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Evolution on a Frozen Continent
Ancient-DNA studies of Adélie penguins combined with a detailed picture of a
remarkable continent’s geological past provide a window on evolution
David Lambert, Craig Millar, Siva Swaminathan and Carlo Baroni
A
fundamental idea in evolutionary
biology is that animals are adapted
to the environments in which they live,
yet environments are unstable, and as
environments change, animal populations respond to that change. From
parasites in the gut of vertebrates, to
marine animals that live in the deepest
tropical oceans, to terrestrial animals
that live below ground, species manage
to persist and eke out a living.
No environment is more harsh than
Antarctica. During winter the continent and the seas surrounding it are
dark 24 hours a day, and air temperatures are typically lower than –40 degrees Celsius. During that time Adélie
penguins (Pygoscelis adeliae) live on
ice floes off the coast of this huge and
dramatic continent. When summer arrives, there are 24 hours of daylight
and life becomes easier, but mean temperatures can still be –20 degrees Celsius. Penguins then come ashore on
the continent to construct nests, mate,
David Lambert is professor of evolutionary
biology at Griffith University in Australia. He
received his Ph.D. at the University of the Witwatersrand in Johannesburg. Craig Millar earned
his Ph.D. from the University of Auckland where
he is a senior lecturer in the School of Biological
Sciences. He is a principal investigator in New
Zealand’s Allan Wilson Centre for Molecular
Ecology and Evolution. Siva Swaminathan
received his Ph.D. from Jawaharlal Nehru University in India and is currently a senior scientist
and head of the Biotechnology Division at the
Environment Protection Training and Research
Institute, Hyderabad. Carlo Baroni is professor of
geomorphology at the University of Pisa where he
teaches applied geomorphology and geoarchaeology. Address for Lambert: Griffith University,
170 Kessels Road, Nathan, Qld 4111, Australia.
Email: [email protected]
386 American Scientist, Volume 98
raise their chicks and finally return to
the sea. The appropriateness of Adélie
penguins to their conditions of life is
obvious. For example, their hydrodynamic body shape is very similar to
that of seals and is well suited to the
marine environment in which both animals live. Physiological and metabolic
adaptations enable them to withstand
the very cold temperatures of their terrestrial and aquatic environments.
However, we know that when environments change—for example, when
temperatures increase or decrease—
many animal species, rather than adapt
to their new conditions, simply move
to stay within their preferred temperature limits. When times were colder
than they are now, such as in the cold
phases of the Pleistocene period (2.5
million to 11,700 years ago), it seems
that the Antarctic might not have been
a good place for an Adélie penguin to
live. Nearly all of Antarctica would
have been covered in snow and ice
and because Adélies breed only in icefree areas, the usable breeding grounds
for the species would have been very
restricted. There is no evidence that
Adélie penguins moved in response to
this altered environment and went to
warmer, ice-free areas to breed, as we
might expect.
In a world increasingly concerned
with global climate change and particularly the likelihood of rising average temperatures, spare a thought for
Adélie penguins. Only the emperor
penguin and the Adélie nest solely on
the Antarctic continent or islands close
to it, and the Adélie is the one penguin
that breeds only on ice-free areas of the
continent. (The emperor breeds on the
ice itself.) Other species, such as the
closely related chinstrap and gentoo,
breed mainly on sub-Antarctic islands.
If global temperatures increase, Adélie
penguins will not be able to simply
migrate to a colder part of the continent—they will have nowhere to go
because they already live in the coldest
place on Earth. This makes the Adélie
penguin an ideal species for studying
adaptive evolution in the context of
global climate change.
Pleistocene Antarctica
In Antarctica, the Pleistocene epoch
was distinguished by the repeated
expansion and collapse of huge
marine-based ice sheets (thick floating
platforms of ice that form where
glaciers project into the sea), as well as
by fluctuations in the volume of ice on
the Antarctic landmass. These changes
would have certainly caused largescale disruptions to animal habitats
and populations. Adélie penguins
generally breed in large colonies on
ice-free areas close to the sea. For
Figure 1. Cape Adare at the mouth of the
Ross Sea hosts the largest colony of Adélie
penguins in Antarctica, comprising about
220,000 breading pairs. Adélie penguin rookeries offer a singular laboratory for DNA
studies ancient and modern. Successive generations return to the same breeding site,
usually to within hundreds of yards of their
birthplace. The harsh conditions and heavy
predation encountered by the penguins result in a deep record of remains, and the remains are uniquely preserved in the cold, dry
conditions of the Antarctic. Adélie penguins
breed on the bones of their ancestors, and by
comparing serially preserved, precisely dated
samples across time, scientists are deriving
new insights about the tempo and mode
of evolution. (Photograph courtesy of John
Macdonald.)
www.americanscientist.org
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Figure 2. Adélie penguins are distributed sporadically along the entire Antarctic coast and
some nearby islands, with a total population of about 5 million birds. Overall their requirements for acceptable habitat are rather narrow. The formation of too much pack ice can
make the migration to breeding grounds unacceptably long; too little ice can disrupt their
hunting patterns during the nonbreeding season. For nesting, they require that the ground
be free of ice.
example, Ross Island, situated at the
edge of the Ross Ice Shelf, is presently
home to several hundred thousand
breeding pairs of birds. In Antarctica,
even small fluctuations in the volume
of ice can have a significant impact
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on the number and extent of ice-free
areas. At the Last Glacial Maximum
(LGM, about 25,000–18,000 years
ago), the entire Ross Sea coastline
was uninhabitable to Adélie penguins
because of the extent of the Ross Ice
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Shelf; Ross Island itself was almost
900 kilometers inland from the edge
of the ice and the open sea. Such
glacial events undoubtedly influenced
penguin abundance, distribution and
genetic diversity.
As suggested by the observations of
Robert F. Scott at the beginning of the
last century, Antarctica during the LGM
was covered by an expanded ice sheet
advancing onto the continental shelf,
and coastal areas were buried by hundred of meters of ice. In the Ross Embayment, the coastline became ice-free
only about 8,000 years ago, after the retreat of the LGM ice sheets and of their
fringing ice shelves. Moraines are deposits of soil and rock debris left behind
by retreating glaciers; their locations in
ice-free areas document fluctuations in
the extent of glaciers. On the low, rocky
coastlines of the Ross Sea, raised beaches and marine terraces of the Holocene
epoch (reaching back from the present
to about 11,000 years ago) resulted from
sea-level changes caused by the large
amounts of water released by retreating ice sheets, together with isostatic
rebound, the rise of land masses previously depressed by the huge weight of
the ice during the LGM of the Antarctic
coastal belt.
Up to the Holocene
Adélie penguins are the dominant
terrestrial species in Antarctica. They
have been described by ecologist
David G. Ainley as a bellwether
of climate change, in part because
they are adapted to a narrow habitat
optimum between too much sea ice
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Figure 3. The breeding season for Adélie penguins on Ross Island begins in late October, the start of the Antarctic spring. During the other
seasons of the year they likely travel as far as a few hundred kilometers north of the Antarctic continental shores before returning to their
breeding grounds. Colonies range in size from a few dozen pairs to over 200,000. Female Adélies lay two eggs, and then both parents share
388 American Scientist, Volume 98
and not enough. Certainly Adélies
have lived through many dramatic
changes in temperature. Over the
past two million years there has been
a series of ice ages in Antarctica and
elsewhere. Evidence of these events,
directly preserved in the East Antarctic
Ice Sheet and described in our work
and that of others, indicates that ice
ages occurred regularly every 41,000
years in the early Pleistocene and
about every 100,000 years since 430,000
years ago. During the last glacialinterglacial transition (circa 18,000–
12,000 years ago), climate change in
the Antarctic was the most extreme on
Earth, with the average temperature
rising by about 13 degrees Celsius, as
documented by ice cores. Since that
period Adélie penguins have been
numerous in Antarctica, both in terms
of total biomass and of the numbers
of breeding individuals. David Ainley
estimates that the current population
of Adélie penguins is about 5 million
individuals.
Adélies breed in colonies at ice-free
sites around the coast of Antarctica
and on some islands off the Antarctic coastline. On the continent these
colonies have a patchy distribution,
presumably in part at least because
of the criteria the birds use to identify breeding sites. Adélie penguins
construct their nests from pebbles of
a very specific size range. In areas
where meltwater may wash over the
breeding grounds, the nesting stones
act to keep the developing eggs and
chicks above the surface where they
can remain dry. Ainley has identified
Figure 4. Adélie penguin rookeries are sites of considerable carnage. Predators include leopard seals, killer whales, and skuas, which are sturdy gulls that prey on eggs in the nest and
chicks left vulnerable by inattentive parents. (Photograph courtesy of Carlos Olavarria.)
common features of Adélie breeding
colonies, including close proximity to
pack ice during the winter and early
spring, and accessibility to the sea by
walking during summer. In 1915 the
British explorer George Levick noted
the apparent importance of locations
in which high winds were common,
suggesting that the winds swept the
ground and pebbles of snow. Adélie
penguin colonies vary hugely in size,
from less than 100 individuals to the
largest colony in Antarctica at Cape
Adare. This colony lies at the mouth
of the Ross Sea and comprises about
220,000 breeding pairs (as reported in
a personal communication from Phil
Lyver, zoologist with New Zealand’s
Landcare Research organization). Currently there are 24 known breeding
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the chores of incubating the eggs and foraging for food. (Photographs courtesy of Yvette
Wharton (b, c, d) and Brian Karl (e, f).
www.americanscientist.org
colonies along the coast of the Ross
Sea and a large number of abandoned
rookeries between Terra Nova Bay and
Ross Island.
Adélie penguins begin a regular annual cycle of breeding during the Antarctic spring, with males typically arriving at Ross Island colony sites in the last
week of October and early November,
on average four days earlier than females. Adélie penguins are generally
monogamous. Males typically begin
breeding at 5 to 7 years, females at 4
to 6 years. In mid November, females
usually lay two eggs and then leave
to feed at sea for 8 to 14 days. During
that period, males incubate the eggs.
The adults then change places and the
nonincubating bird returns to the sea
to feed.
High breeding-site fidelity is characteristic of the species. According to
data collected by Ainley, 96 percent
of breeding birds have been recorded
nesting at their natal colony and 77
percent bred within 100 meters of their
natal site. However, it is clear that environmental conditions can dramatically interfere with this generally high
level of return. For example, the ability
of adults to feed at sea and provide
sustenance for their growing chicks
can be disrupted by massive icebergs,
which if grounded near breeding colonies may greatly increase the distance
adults must travel to find open sea.
As chicks get older they are recognised by their parents, and after about
three weeks they begin to leave the nest
and mix with other chicks in the colony.
Chicks become independent of the nest
at this crèche stage. The larger size of
2010 September–October 389
chicks at this time requires both parents
to forage at sea. On returning, parents
are able to recognise their chicks among
the large number of juveniles in the
crèche by their calls. Chicks eventually
fledge in early February.
During the breeding season, colonies are grim places in which predation of eggs and chicks occurs at high
levels. Adélie penguin remains lie on
the ground for seasons and are well
preserved by the cold, dry Antarctic
climate until they are eventually bur-
ied by the remains of new nests and
other deposits. Penguin guano seeps
through the permeable, pebbly nests
and accumulates at their bases. Each
successive occupation of a colony creates a layer made from nest pebbles,
penguin remains and guano to form ornithogenic soils. The extent and thickness of these organic layers is a function of the size, age and persistence of
the colony—the older the colony, the
thicker the accumulation of pebbles
and guano. Hence, ornithogenic soils
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Figure 5. Under the pebbly ground of Antarctica can be found a well-developed stratigraphic
record of Adélie penguin colonies. Careful archaeological excavation reveals layers of guano,
bones, eggshell fragments, and dietary remains such as fish bones and squid beaks. From
these a highly detailed record of radiocarbon-dated remains has been assembled. (Photograph
courtesy of Carlo Baroni.)
390 American Scientist, Volume 98
contain a well-developed stratigraphic record of Adélie penguin colonies:
guano, bones, eggshell fragments and
dietary remains (fish otoliths, bones
and teeth, and squid beaks).
Members of our research team regularly excavate ancient colonies to recover these precious remains for radiocarbon dating and DNA analysis.
Hundreds of such radiocarbon-dated
penguin remains collected from ornithogenic soils document the past availability of ice-free coastal sites suitable
for nesting and breeding. Along the
Victoria Land coast, two recent sets of
radiocarbon dates indicate a Late Pleistocene occupation at about 45,000 to
25,000 years ago and a later Holocene
recolonization of these coastal areas.
Furthermore, dates from ornithogenic
soils, together with other datable organic materials, provide data for reconstructing the retreat of glaciers in
coastal areas after the LGM and the
subsequent emersion of coastline starting about 8,000 years ago during the
Holocene period.
Ornithogenic soils in the vicinity of
currently occupied colonies suggest
that the penguin population expanded
and contracted repeatedly during the
Holocene. Abandoned nests are easily
identifiable as accumulations of wellsorted pebbles. After the abandonment
of these breeding sites, scouring winds
leave a concentration of pebbles at the
surface that protects the guano layers
below from erosion.
Abandoned penguin nesting sites in
areas where Adélies do not currently
nest have been recognized as relict
colonies and are common landscape
features along the Antarctic coasts.
The accurate geomorphologic survey
of ice-free areas led to the discovery
of tens of relict colonies. Applying the
usual techniques of archaeological research, such as precise stratigraphic
excavation of penguin settlements, we
have been able to identify phases of
occupation and abandonment of the
relict colonies, with the phases separated by mineral layers such as aeolian
deposits, sand and gravel of colluvial
or periglacial origin, and so on. From
these data we are able to reconstruct
the history of penguin populations.
In the Ross Sea area, penguin recolonization is intimately associated
with elephant seal (Mirounga leonina)
presence and distribution related to
warmer-than-present conditions in the
area. After the deglaciation and until
about 4,000 years ago, the two species coexisted along the Victoria Land
coast, indicating that there was less sea
ice than at present, a state preferred
by elephant seals, but still sufficient
regional pack ice for Adélie penguins.
The period between 4,500 and 2,500
years ago registered the ‘‘penguin optimum,’’ a period of particularly favorable environmental conditions for
penguins (perhaps because an increase
in pack ice resulted in more favorable
foraging ecology). During this period
there was a more extensive settlement
of these coastal areas by penguins.
Now there are fewer penguin colonies,
a reduction associated with a decline
in the populations of elephant seals.
The sudden decrease of penguin colonies and populations occurred approximately 2,500 years ago.
Between 2,300 and 1,100 years ago,
the establishment and persistence of
sub-Antarctic climatic and environmental conditions inhibited the establishment of Adélie penguin colonies,
as documented by the contemporary
spreading of elephant seals. This period
represents the greatest sea-ice decline
(and probably the warmest ocean and
air temperatures) in the Ross Sea in the
last 8,000 years. In the last 1,000 years,
penguins populations expanded again
and elephant seals abandoned the area.
to measure the rate at which the
changes in DNA occurred. To put the
importance of the rate measurement in
context, we might say that measuring
the speed of evolution is as important
to biologists as measuring the speed
of light was for physicists. Knowing
how fast DNA changes over time has
relevance for many disciplines from
forensics and evolutionary biology
to taxonomy. It enables biologists
to calibrate the timing of important
evolutionary events in the history of
life and more generally to provide
a ”clock” for evolution itself. So, for
example, if one compares DNA from
modern (living) individuals and those
that lived 1,000 years ago, 2,000 years
ago and so on, the changes over these
time periods can reveal the speed—
and potentially even something about
the nature—of evolution itself. But
to do this analysis, we need serially
preserved samples of precisely known
age from which ancient DNA can be
recovered. Samples from living animals
of the same species—from time zero
if you like—are also necessary. The
woolly mammoth and Neanderthals
are not suitable subjects for such
evolutionary studies because no
modern populations of these species
exist. And of course ancient DNA is
not available for all species. DNA is
best preserved in low temperatures
and dry conditions. Species that live
in equatorial regions and those that
inhabit wet environments are unlikely
Clocking Evolution
This detailed picture of the glacial
history of Antarctica and changes in
the number and distribution
of Adélie penguins provides
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the necessary backdrop for our
investigation of evolution itself.
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In principle, by comparing
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genomic regions in individuals
of one species that lived at
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possible to determine what
evolutionary changes have
occurred over time and then
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Figure 6. The maps show the distribution of Adélie penguin colonies across
the Ross Sea over time. Changes in
temperature and ice conditions affect
the suitability of the environment
for both Adélies and their ecological
rivals, elephant seals. Applying the
techniques commonly used in archaeological research, as shown in figure 5,
it has been possible to identify phases
of colonization, abandonment, and
recolonization in the ornithogenic soil
of excavated strata.
www.americanscientist.org
to be good targets for such work.
Therefore it is not surprising that much
ancient-DNA research has focused on
animal species inhabiting the polar
and temperate regions. These studies
have dramatically improved our
estimates of rates of molecular change,
our understanding of the biology of
ancient populations and our estimation
of the amount of genetic variation that
has been lost or gained in these species
over time.
Evolution consists of changes in the
genome, some in DNA regions under
selective control, others in neutral sequences. Many evolutionary studies
concentrate on neutral sequences because those under selective control are
responsive to episodic environmental
changes and are unlikely to change at
a constant rate.
Evolution occurs in the mitochondrial genome as well as the nuclear
genome. Mitochondrial DNA has been
a prime target for ancient DNA studies
because there are hundreds to thousands of copies of mitochondrial DNA
present in each cell, versus one copy of
the nuclear genome; because the rates
of mitochondrial DNA change are typically high; and because ancient mitochondrial DNA sequences can be up to
300 base pairs long, whereas nuclear
sequences are virtually never longer
than 150 base pairs. Nevertheless, owing to the extraordinary quality of ancient Adélie penguin DNA preserved
in the cold dry storage of the Antarc-
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Figure 7. Most ancient DNA studies focus on mitochondrial DNA, which occurs in many copies in each cell and offers longer DNA segments
in ancient samples. However, biological material is uniquely well preserved in the cold, dry Antarctic, making it possible to do comparative
studies of ancient DNA using nuclear genetic material. Allele frequencies for nine nuclear microsatellite DNA loci are shown above. Matching
alleles have the same color. The sizes of each wedge of a particular color show the difference in allele frequency in modern (top) and ancient
(bottom) samples. White and gray wedges are private alleles, those present only in the modern or ancient samples.
Subfossil bones from this population
were excavated using a stratigraphic
method that allowed the identification
of individuals even within the same
layer. After comparing the allele frequencies in the ancient population
with those recorded from the modern
population at the same site in Antarctica, we reported significant changes in
the frequencies of alleles at four of the
nine loci we examined, demonstrating microevolutionary change over the
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tic, we were encouraged to attempt to
reconstruct a sample of nuclear gene
loci using subfossil remains of breeding birds from Inexpressible Island in
the Ross Sea. Using nine nuclear microsatellite DNA loci (microsatellites
are sequences of a few repeating base
pairs of DNA), we genotyped an ancient population of Adélie penguins
from a single stratigraphic layer using two radiocarbon-dated bones aged
6,082 ± 55 years and 6,092 ± 60 years.
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approximately 6,000-year period. This
outcome was the first demonstration
of a change in the frequency of alleles
in the nuclear genome over such a geological time frame.
Because most microsatellite DNA
loci are noncoding, natural selection is
unlikely to have significant influence
on the evolution of such genes. From
the findings of a large number of excavations carried out in the Adélie penguin colony at Inexpressible Island, it
appears that this population has been
large over the 6,000-year period of this
study. However, we cannot exclude
the possibility that population bottlenecks may have occurred during this
time that significantly affected gene
frequency changes.
Figure 8. The rates of evolution of mitochondrial DNA were calculated using three different statistical methods (red, yellow and blue
bars). The error bars indicate 95 percent confidence intervals. Overall, the evolution rates
were higher than most previous estimates.
This higher rate held both for synonymous
positions, for which nucleotide substitutions
do not change the amino acid sequence of the
gene product, and for nonsynonymous positions, in which substitions affect the gene
product and possibly fitness of the organism.
Studies of mutation rates in modern samples
and longer-term molecular rates of change in
ancient and modern samples contribute to
our understanding of how genetic variation
arises and how it is retained in the allelic
endowment of the population.
Unlike other genetic markers that
typically mutate by single nucleotide
changes, the predominant type of mutation for microsatellite DNA loci is
changes in the lengths of their repeat
tracts, which arise due to slippage
during replication and to unequal
exchange of genetic material during
recombination. Certainly it is widely
recognised that microsatellite DNA alleles tend to increase in length over
time, at least when alleles are short and
phylogenetically young. Consequently,
we compared the length of alleles in
ancient and modern populations and
showed that the ancient population
has significantly shorter microsatellite
DNA alleles at four of the nine loci
examined. Three of the remaining loci
showed longer alleles in the modern
population, although the differences
were too small to be statistically significant. In addition, the ancient population is characterised by short private
alleles (alleles that are unique to a population) whereas the modern population reveals a larger number of private
alleles that are generally among the
longest variants at each locus. This
result suggests that we have identified the mutational processes—errors
during DNA replication that result in
length changes—that have contributed
to the microevolutionary change we
detected.
In addition to our findings about
nuclear DNA, we have been able to
estimate rates of molecular change by
studying changes in mitochondrial
DNA sequences using many serially
preserved subfossil remains of Adélie
penguins. The rates we derived are
higher than many other previous estimates, yet they are generally robust
to different methods of analysis. The
rate of molecular evolution of the HVR
I region, determined using DNA sequences from 162 subfossil bones of
known age spanning a 37,000-year period, was 0.86 substitutions per site per
million years (with a 95 percent confidence interval of 0.53 and 1.17).
We have also recently been able
to sequence complete mitochondrial
genomes of Adélie penguins up to
44,000 years old. Using these data,
we have been able to estimate rates of
molecular change for the entire mitochondrial genome, as well as rates for
components of the genome, such as
sequences coding for transfer RNAs
and ribosomal RNAs, as well as protein-coding regions. For the latter,
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we have been able to determine rates
for synonymous sites (the variations
found do not change the amino-acid
sequences of the coded proteins) and
nonsynonymous sites (the amino acid
sequences coded by the alleles are different). These rates are all generally
high, indicating a rapid rate of molecular evolution over geological time.
Direct observations of mutation
rates (obtained by studying modern
samples) and longer-term molecular
rates of change (obtained by comparing modern and ancient DNA) will
help us understand how fast genetic
variation arises and how fastidiously
it is preserved. Are the two related?
Perhaps the high evolutionary rates
we discovered are elevated because
of high mutation rates? We have been
able to study both mutational and
evolutionary processes using Adélie penguins as a model organism.
By taking blood samples from adult
breeding birds and their chicks, we
have been able to detect new mutations and to analyze whether they are
germline mutations inherited across
generations. Our results have been
surprising. We sequenced DNA from
the mitochondrial HVR I region from
penguins comprising a large number of penguin families. Our sample
consisted of more than 900 chicks and
both parents of each chick. We recorded a total of 62 germline heteroplasmic
mutations (those in which two DNA
variants were recorded at the same
position in the mitochondrial genome
within the same individual) in these
families. These variants were detected
in mothers and also in their offspring,
consistent with maternal inheritance.
The data give an estimated mutation
rate of 0.55 mutations per site per million years (95 percent confidence interval of 0.29 and 0.88) after accounting
for the persistence of these heteroplasmies and the sensitivity of current detection methods. Importantly, this rate
is not significantly different from rates
of evolutionary change we have estimated using serially preserved subfossil remains of Adélie penguins. This
study suggests that molecular rates of
change—either mutational rates occurring between successive generations,
or evolutionary changes over much
longer periods—are essentially no different. The challenge now is to recover
much longer regions of the nuclear genome and to focus on regions that may
help these remarkable birds respond to
the challenges they will encounter in
the face of a changing climate.
Playing on the famous metaphor
of ecologist George Evelyn Hutchinson, the frozen continent of Antarctica
is a remarkable “ecological theater”
in which Adélie penguins are central
characters performing in an “evolutionary play.” As the nature of the theater changes with every ice age, or in
our case with every interglacial warming period, the storyline of the play
changes. But will it always do so? As
the planet warms, Adélie penguins
have nowhere colder to go to escape
the change. They must either adapt or
perish. Researchers can expect to read
the script of this drama in the allelic
variations of the penguins’ DNA.
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2010 September–October 393