and constantly engaging
their neighbors in lethal conflict? Probably
both, at different times and in different places
(although it may be possible to steal someone’s cultural innovations and kill them too).
Neither study claims that its model provides
the unequivocal explanation. Indeed, there
are many alternative explanations both for
altruistic behavior in human groups and for
the emergence of cultural modernity. Some
alternative explanations may be more due to
semantics than real differences in evolutionary processes (9), and some may work in
addition to the processes proposed here. But
by combining models with data, both studies
put their hypotheses firmly up the list of possibilities to be taken seriously.
References
1. S. Bowles, Science 324, 1293 (2009).
2. A. Powell, S. Shennan, M. G. Thomas, Science 324, 1298
(2009).
3. R. Dawkins, The Selfish Gene (Oxford Univ. Press, Oxford,
1976).
4. P. J. Richerson, R. Boyd, Not by Genes Alone: How Culture
Transformed Human Evolution (Univ. of Chicago Press,
Chicago/London, 2005).
5. R. Andrés Guzmán, C. Rodriguez-Sickert, R. Rowthorn,
Evol. Hum. Behav. 28, 112 (2007).
6. N. Chagnon, Yanomamo: The Fierce People (Holt,
Rinehart & Winston, New York, 1983).
7. J. Henrich, Am. Antiq. 69, 197 (2004).
8. S. H. Ambrose, J. Hum. Evol. 34, 623 (1998).
9. S. A. West, A. S. Griffin, A. Gardner, J. Evol. Biol. 21, 374
(2008).
10.1126/science.1175383
CELL BIOLOGY
The range of protective effects that a sirtuin
deacetylase affords to cells and organisms
under stressful conditions continues to grow.
Hypoxic Hookup
Leonard Guarente
ypoxia-inducible factors HIF-1α and
HIF-2α are homologous transcription
factors that activate an adaptive response in mammalian cells to low concentrations of environmental oxygen (1, 2). HIFactivated genes protect against damaging
reactive oxygen molecules generated by mitochondria in response to hypoxia, and also
stimulate erythrocyte proliferation and blood
vessel formation to enhance organism survival. Under normal oxygen conditions, HIF1α and HIF-2α are hydroxylated on key prolines, which promotes their degradation.
However, under hypoxic conditions, the HIF
proteins are stabilized and accumulate in
cells. On page 1289 of this issue, Dioum et al.
show that during hypoxia, HIF-2α is deacetylated and thereby activated by SIRT1, a nicotinamide adenine dinucleotide (NAD)–depend-
H
Paul F. Glenn Lab and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139,
USA. E-mail: leng@mit.edu
ent deacetylase (3). This finding extends the
reach of SIRT1 as a cell and tissue maintenance and anti-aging factor to include resistance to hypoxic stress. SIRT1 has already
been shown to protect against metabolic,
genotoxic, and heat stress by deacetylating
other key transcription factors that respond to
those stressors (4–8) (see the figure).
Dioum et al. show that in cultured mammalian cells, SIRT1 bound to and deacetylated
HIF-2α and activated the HIF-2α target genes
Sod2 (superoxide dismutase 2), VegfA (vascular
endothelial growth factor A), and Epo (erythropoietin). A catalytically inactive form of SIRT1
was unable to alter HIF-2α activity, indicating
the importance of HIF-2α deacetylation in the
activation mechanism. Mutating three lysines
of HIF-2α, which are acetylated, did not completely abolish activation by SIRT1. This indicates that other, unidentified lysines are important for HIF-2α regulation. It is not yet clear
whether additional deacetylases (histone deacetylases or SIRTs 2 to 7) also play important
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Published by AAAS
roles in HIF-2α activation. However, depletion
of SIRT1 alone increased the amount of acetylated HIF-2α during hypoxia, suggesting that
SIRT1 is the primary HIF-2α deacetylase.
The relationship between SIRT1 and HIF2α was also shown in biological settings. The
liver is the chief source of erythropoietin production during mid-gestation in mice. Embryos
lacking either Sirt1 or HIF-2α showed a defect
in erythropoietin expression in the liver during
this gestational period. Tail vein injection
of adenoviral expression vectors containing
Sirt1-encoding DNA along with vectors
encoding either HIF protein demonstrated the
potential of Sirt1 to activate HIF-2α, but not
HIF-1α, in the adult liver. And a viral vector
that triggered RNA interference of endogenous
Sirt1 reduced expression of the liver Epo gene.
Because HIF-2α is only stable under hypoxic conditions in the studies described,
Dioum et al. do not address whether SIRT1
itself is activated by hypoxia. This issue is
extremely relevant to possible roles for sirtuin
5 JUNE 2009
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Powell et al. now argue that changes in
population size and structure can explain the
patterns of acquisition (and loss) of culturally
inherited skills. The authors build on a model
by Henrich (7), who showed that small populations were more likely to lose complex
skills. Powell et al. examine a more realistically structured population, in which individuals live in groups (subpopulations) and
inherit (learn) skills from others in the group
or by contact due to migration between
groups. The results show that the time since
first occupation of a region is a far less reliable
predictor of the accumulation of cultural skills
than is the density of subpopulations and the
degree of migration between them.
The authors then use coalescent models (a
statistical approach assuming neutral traits
which are subject to drift) of genetic variation
in mitochondrial DNA to estimate prehistoric
population densities at various sites. The
resulting population density estimates are
compatible with those necessary to prompt
the onset of behavioral modernity at the
appropriate time in sub-Saharan Africa, and
then later in the Middle East. The genetic evidence cannot really help to explain the subsequent disappearance of these traits in subSaharan Africa, but there is some archaeolog-
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