NEWS & VIEWS RESEARCH
their home and day ranges to a circumscribedarea. The 87Sr/86Sr values seen in the male teeth
derive from a dolomite-rich region that is only
30 square kilometres in extent, distributed in anortheast–southwest direction. The minimum
distances from the caves to bedrock of differing ratios are only 2–3 km to the southeast and
5–6 km to the northwest. There are no barriers, yet the males stayed in the dolomitic areas,
apparently because their foods existed only insuch regions. Young females apparently fed inother, unspecified areas during tooth mineralization, and moved into the males’ region as
young adults for reproductive purposes.
These results have implications for understanding australopithecine diet, group size,
predator avoidance and home-range size.
Living primate species offer insights into thesevariables2. Among modern primate groups,
ecology influences the temporal and geographic patterns of exploitation of food items,group size and predator pressure, and all ofthese factors strongly influence group ranging
patterns. For example, leaf-eating primates havesmaller home ranges than fruit-eating primatesof the same body size. Body size and group size
influence when and where individual primateswould be vulnerable to predators.
Australopithecines lived in woodland savannahs, which provide tree foods and grass3. The
carbon stable isotope ratios (13C/12C) in tooth
enamel suggest that most of them ate both
foodstuffs, with some East African members
eating only grass4,5. Their tooth-enamel structure and its microscopic scratches and pits
imply that they also ate hard objects (seedsand nuts) or plant tubers and swollen stems6.
This diet contrasts with that of extant chimpanzees, which select only tree foods whenliving in savannah regions7. In such habitats,chimpanzees elude predators by avoiding open
areas, forming larger than normal groups, andcovering large home ranges3. For example, therange of chimpanzees at Ugalla, Tanzania3, issome 600 km2 in extent, much larger than the30 km2 proposed by Copeland et al.1 for theSouth African australopithecines. The small
home ranges suggested by the 87Sr/86Sr ratios
argue against australopithecines having targeted
only tree foods and in favour of their including amore ubiquitous food such as grass. Mountaingorillas8 feed on ubiquitous terrestrial vegetation in a home range of up to 25 km2, similar tothat suggested by the strontium isotope data formale australopithecines1. But male gorillas arevery large, thereby providing group protection,and they live in forest habitats without large
predators2. In contrast to the mountain gorilla,
the australopithecines lived in an open habitat,
had a smaller body size and faced many speciesof large carnivores. How did they avoid predation while eating grass in an open savannah?
For diet, the closest equivalent to that of
the australopithecines is found in the extant
baboon Theropithecus gelada and in its
giant fossil ancestor9, which had a body size

roughly equivalent to that of the australopithecines5 and which occupied the same ora similar habitat. Modern T. gelada are muchsmaller than either fossil group and practise
male philo­patry; they avoid predation in theiropen savannah habitat by living in bands up to60 strong, and have overlapping home rangesof sizes roughly equivalent to that estimatedfor the australopithecines (see referencesin ref. 2). But how could two large primate
species of similar body size, one quadrupedal(giant baboon) and the other bipedal (australopithecine), have co­existed? They would
have been competing with each other, as wellas with other fruit-eating animals, and withgrass-eaters such as pigs, hippos and zebra
ancestors, along with other ungulate species5.
How the australopithecines balanced predator
avoidance and the need to compete for foodremains an open question.
In Lewis Carroll’s flight of nonsensicalwhimsy, The Hunting of the Snark10, there is
the warning about the day that “your Snark bea Boojum!” — for the consequence of that isinstant disappearance. We are in the midst ofa fascinating hunt, but for us a Snark that turns
out to be a Boojum would mean success, notfailure. What is needed in this field of research
is for conjectures about the australopithecines
to vanish, instead of arising time and timeagain5,9. We must hope that continued investigation along the lines of Copeland and colleagues’ study1 will one day allow us to winnowaway some of that speculative thinking. ■Margaret J. Schoeninger is in theDepartment of Anthropology and the Centerfor the Advanced Research and Training inAnthropogeny, University of California at San
Diego, La Jolla, California 92093, USA.
e-mail: mjschoen@ucsd.edu.
1. Copeland, S. R. et al. Nature 474, 76–78 (2011).
2. Strier, K. B. Primate Behavioral Ecology 3rd edn(Allyn & Bacon, 2007).
3. Moore, J. J. in Topics in Primatology Vol. 1 (eds
Nishida, T. et al.) 99–118 (Univ. Tokyo Press, 1992).
4. Lee-Thorp, J. & Sponheimer, M. Am. J. Phys.
Anthropol. 131, Suppl. 43 Yb. Phys. Anthropol.
131–148 (2006).
5. Cerling, T. et al. Proc. Natl Acad. Sci. USA
doi:10.1073/pnas.1104627108 (2011).
6. Lucas, P. et al. BioEssays 30, 374–385 (2008).
7. Schoeninger, M. J., Moore, J. & Sept, J. M. Am. J.
Primatol. 49, 297–314 (1999).
8. Watts, D. P. Int. J. Primatol. 19, 651–680 (1998).
9. Jolly, C. J. Man 5, 5–26 (1970).
10. Carroll, L. The Hunting of the Snark: An Agony inEight Fits (Macmillan, 1898).

M O L EC UL A R E VOLU T I ON

Hidden diversity
sparks adaptation
Although some genetic mutations have clear effects, others have been considered
neutral and inconsequential. Such cryptic mutations can nonetheless facilitate
adaptation to new environments. See Letter p.92
JEREMY A. DRAGHI & JOSHUA B. PLOTKINI

s genetic variation primarily neutral, or isit predominantly shaped by natural selection? Biologists have debated this question
for decades. And although the neutralist–selectionist argument has fuelled advances in
our understanding of molecular evolution, ithas contributed less to our knowledge of howorganisms adapt to changing environments.
Recent theories about robustness and evolvability, as well as experiments with enzymes
and with microbes, suggest that adaptation
may depend on a deep and largely unappreciated interaction between neutral and beneficial mutations. On page 92 of this issue,
Hayden et al.1 describe an empirical test of thishypothesis.
When exposed to a new environment,a microbial population will rapidly adapt
through the emergence and fixation of bene­
ficial mutations2. Nevertheless, microbialevolution experiments have uncovered factors© 2011 Macmillan Publishers Limited. All rights reservedthat complicate this simple picture. One suchfactor, called epistasis — whereby the effects
of one mutation are modified by other mutations — explains why some populations adapt
faster or more predictably than others. These
differences in evolvability, or in the propensity
to produce beneficial mutations, account forseveral surprising results (such as the sudden
emergence of a major metabolic adaptation3 or
the long-term coexistence of lineages in a population4). The renewed interest in epistasis also
points to an exciting and constructive role forneutral mutations in the process of adaptation.
The key finding that links neutral mutations
to beneficial changes is that neutrality is often
conditional: a mutation may have no detectable effect when it arises in a given environment
and against a specific genetic background, butsubsequent changes to the environment or
genome may reveal hidden fitness effects5.
Theoretical work suggests that conditionallyneutral, or ‘cryptic’, mutations may accumulate within a population and later be expressed
2 J U N E 2 0 1 1 | VO L 4 7 4 | NAT U R E | 4 5

RESEARCH NEWS & VIEWSab New environment

Genotype–environment
interaction

Epistasis

Figure 1 | Role of cryptic genetic variation inadaptation. In this depiction, genotypes (nodes) are
separated by mutations (lines). Node size indicatesthe frequency of a genotype in the population, andbackground colour shows the phenotype in a given
environment. a, A population under selection
for the blue phenotype occupies a network ofequally fit genotypes. b, When the population ischallenged with a new selective environment (redbox), some of the previously neutral genotypes
may already express the adaptive phenotype(green). Adaptation to the new environment is also
facilitated by epistasis between a beneficial mutation(red) and a mutation that was neutral in the originalenvironment. Hayden et al.1 confirm that neutral
genetic variation accumulated in one environment
can facilitate adaptation to a novel environment,
either through interaction between genotype andthe environment or by epistasis.

after an environmental change, either directly
in response to the new environment6, or by epistatic interactions with subsequent mutations7(Fig. 1). Hayden et al.1 test this theory by direct
experimentation.
The authors evolved two populations of aribozyme (RNA enzyme) under selection foractivity with its native substrate; one population was subject to strong selection, the otherto weaker selection. The populations accumulated cryptic genetic variation that waslater revealed when they were challenged tocatalyse a different substrate. By measuring theincrease in catalytic activity over time in thisnew selective environment, Hayden and colleagues found that the rate of adaptation wasproportional to the amount of cryptic variation
present in each population. In other words,
cryptic genetic variation that had accumulated
in one environment facilitated adaptation to a
new environment.
This in vitro ribozyme system facilitates
precise measurements of genetic variation
throughout experiments. It also allows themutations responsible for adaptation to beidentified, sequenced and reconstructed in the
4 6 | NAT U R E | VO L 4 7 4 | 2 J U N E 2 0 1 1

ancestral ribozyme strain. To interrogate thegenetic basis of adaptation, Hayden et al. took
advantage of these features. They confirmedthat the beneficial genotypes arose from previously cryptic genetic variation, supporting acausal connection between neutral mutations
and adaptation.
The analysis1 further revealed a complex,
ecological dynamic: in one of the populations,the proper functioning of an evolved geno­type
depended on the presence of other geno­types
in the population. So by tracking population
variation through deep sequencing, theresearchers were able to capture a more detailed
picture of the underlying genetics and ecologythan is feasible in most evolution experiments
using organisms with large genomes.
Hayden et al.1 applied a very high per-basemutation rate to their short ribozyme sequence
to approximate the typical genomic mutation
rate of a living organism. But extrapolating
their results to real organisms is not straightforward, because there might be different
patterns of epistasis among the sites of a single
enzyme from those among the genes in a large
genome. Nevertheless, other work8–10 suggeststhat epistasis is prevalent at the genomic scale,and that novel environments reveal pre­viously
cryptic phenotypic variation in complex
organisms. Together with Hayden and colleagues’ work, these studies of natural populations suggest a general and important role forcryptic variation in determining a population’s
adaptive potential.
Sewall Wright, a vigorous proponent of theimportance of epistasis in evolution, presaged the modern view in his comment11 on
Kimura’s neutral theory: “Changes in wholly
nonfunctional parts of the molecule would be
the most frequent ones but would be unimportant, unless they occasionally give a basis forlater changes which improve function in thespecies in question which would then become
established by selection.” Indeed, Hayden
et al.1 have now verified that cryptic variation can shape the process of adaptation. We
can hope that future studies of this type will
elucidate the specific mechanisms by which
neutral mutations potentiate adaptation (seeref. 12, for instance), and so eventually lead toa quantitative understanding of a population’srate of adaptation.
As climate change brings organisms into
new environments and facilitates contact
between novel pathogens and humans, a comprehensive theory for how populations adapt
will have pay-offs for conservation and publichealth, as well as for our understanding of thediversity of life. ■Jeremy A. Draghi and Joshua B. Plotkin
are in the Department of Biology, Universityof Pennsylvania, Philadelphia, Pennsylvania
19104, USA.
e-mail: jplotkin@sas.upenn.edu
1. Hayden, E. J., Ferrada, E. & Wagner, A. Nature 474,
92–95 (2011).
2. Elena, S. F. & Lenski, R. E. Nature Rev. Genet. 4,457–469 (2003).
3. Blount, Z. D., Borland, C. Z. & Lenski, R. E. Proc. Natl
Acad. Sci. USA 105, 7899–7906 (2008).
4. Woods, R. J. et al. Science 331, 1433–1436 (2011).
5. Wagner, A. Robustness and Evolvability in Living
Systems (Princeton Univ. Press, 2005).
6. Hermisson, J. & Wagner, G. P. Genetics 168,2271–2284 (2004).
7. Draghi, J. A., Parsons, T. L., Wagner, G. P. & Plotkin,
J. B. Nature 463, 353–355 (2010).
8. Masel, J. & Trotter, M. V. Trends Genet. 26, 406–414(2010).
9. Schlichting, C. D. Ann. NY Acad. Sci. 1133, 187–203(2008).
10. Jarosz, D. F. & Lindquist, S. Science 330,1820–1824 (2010).
11. Provine , W. B. Sewall Wright and Evolutionary
Biology (Chicago Univ. Press, 1986).
12. Bloom, J. D., Labthavikul, S. T., Otey, C. R. & Arnold,
F. H. Proc. Natl Acad. Sci. USA 103, 5869–5874(2006).

C L I M ATE C HA NG E

Ancient Antarctic fjords
The East Antarctic ice sheet, the largest in the world, lies seemingly frozen intime. Discovery of a rugged landscape buried beneath the thick ice provides
evidence of a more dynamic past. See Letter p.72
S A N D R A PA S S C H I E R

Ice sheets reflect 90% of incoming solar
radiation and are of considerable mass,and hence affect Earth’s global geophysicalparameters. To gain insight into the mechanisms of the potentially long response times ofice sheets, it is necessary to study them from along-term geological perspective. In Antarctica, reconstructing ice-sheet drainage patterns
at times of past ice-sheet minima is a challenge:© 2011 Macmillan Publishers Limited. All rights reserved

today 98% of the continent is buried underseveral kilometres of ice. Airborne geophysical surveys that penetrate the ice have helped
to meet that challenge, and have contributed
significantly to what is known about Antarctica’s bed topography. In reconstructing thesubglacial topography of the deep Aurora Subglacial Basin in East Antarctica, Young et al.1
(page 72 of this issue) have made a notablediscovery by revealing subglacial landscapesin astonishing detail.