PERSPECTIVES
(below 1 Å) in TEAM I, which is equipped
with spherical and chromatic aberration correctors, was achieved with primary electrons
of 80 keV, which are much less damaging to
samples than the 300-keV electrons used in
(13). The use of correctors that can tolerate
objective lenses with larger gaps between
the pole pieces also enhances the free space
available for the specimen holders.
With the new level of performance demonstrated in this work, Yuk et al. have studied in detail various (and unexpected) stages
of the colloidal growth of Pt nanoparticles.
Open questions remain, such as the role of the
ligand molecules attached to the metallic species or how the first burst of electrons acts as
the seed of the nucleation process. The properties of nanoparticles are highly dependent
on their size, shape, and environment, and
such studies should provide insights that may
allow the design of homogeneous assemblies
of nanoparticles of defined sizes, morphology, and connectivity. Their approach opens
new domains of research in the physics and
chemistry in the fluid phase in general. How
this new generation of liquid cells will be useful for biochemical and biological problems,
where the use of microchip-based liquid cells
has not been fully exploited, in spite of the
spectacular advances recently shown for
imaging of whole biological cells in liquids
(14) is to be further explored.
References
1. R. Erni, M. D. Rossell, C. Kisielowski, U. Dahmen, Phys.
Rev. Lett. 102, 096101 (2009).
2. D. A. Muller et al., Science 319, 1073 (2008).
3. L. F. Zagonel et al., Nano Lett. 11, 568 (2011).
4. J. M. Yuk et al., Science 336, 61 (2012).
5. See http://ncem.lbl.gov/team/TEAMpage/TEAMpage.html.
6. N. de Jonge, F. M. Ross, Nat. Nanotechnol. 6, 695 (2011).
7. E. Ruska, Kolloid Z 100, 212 (1942).
8. J. M. Grogan, L. Rotkina, H. H. Bau, Phys. Rev. E Stat.
Nonlin. Soft Matter Phys. 83, 061405 (2011).
9. A. Radisic et al., Nano Lett. 6, 238 (2006).
10. K. Suenaga et al., Science 290, 2280 (2000).
11. T. Okazaki et al., Angew. Chem. Int. Ed. 50, 4853 (2011).
12. J. M. Yuk et al., Nano Lett. 11, 3290 (2011).
13. H. Zheng et al., Science 324, 1309 (2009).
14. N. de Jonge, D. B. Peckys, G. J. Kremers, D. W. Piston,
Proc. Natl. Acad. Sci. U.S.A. 106, 2159 (2009).
10.1126/science.1219835
ECOLOGY
How Bacterial Lineages Emerge
Bacterial speciation is driven by interplay
between natural selection, genetic linkage,
and lateral gene transfer.
R. Thane Papke and J. Peter Gogarten
M
ost people today recognize bacterial names like Escherichia coli
and Neisseria meningitidis. Yet,
from an evolutionary viewpoint, the clarity of
species labels for bacteria is blurred by rampant horizontal gene transfer between bacteria (1). The forces driving speciation in bacteria include niche adaptation, selective sweeps,
genetic drift, recombination of genetic material, and geographic isolation. How do those
forces maintain species homogeneity or bring
about lineages, when gene swapping is apparently so rife?
On page 48 of this issue, Shapiro et al. (2)
address these questions by providing a highresolution snapshot of early lineage divergence in marine bacteria. They find clues to
the dynamics of prokaryotic genomes, such
as with whom the organisms frequently
exchange genes, how lineages originate, and,
ultimately, what is (or is not) in a name.
Most theoretical and observational
insights into what species are and how they
came to be are derived from studies of sexually reproducing eukaryotes (3), in which
reproduction and recombination are necessarily connected. Asexual lineages in both
prokaryotes and eukaryotes have often been
described in terms of selection and genomewide genetic linkage, which resets to zero the
genetic diversity at every locus (4). However,
even though Bacteria and Archaea reproduce
Department of Molecular and Cell Biology, University of
Connecticut, Storrs, CT 06269–3125, USA. E-mail: thane@
uconn.edu; gogarten@uconn.edu
asexually, many prokaryotic populations
evolve in ways that resemble randomly mating, sexually reproducing eukaryotes: Alleles
in these bacterial populations are randomly
assorted among individual cells (strains), and
diversity at single loci can be purged independently of the other chromosomal loci.
The only mechanism that can explain
these observations is a high rate of horizon-
tal gene flow compared to the rates of clonal
expansion or reproduction. The main difference from eukaryotes is that prokaryotic
reproduction is independent of DNA acquisition and recombination. Instead, DNA is
obtained from fragmented chromosomes
obtained via parasexual means (that is, without reproduction). These mechanisms of
DNA exchange are not restricted to gene
exchange within species,
and therefore traits can and
J
J
do come from highly divergent organisms. For example, imagine that acacia trees
A
B
could exchange DNA with
lions and that the resulting
new tree developed “limbs”
B
that allowed them to attack
A
K
grazing giraffes. This is in a
sense what prokaryotes do
K
all the time. Very different
B
pathways for bacterial speciation have been described
A
(5, 6); often the data reveal
B
frequent gene flow within
A
C
multiple exchange groups.
Horizontal gene flow is
A structured exchange community. Members of two distinct niches are thus both a homogenizing
shown as green and orange squares; gray squares are relatives occupy- and a diversifying force. It
ing different niches. Genes that adapt their hosts to these niches are typically involves groups
mostly exchanged or recombined between members of the same niche
of organisms that preferen(green and orange arrows), but they might also be shared with recent
niche invaders (blue square), accelerating their adaptation to a new hab- tially exchange genetic mateitat. Other genes are freely exchanged between members of different rial. Mathematical models
niches (gray arrows). Shapiro et al. show that semi-stable adaptations of gene flow independent
to specific niches can emerge in the presence of high rates of gene flow of selection and based on
within and between lineages.
sequence similarity alone
www.sciencemag.org SCIENCE VOL 336 6 APRIL 2012
Published by AAAS
45
PERSPECTIVES
show that even when rates of relative homologous recombination to mutation are low [in
the range of 0.25 to 4 (7)], populations remain
recognizably coherent, indicating that selection is not required to give the appearance of
delineated species. However, such models
do not capture the complexity of gene flow
in natural populations. Genetic analysis of
closely related strains has shown that genes
rarely have the same phylogenetic history (8).
Shapiro et al. now examine the genomes
of 20 closely related, yet ecologically differentiated strains of Vibrio cyclitrophicus
adapted to living on various-sized particles in
the Atlantic Ocean. They find that 99% of the
core gene families (which are common to all
strains) have different evolutionary histories.
Thus, gene acquisition from other lineages,
selection on those adaptive alleles, and frequent intraspecies recombination unlinking
loci within V. cyclitrophicus have created a
thousand-organism chimera. A further indication of vast and frequent gene flow in these
asexual organisms comes from pairwise comparisons of genomes. The authors report that
in the time it took to accumulate a handful of
nucleotide polymorphisms in the core genes,
individuals gained reams of new DNA encoding proteins and enzymes that other cells in
the population did not have.
These astounding observations reiterate
that prokaryotic genomes can be extreme
mosaics caused by high rates of gene flow and
strong selection. When 99% of genes from a
population of very closely related strains do
not have the same common ancestor, the only
reasonable conclusion is that prokaryotic speciation does not have much to do with divergence from common ancestors—a startling
anti-Darwinian outcome.
Surprisingly, in terms of evolutionary outcomes, prokaryotes tend to resemble Darwin’s finches. Finches from different species
coexisting on the same island become more
similar to one another in their overall genome
through frequent introgression (incorporation
of genetic material via repeated backcrossing
of an interspecific hybrid), but the characters
defining their ecological niche appear to be
maintained through selection.
Genetic exchange groups appear to be the
basis of many lineages observed in prokaryotes and are initiated or extinguished by sharing a common spatiotemporal existence with
other exchange groups (9, 10). Exchange
groups can degenerate through movement to
a new habitat or geographic location, or by
any mechanism that generates “sexual” isolation, including illegitimately recombined loci
(11) and the molecular machinery that shuttles DNA between cells. Perhaps a common
46
mechanism for biasing gene exchange and
generating “sexual” isolation is quorum sensing. Many prokaryotes, including pathogens,
soil, and marine dwellers, use quorum sensing to regulate gene exchange (12): They only
exchange DNA when their numbers dominate in any particular place and time—for
example, in a biofilm (13). Quorum sensing
is also used by Vibrio populations in biofilms
to regulate gene exchange (14). But gene flow
regulation does not prohibit divergent DNA
from entering or recombining, and exchange
groups may be as numerous as potential
niches and geographic locations allow.
As Shapiro et al. show, the habitat-specialized Vibrio strains of their study have a
gene and niche bias for genetic exchange.
Loci that are less important for niche adaptation participate in different and more diverse
exchange groups (see the figure). It would
seem that the genetic exchange group that
has dominated a bacterial population most
recently will determine how we observers
interpret their evolutionary history of divergence—hopefully while realizing the possibility that newly acquired exchange partners
purge evidence of past ones (9, 10). Instead
of prokaryotic species having common
ancestors, it seems that they are each more
like emergent ports-of-call, defined by which
genetic vessels are currently moored in their
chromosomal harbors.
References
1. W. P. Hanage, C. Fraser, B. G. Spratt, BMC Biol. 3, 6 (2005).
2. B. J. Shapiro et al., Science 336, 48 (2012).
3. J. A. Coyne, H. A. Orr, Speciation (Sinauer, Sunderland,
MA, 2004).
4. J. F. Crow, M. Kimura, Am. Nat. 99, 439 (1965).
5. D. Gevers et al., Nat. Rev. Microbiol. 3, 733 (2005).
6. W. F. Doolittle, O. Zhaxybayeva, Genome Res. 19, 744
(2009).
7. C. Fraser et al., Science 315, 476 (2007).
8. R. T. Papke et al., Proc. Natl. Acad. Sci. U.S.A. 104,
14092 (2007).
9. O. Zhaxybayeva et al., Genome Biol. Evol. 1, 325 (2009).
10. O. Zhaxybayeva et al., Proc. Natl. Acad. Sci. U.S.A. 106,
5865 (2009).
11. A. C. Retchless, J. G. Lawrence, Science 317, 1093
(2007).
12. L. S. Havarstein, D. A. Morrison, in Cell-Cell Signaling
in Bacteria, G. M. Dunny, S. C. Winans, Eds. (American
Society for Microbiology, Washington, DC, 1999).
13. Y. H. Li et al., J. Bacteriol. 184, 2699 (2002).
14. K. L. Meibom et al., Science 310, 1824 (2005).
10.1126/science.1219241
PALEONTOLOGY
Reading Pliocene Bones
Jackson Njau
Standardized criteria will help to reliably distinguish marks made by hominid tools from feeding
traces of other animals.
T
he human ability to make complex
tools is unparalleled in the animal
kingdom and is a key character of
Homo sapiens. Flaked stone tools and cutmarked bones are the first traces of this
behavior. Yet the interpretation of bone modifications is complicated by similar traces
left, for example, by carnivorous animals
(see the figure). Given the scarcity of butchered bones from the Pliocene (5.3 to 2.6 million years ago) and Early Pleistocene (2.6 to
0.76 million years ago), even a single misidentification can have profound effects on
the interpretation of early hominid behavior.
How can such misidentification be avoided?
The current consensus is that the world’s
oldest tools and associated butchered bones
come from Gona, Ethiopia, dated to 2.6 million years ago (1, 2). This early technology,
termed Oldowan, has also been found elseDepartment of Geological Sciences, Indiana University,
Bloomington, IN 47405, USA. E-mail: jknjau@indiana.edu
where in Africa but did not extend beyond
this continent until about 2 million years
ago. Although there is one report of butchered bones 3.4 million years old from
Dikika, Ethiopia (3), this evidence has been
disputed (4), in part because tools older than
2.6 million years have yet to be found anywhere, despite intensive searching in older
African sediments during the past 40 years.
By the mid-19th century, scientists had
begun to recognize cut marks, associated
with worked flints, on the bones of extinct
Pleistocene animals ( 5). These physical traces were correctly attributed to past
human butchery, but the importance of bone
modification was not recognized until a century later, after a surge of hominid discoveries in eastern Africa. Major excavations at
sites such as Olduvai Gorge, where associated stone artifacts and fossils were recovered, led archaeologists to speculate that by
2 million years ago, hominids were hunting
and butchering at home bases (6). Others
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