E VO L U T I O N
PERSPECTIVES
An Eocene Big Bang for Bats
Nancy B. Simmons
ats, the only mammals capable of pow-
B ered flight, constitute more than 20% of
living mammal species (1). Unlike
birds and other terrestrial vertebrates, most
bats use echolocation—a biological form of
sonar—to locate and track their prey (2). Bats
are found on every
Enhanced online at continent except
www.sciencemag.org/cgi/ Antarctica, and they
content/full/307/5709/527 exploit a wide vari-
ety of food sources
including insects, small vertebrates, fruit,
nectar, pollen, and even blood (1–3). More
than 110 bat species may coexist in some eco-
logical communities, a number that far
exceeds that of any other mammalian group
(1, 3). Despite their prominent position
among mammals, the evolutionary history of
bats is largely unknown because of a limited
fossil record and incomplete phylogenies. On
page 580 of this issue, Teeling et al. (4) pro-
vide a new evolutionary tree for bats that
helps to explain how, when, and where this
extraordinary diversity may have originated.
Living bats are classified into 18 fami-
lies on the basis of shared anatomical spe-
cializations and echolocation habits (see
the figure), and another six families are
known from fossils (1, 5, 6). Although biol-
ogists have long agreed that these groups
represent distinct evolutionary lineages,
there has been no consensus concerning
relationships among them. The lack of a
well-resolved phylogeny (evolutionary
tree) for bats has hindered attempts to
understand the origins of major specializa-
tions in these mammals, and has compli-
cated efforts to untangle the temporal and
biogeographic history of the group.
One extant family (Pteropodidae, or Old
World fruit bats) lacks the sophisticated
echolocation abilities of other bats. Because
bat echolocation is a complex system involv-
ing specialization of the respiratory system,
ear, and brain (2), it has generally been
assumed that echolocation evolved only once
in bats. This hypothesis has been supported by
phylogenetic analyses of morphological data
by a number of groups [e.g., (5)]. These analy-
ses revealed a basal split among bats between
a single lineage leading to all echolocating
The author is in the Division of Vertebrate Zoology,
American Museum of Natural History, New York, NY
10024, USA. E-mail: simmons@amnh.org
www.sciencemag.org
Weaknesses in prior molecular studies
have left some doubt about their interpreta-
tion. For example, analyses of different
genes yielded incompatible phylogenetic
trees, and sampling of living bat families
was incomplete, leaving open the possibility
bats (Microchiroptera) and another lineage that sampling biases were responsible for the
leading to non-echolocating pteropodids
(Megachiroptera). However, recent analyses
of DNA sequence data have challenged this
surprising molecular results. The new study
by Teeling et al. (4) overcomes these diffi-
culties by simultaneously analyzing portions
hypothesis, instead suggesting that some of 17 nuclear genes sampled in all extant
echolocating bats (rhinolophoids) are more families. The resulting phylogenetic tree,
closely related to pteropodids than to other which is strongly supported by the data, con-
echolocating bats [e.g., (7, 8)]. These rela- firms the results of earlier molecular studies
tionships imply that echolocation either (see the figure). Non-echolocating pteropo-
evolved twice in bats or evolved once but was dids nest among lineages of echolocating
later lost in pteropodids. Either scenario bats, implying a dual origin for echolocation
Downloaded from http://science.sciencemag.org/ on February 8, 2018
would require a complete rethinking of our or its loss in pteropodids. The authors do not
understanding of the evolutionary history of attempt to choose between these alterna-
bats, including new evolutionary explana- tives, but a second analysis including several
tions for more than 20 different anatomical extinct families (4) suggests that a single ori-
specializations shared by living echolocating gin for echolocation (followed by its loss in
bats [but not pteropodids (5)]. pteropodids) is most likely.
Families of living bats
Pteropodidae (Old World fruit bats)
Rhinolophidae (horseshoe bats)
Hipposideridae (Old World leaf-nosed bats)
A
Megadermatidae (false vampire bats)
Craseonycteridae (bumblebee bats)
Rhinopomatidae (mouse-tailed bats)
B Nycteridae (slit-faced bats)
Emballonuridae (sheath-tailed bats)
Phyllostomidae (New World leaf-nosed bats)
Mormoopidae (leaf-chinned bats)
Noctilionidae (fishing bats)
Furipteridae (smoky bats)
Thyropteridae (disk-winged bats)
C
Mystacinidae (New Zealand short-tailed bats)
Myzopodidae (sucker-footed bats)
Vespertilionidae (evening bats)
D Molossidae (free-tailed bats)
Natalidae (funnel-eared bats)
Cretaceous
Paleocene
Oligocene
Pliocene
Miocene
Eocene
70 60 50 40 30 20 10 0
Million years ago
Temporal pattern of bat diversification. Teeling et al. (4) used their molecular tree and a series of
fossil calibration points to reconstruct the timing of bat radiation.They calculate that living bats last
shared a common ancestor at or just after the Cretaceous-Tertiary boundary.The four major lineages
of living echolocating bats (A to D) appear to have subsequently originated within a narrow time
frame in the Early Eocene [52 to 50 million years ago (4)].Although divergence dates estimated from
models of DNA sequence evolution are notoriously subject to biases, the Eocene dates in this study
are reasonably consistent with the results of morphology-based reconstructions [e.g. (3, 6)]. The
results of Teeling et al. suggest that all 18 of the living families of bats were distinct by the end of the
Eocene (about 34 million years ago). [Adapted from (4)]
SCIENCE VOL 307 28 JANUARY 2005 527
Published by AAAS
 PERSPECTIVES
Teeling et al. reanalyzed a previously
published morphological data set that
included four extinct families (5), using
their DNA tree as a constraint. The resulting
trees placed the Eocene fossil families as
sister taxa (close relatives) to the lineage
leading to all living bats. Previous analyses
of fossilized stomach contents, ear anatomy,
and limb structure concluded that two of the
fossil families were sophisticated echoloca-
tors similar to most living bats (5). The
other fossil groups are also thought to have
been capable of echolocation, although they
may not have been able to track flying prey
(5). Taking the relationships of these fossils
into account, it seems most likely that
echolocation evolved only once in bats,
before diversification of the group. The lin-
eage leading to bats was thus characterized
by two remarkable specializations seen in
no other land mammals: powered flight and
echolocation. The coincidence of these
adaptations—which may have been func-
tionally and evolutionarily linked (9)—was
probably the key that started the evolution-
ary diversification of the group.
The scope of this “big bang” Eocene
radiation is unprecedented in mammalian
history. What may have caused it? Teeling et
al. speculate that bats diversif ied in the
Early Eocene in response to an increase in
prey diversity, and that the varied echoloca-
PA R A S I T O L O G Y
Malaria Vaccines:
Back to the Future?
A. P.Waters, M. M. Mota, M. R. van Dijk, C. J. Janse
alaria is the scourge of many devel-
M oping countries, particularly those
in sub-Saharan Africa, claiming
several million lives each year. Researchers
have struggled for decades to make a suc-
cessful subunit or attenuated whole-organ-
ism vaccine but with limited success.
Factors that have hampered the develop-
ment of a subunit vaccine include the com-
plexity of the malaria life cycle, the wide
variety of immune response induced by the
malaria parasite, and an incomplete knowl-
edge of protective immunity. In contrast,
attenuated whole-organism vaccines are
better understood and in principle should
provide full protective immunity. Encour-
A. P. Waters, M. R. van Dijk, and C. J. Janse are in the
Department of Parasitology, Leiden University
Medical Centre, Leiden 2300 RC, Netherlands. M. M.
Mota is at the Instituto Gulbenkian de Ciência, 2780-
156 Oeiras, Portugal. E-mail: a.p.waters @lumc.nl
528 28 JANUARY 2005
tion and flight strategies that characterize
families may have evolved as a result of dif-
ferential exploitation of ecological niches
available at that time. The origin of the
major bat lineages in the Eocene is appar-
ently coincident with a rise in mean annual
temperature, a significant increase in plant
diversity, and the peak of Tertiary insect
diversity (4). The evolutionary success of
bats thus may have resulted from ancestral
bats being in the right place at the right time.
As flying predators capable of capturing
prey on the wing, they would have had few
competitors for the rich resources of the
Eocene night. The only other vertebrates
that exploit niches for nocturnal flying
predators are the owls and nightjars.
Interestingly, owls may also have undergone
an adaptive radiation in the Eocene (10).
The geographic origin of bats has been a
source of debate because Eocene bat fossils
have been found on most continents (5, 6).
Teeling et al. (4) seemingly have solved this
problem with their new phylogeny, which
unambiguously indicates a Laurasian
(Northern Hemisphere) origin for bats.
Once the group was established, different
lineages of bats probably diversified on dif-
ferent continents, but the scale of the
Teeling et al. analysis does not allow them
to untangle these patterns. Indeed, it is the
scale of bat diversity that makes this study
aging news in this regard comes from
Mueller et al. reporting in a recent issue of
Nature (1). They show that mice immu-
nized with genetically attenuated sporo-
zoites of the rodent malaria parasite
Plasmodium berghei are completely pro-
tected against challenge with wild-type
sporozoites.
A malaria infection is initiated by injec-
tion of sporozoites into the host blood by a
female anopheline mosquito as she takes a
blood meal (see the figure). The sporozoite
must migrate to the liver and colonize a
hepatocyte (liver cell) in order for the infec-
tion to progress. This journey is hazardous,
requiring traversal of resident macrophages
(Kupffer cells) lining the liver’s blood ves-
sels and passage through a number of hepa-
tocytes before the sporozoite finds a liver
cell to invade (see the figure). Here, the
sporozoite differentiates, grows, and multi-
plies within the hepatocyte, producing
VOL 307 SCIENCE www.sciencemag.org
Published by AAAS
so tantalizing. Their results give us a new
framework for understanding bat evolution,
but it is only the tip of the iceberg. Although
broad in scope, their evolutionary tree
includes fewer than 40 out of more than
1100 living bat species—just 3%.
Understanding the patterns of evolution of
different echolocation strategies, diets,
body sizes, flight styles, and reproductive
habits of bats will require much more fine-
grained phylogenies than are now available.
As always, the devil will be in the details.
References
1. N. B. Simmons, in Mammal Species of the World: A
Taxonomic and Geographic Reference, D. E. Wilson, D.
M. Reeder, Eds. (Johns Hopkins Univ. Press, Baltimore, in
press).
2. H. T. Arita, M. B. Fenton, Trends Ecol. Evol. 12, 53
(1997).
3. N. B. Simmons, T. M. Conway, in Bat Ecology, T. H. Kunz,
M. B. Fenton, Eds. (Univ. of Chicago Press, Chicago,
2003), pp. 493–535.
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4. E. C. Teeling et al., Science 307, 580 (2005).
5. N. B. Simmons, J. H. Geisler, Bull. Am. Mus. Nat. Hist.
235, 1 (1998).
6. N. B. Simmons, in Origins of the Major Clades of
Placental Mammals, K. Rose, D. Archibald, Eds. (Johns
Hopkins Univ. Press, Baltimore, in press).
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(2003).
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(2004).
9. J. R. Speakman, Symp. Zool. Soc. London 65, 39 (1993).
10. A. Feduccia, The Origin and Evolution of Birds (Yale
Univ. Press, New Haven, CT, ed. 2, 1999).
10.1126/science.1108871
thousands of merozoites that are released
into the bloodstream where they invade red
blood cells, initiating the erythrocytic stage
of the disease.
Of the various antimalaria vaccination
strategies proposed, preventing the sporo-
zoite from infecting a hepatocyte or block-
ing its subsequent intracellular develop-
ment has the advantage of acting before the
onset of pathology that is exclusively asso-
ciated with the erythrocytic stage of infec-
tion. However, “pre-erythrocytic” vaccines
must be 100% effective because a single
surviving sporozoite can still cause a lethal
blood-stage infection. In 1967, Nussen-
zweig and colleagues (2) generated sterile
protective immunity in a mouse model by
administering whole P. berghei sporozoites
that had been attenuated by gamma irradia-
tion. These radiation-attenuated sporo-
zoites (RAS) were incapable of infecting
mice, yet when given to mice as a vaccine in
a prime-boost combination, they generated
long-lasting immunity to subsequent chal-
lenge with normal nonirradiated parasites.
Immunity results from multifactorial
responses that are thought to include sporo-
zoite-specific antibodies, effector CD8 +
and CD4 + T cells, and memory CD8 + T
cells that recognize the infected hepatocyte
(3, 4).
An Eocene Big Bang for Bats
Nancy B. Simmons

Science 307 (5709), 527-528.

DOI: 10.1126/science.1108871

Downloaded from http://science.sciencemag.org/ on February 8, 2018

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