Laurasiatheria Afrotheria

Convergencia en Morfología y Ecología entre

Placentarios y Marsupiales
a eutriconodont) shows the skin membrane (patagium) associated synapsids to mammaliaforms shows incremental acquisition of
with elongate limbs for gliding, convergent to marsupial sugar gli-
ders, and ‘flying’
(Fig. 2f).
squirrels
Vol 450j13 dermopterans among placentals49
and2007jdoi:10.1038/nature06277
December
REVIEWS
mammalian apomorphies8,9,41,50. Stepwise assembly of incremental
precursor conditions towards complex mammal structure is an
evolutionary paradigm of functional adaptation and taxonomic
Treated individually, these curious cases of convergent adapta- diversification of mammals50–52. Some best-documented ‘textbook’
tions in extinct Mesozoic mammals represent many separate evolu-
REVIEWS
Transformation and diversification
tionary experiments20,37–39,49. But taken together (Fig. 2), they
unveiled a new picture in which ecological diversification is
in early
scenarios are acquisitions of key characters along a transformation
series: transformations of the mammalian middle ear and the jaw
hinge (Fig. 3), and evolution of the tribosphenic molars (Fig. 4).

mammal evolution
not unique to the Early Cenozoic mammalian radiation, and that
many dead-end Mesozoic mammal clades developed similar eco-
Homoplasies in mammal middle-ear evolution. The postdentary
bones in the posterior part of the mandible make up the jaw hinge

Although far Zhe-Xi

less abundant Transformation and diversification in early
morphotypes long before the analogous modern mammals (Fig. 2).
Luo1 numerically in the Mesozoic than in
the Cenozoic, within the limited snap-shot windows of the Middle
and the mandibular middle ear in premammalian cynodonts. They
show a gradual size reduction in the mandible—as the dentary bone
shows gradual enlargement—among transitional taxa successively
mammal evolution
Evolution of the earliest mammals shows successive episodes of diversification. Lineage-splitting in Mesozoic mammals is
coupled with many independent evolutionary experiments and ecological specializations. Classic scenarios of mammalian
morphological evolution
Ecomorphs Terrestrial-generalized tend to posit an orderly acquisition of key evolutionary innovations leading to adaptive
Semiaquatic-swimming Terrestrial-ambulatory Fossorial-digging Scansorial-climbing Volant-gliding
1
Insectivore
Dietary patterns diversification,
Zhe-Xi Luo but newly discovered
Crab-eating
Carnivorefossils show that Carnivore
evolution of such key characters
Feeding as the middle ear and the
Insectivore Insectivore
a Omnivore b
tribosphenic teeth is far Omnivore c Scavenging d Colonial e
sealmore labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups f Omnivore
Herbivore Insects
Evolution
multipliedofthetheopportunities
earliest mammals shows
for many successive
dead-end episodes
lineages of diversification.
to iteratively Lineage-splitting
evolve developmental in Mesozoic
homoplasies andmammals
convergent is
coupled with
ecological many independent
specializations, evolutionary
parallel to those inexperiments
modern mammal and ecological
groups. specializations. Classic scenarios of mammalian Flying squirrel
morphological evolution tend to posit an orderly acquisition of key Aardvark
evolutionary innovations leading to adaptive
Modern

diversification, but newly discovered fossils show that evolution of such key characters as the middle ear and the

M
ammals are an important
Otter group for under- Temporal pattern of early mammal evolution
tribosphenic standing
teeth is life
far and
more labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups
its evolution. With some The evolution of early mammals occurred Sugar glider
in successive
multiplied the5,400opportunities for many dead-end
extant species and 4,000 fossil genera, lineages to iteratively evolve developmental homoplasies
Tree shrew and convergent
diversifications or episodes of quick splitting of relatively
Short-tailed ecological specializations,
they developed parallel to those
a spectacular in modern
diversity of mammal groups. short-lived clades. Most order- or family-level clades are
ecomorphological Beaver
opposum specializations, ranging from the Raccoon Armadillo clustered around the several nodes of their evolutionary
1-gram bumblebee bat to the 100-tonne blue whale. tree. Mapped on the geological time scale, successive

M
ammals areofanthe
Basal diversifications important
three extantgroupmammalian
for under- Temporal pattern of early mammal evolution
clusters of emergent clades represent waves of diversifica-
standing (egg-laying
life and its evolution.
mammals),With some The
groups, monotremes marsupials tionevolution of early
(Fig. 1). Clades in amammals
precedingoccurred
episode of indiversifica-
successive
Early Cretaceous

Zhangheotherium 5,400 extant species and

(pouched mammals) and placentals, occurred in the 4,000 fossil genera, diversifications or
tion are mostly dead-end episodes of quick splitting of relatively
Eomaia evolutionary experiments; the
they developed a spectacular
Mesozoic Era1–4. Their ancestors are nested in a great diversity of short-lived
majority ofclades.them Mosthave order-
no director family-level clades are
ancestor–descendant
ecomorphological specializations, ranging
evolutionary bush with 25 or so lineages that co-existed from the clustered around the several nodes of
relationship to the emergent clades in the succeeding their evolutionary
1-gram bumblebee
with non-avian bat to the
dinosaurs and 100-tonne
other smallblue whale. during the episode of diversification,
vertebrates tree. Mapped consistenton the geological time scale,
with significant successive
taxonomic suc-
Basal diversifications of the three extant
Mesozoic. Mammals were not abundant in the Mesozoic, but mammalian clusters of emergent clades represent
cession and turnover between mammaliaform faunas of different waves of diversifica-
groups,
they were monotremes (egg-laying
relatively diverse. mammals),
Compared to the marsupials
547kgknown dinosaur tion (Fig.The
geological epochs. 1). main
Cladesepisodes
in a preceding episode of diversifica-
of diversification are: diver-
10
(pouched 5 mammals)
genera , over1–4 and placentals, occurred
310 Mesozoic mammaliaform genera are now in the known sification of premammalian mammaliaforms—theexperiments;
tion are mostly dead-end evolutionary extinct relatives the
Repenomamus
Mesozoic
Yanoconodon
to Era . Their ancestors are nested in
science, two-thirds of which were discovered in the last 25 years a great majority of them
outside mammals—during theSinodelphys have no direct ancestor–descendant
Late Triassic and Early Jurassic (Fig. 1,
evolutionary
(Box 1). bush with 25 or so lineages that co-existed relationship to the
node 1), the Middle Jurassic diversificationemergent clades in the succeeding
of docodonts, theriiform
withThe non-avian dinosaurs and other small
rise of mammals from premammaliaform cynodonts is an vertebrates during the episode of diversification, consistent
mammals, and the australosphenidan mammals that with significant taxonomic
are basal suc-
to
Mesozoic. Mammals were not
important transition in vertebrate evolution abundant in the
1,2,6–9 Mesozoic, but
. This already richly cession and turnover between mammaliaform
monotremes (Fig. 1, node 2), the Late Jurassic diversification withinfaunas of different
they were relatively
documented diverse.
transition
Castorocauda
Compared
has been rapidlytore-written
the 547 known by recent discov- geological
dinosaur the extinctepochs.
theriiformThegroups
main episodes
(Fig. 1, node of diversification
3) that are closer are:todiver-
mar-
genera 5
, over 310 Mesozoic mammaliaform 500– genera are now known sification of premammalian mammaliaforms—the extinct relatives
Jurassic

eries of very informative fossils (Box 1), by the increasingly compre- supials and placentals than to monotremes (Fig. 1, node 4), and the
800 g outside mammals—during the
tohensive
science, two-thirdswith
phylogenies of which
whichwere discovered
to infer the pattern in the last 25 years
of diversification Early Cretaceous divergence ofLate Triassic and
the marsupial Early and
lineage Jurassic (Fig. 1,
the placen-
(Box 1).
(Fig. 1), and by a more complex picture of the evolution of key node 1), the Middle Jurassic
tal lineage (Fig. 1, nodes 5 and 6). diversification of docodonts, theriiform
The rise offeatures.
anatomical mammals Thefromnewlypremammaliaform
improved fossil cynodonts
record can is an
recipro- mammals,
Cenozoicand the australosphenidan
placentals and marsupials mammals represent that a newareepisode
basal to of
1,2,6–9
important transition in vertebrate evolution
cally illuminate the molecular evolution of mammals, especially . This already richly monotremes (Fig. 1, node 2), the Late Jurassic diversification
in g diversification in succession to the Cretaceous stem eutherians and within
up to 500
documented
light of the transition
large has
discrepancies been rapidly
between re-written
the molecular by recent
time discov-
estimates the extinct theriiform groups (Fig. 1, node
metatherians.
Fruitafossor Cenozoic marsupials
3) thatasarea closer
are nested, whole,toVolaticotherium
inmar-
the
Morganucodon Haldanodon Sinoconodon Henkelotherium
eries of very informative fossils (Box 1), by the increasingly
and the fossil records for the origins of major marsupial and placental compre- supials and placentals than to monotremes
Cretaceous metatherians, but the emergent Cenozoic marsupial (Fig. 1, node 4), and the
‘Stereotypes’
hensive
super-orderphylogenies with
lineages. which
These new to fossils
infer the and Newly
pattern discovered
of ecomorphological
new Early
diversification
their analyses shed orders diversification
Cretaceous
or families in cannot
Mesozoic
divergence of bemammals
the marsupial lineage and
related directly the placen-
to the known
(Fig. 1), and by a more
light on several controversies: complex picture of the evolution of key tal lineage (Fig. 1, nodes 5 and 6).
Cretaceous metatherian genera by the best available morphological
Figure 2 | Diverse evolutionary
anatomical
. Temporal experiments
features. The newly
evolution: of Mesozoic
improved
is early mammal mammals
fossilevolution
record canbest andchar- (predation
recipro- Cenozoic
data or feeding
sets10–12placentals
. The latestand onmarsupials
analysesother vertebrates)
of all representalso
eutherians in
a newlarge gobiconodontids
episode
strongly favourof
42
and
41
their ecological convergence
acterized by tomajor
cally illuminate modern
the molecular
longmammal
evolution
branches ecomorphotypes.
reaching deep into the large
of mammals, especially in individuals
diversification
placement in succession
of all known eutherians of; d
of Sinoconodon
to the Cretaceous, scratch-digging
the stem eutherians
Cretaceous outside andthe
andfeeding on
metatherians. Cenozoic marsupials 20 are nested, as a whole, in limb
the characteristics
a, Representationlight of the
of the
Mesozoic large
and discrepancies
traditionalby theassumption between
long evolutionary thattheMesozoic
molecular time
fuse that mammals estimates
delayed diver- colonial
Cenozoicinsects
placentalsin 13,14
Fruitafossor
, in contrast ;toe,ascansorial (climbing)
previous analysis 15
. The suc-
were generalizedand smallthe animals
sificationfossilwithin
records
withforgeneralized
long the origins of
branches? major
feeding
Or is this marsupial
and anddominated
terrestrial
evolution placental in Cretaceous metatherians,
basalclusters
cessive eutherians and but
of emergent the and
metatherians,
clades emergent Cenozoic
andturnover
faunal their near marsupial
between the 11,47,48; and
relatives
super-order lineages. These new fossils and their analyses shed new orders or families cannot be related directly to 49the known
 lutrasimilis as a swimming and burrow-
ing mammaliaform. Abbreviations: as, as-
tragalus; ca, caudal vertebrae; cn, ento-,
meso-, and ecto-cuneiforms; co, coro-
noid process of dentary; cp, carpals; cs,
calcaneus; ec, ectepicondyle and supi-
nator shelf (humerus); ef, entepicondyle
foramen; ep?, probable epipubis; is,
ischium; J, jugal; L1-6, lumbar ribs 1
to 6; m, molars; mb, manubrium of
malleus; mp, metacarpals; mx, maxilla;
px, premaxilla; ra, radius; rc, radial
condyle; S1-2, sacrals 1 and 2; sp,
extratarsal (‘‘poisonous’’) spur; t4-t14
(preserved ribs through thoracic 17); uc,
ulnar condyle; ul, ulna.

posterior aspect of the mandibular angle ac- Fig. 2. Dentition and

commodates the ectotympanic (angular). The mandible of Castorocauda
posterior position of the ectotympanic concav- lutrasimilis (JZMP04-117).
ity on the mandibular angle in docodontans is (A) Labial view of lower
different from and more derived than that in the molars 1 to 6. (B) Lin-
mammaliaforms Sinoconodon and Morganu- gual view of lower molars
codon, in which the ectotympanic concavity 1 to 6. (C) Crown view of
is on the medial aspect of the mandibular angle lower molars 3 to 6. (D)
(6, 7). The manubrium of the malleus (retro- Cusp pattern [cusp desig-
articular process of the articular) is anteriorly nation from (11, 12)]. (E)
Middle ear bones. (F)
curved and long in comparison with the
Reconstructed mandible
short manubrium of Morganucodon and and middle ear bones
Sinoconodon (6, 7, 27). The proportion of (lateral view). c, canine;
the malleus manubrium is similar to that of m, molars.
extant monotremes, although slightly more
robust than in the latter. Castorocauda is sim-
ilar to crown Mammalia and more derived
than Sinoconodon, Morganucodon, and all pre-
mammaliaform cynodonts (27) in preserved mid-
dle ear features.
Our analyses, including new characters of
Castorocauda, corroborate that docodontans
are a mammaliaform clade, less derived than
Hadrocodium but more derived than Sinoco-
nodon and Morganucodon (1, 8, 26, 28, 29).
Among docodontans, Castorocauda is close-
ly related to the Middle Jurassic Krusatodon
and Simpsonodon of England (9–11), sug-
gesting interchange between faunas of the
Eurasian landmasses during the Middle Ju-
rassic time.
Integument. The fur of Castorocauda is
preserved as impressions of guard hairs and
carbonized under-furs. Hairs and hair-related
integument structures are important character- eutriconodontans, and symmetrodonts (1). This and that the origins of biological adaptations
istics of all modern mammals (30, 31). Several indicates that the presence of fur is ancestral of mammalian integument, such as tactile sen-
younger fossils within the crown Mammalia for the crown Mammalia. Castorocauda further sory function and thermal insulation, occurred
are preserved with fur, including basal euthe- shows that fur was also present in mammalia- before the origin of the crown Mammalia
rians and metatherians (32, 33), multituberculates, form relatives of modern mammals (Fig. 3A) (30, 31).

1124 24 FEBRUARY 2006 VOL 311 SCIENCE www.sciencemag.org

164 m.a.
a eutriconodont) shows the skin membrane (patagium) associated synapsids to mammaliaforms shows incremental acquisition of
with elongate limbs for gliding, convergent to marsupial sugar gli-
ders, and ‘flying’
(Fig. 2f).
squirrels
Vol 450j13 dermopterans among placentals49
and2007jdoi:10.1038/nature06277
December
REVIEWS
mammalian apomorphies8,9,41,50. Stepwise assembly of incremental
precursor conditions towards complex mammal structure is an
evolutionary paradigm of functional adaptation and taxonomic
Treated individually, these curious cases of convergent adapta- diversification of mammals50–52. Some best-documented ‘textbook’
tions in extinct Mesozoic mammals represent many separate evolu-
REVIEWS
Transformation and diversification
tionary experiments20,37–39,49. But taken together (Fig. 2), they
unveiled a new picture in which ecological diversification is
in early
scenarios are acquisitions of key characters along a transformation
series: transformations of the mammalian middle ear and the jaw
hinge (Fig. 3), and evolution of the tribosphenic molars (Fig. 4).

mammal evolution
not unique to the Early Cenozoic mammalian radiation, and that
many dead-end Mesozoic mammal clades developed similar eco-
Homoplasies in mammal middle-ear evolution. The postdentary
bones in the posterior part of the mandible make up the jaw hinge

Although far Zhe-Xi

less abundant Transformation and diversification in early
morphotypes long before the analogous modern mammals (Fig. 2).
Luo1 numerically in the Mesozoic than in
the Cenozoic, within the limited snap-shot windows of the Middle
and the mandibular middle ear in premammalian cynodonts. They
show a gradual size reduction in the mandible—as the dentary bone
shows gradual enlargement—among transitional taxa successively
mammal evolution
Evolution of the earliest mammals shows successive episodes of diversification. Lineage-splitting in Mesozoic mammals is
coupled with many independent evolutionary experiments and ecological specializations. Classic scenarios of mammalian
morphological evolution
Ecomorphs Terrestrial-generalized tend to posit an orderly acquisition of key evolutionary innovations leading to adaptive
Semiaquatic-swimming Terrestrial-ambulatory Fossorial-digging Scansorial-climbing Volant-gliding
1
Insectivore
Dietary patterns diversification,
Zhe-Xi Luo but newly discovered
Crab-eating
Carnivorefossils show that Carnivore
evolution of such key characters
Feeding as the middle ear and the
Insectivore Insectivore
a Omnivore b
tribosphenic teeth is far Omnivore c Scavenging d Colonial e
sealmore labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups f Omnivore
Herbivore Insects
Evolution
multipliedofthetheopportunities
earliest mammals shows
for many successive
dead-end episodes
lineages of diversification.
to iteratively Lineage-splitting
evolve developmental in Mesozoic
homoplasies andmammals
convergent is
coupled with
ecological many independent
specializations, evolutionary
parallel to those inexperiments
modern mammal and ecological
groups. specializations. Classic scenarios of mammalian Flying squirrel
morphological evolution tend to posit an orderly acquisition of key Aardvark
evolutionary innovations leading to adaptive
Modern

diversification, but newly discovered fossils show that evolution of such key characters as the middle ear and the

M
ammals are an important
Otter group for under- Temporal pattern of early mammal evolution
tribosphenic standing
teeth is life
far and
more labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups
its evolution. With some The evolution of early mammals occurred Sugar glider
in successive
multiplied the5,400opportunities for many dead-end
extant species and 4,000 fossil genera, lineages to iteratively evolve developmental homoplasies
Tree shrew and convergent
diversifications or episodes of quick splitting of relatively
Short-tailed ecological specializations,
they developed parallel to those
a spectacular in modern
diversity of mammal groups. short-lived clades. Most order- or family-level clades are
ecomorphological Beaver
opposum specializations, ranging from the Raccoon Armadillo clustered around the several nodes of their evolutionary
1-gram bumblebee bat to the 100-tonne blue whale. tree. Mapped on the geological time scale, successive

M
ammals areofanthe
Basal diversifications important
three extantgroupmammalian
for under- Temporal pattern of early mammal evolution
clusters of emergent clades represent waves of diversifica-
standing (egg-laying
life and its evolution.
mammals),With some The
groups, monotremes marsupials tionevolution of early
(Fig. 1). Clades in amammals
precedingoccurred
episode of indiversifica-
successive
Early Cretaceous

Zhangheotherium 5,400 extant species and

(pouched mammals) and placentals, occurred in the 4,000 fossil genera, diversifications or
tion are mostly dead-end episodes of quick splitting of relatively
Eomaia evolutionary experiments; the
they developed a spectacular
Mesozoic Era1–4. Their ancestors are nested in a great diversity of short-lived
majority ofclades.them Mosthave order-
no director family-level clades are
ancestor–descendant
ecomorphological specializations, ranging
evolutionary bush with 25 or so lineages that co-existed from the clustered around the several nodes of
relationship to the emergent clades in the succeeding their evolutionary
1-gram bumblebee
with non-avian bat to the
dinosaurs and 100-tonne
other smallblue whale. during the episode of diversification,
vertebrates tree. Mapped consistenton the geological time scale,
with significant successive
taxonomic suc-
Basal diversifications of the three extant
Mesozoic. Mammals were not abundant in the Mesozoic, but mammalian clusters of emergent clades represent
cession and turnover between mammaliaform faunas of different waves of diversifica-
groups,
they were monotremes (egg-laying
relatively diverse. mammals),
Compared to the marsupials
547kgknown dinosaur tion (Fig.The
geological epochs. 1). main
Cladesepisodes
in a preceding episode of diversifica-
of diversification are: diver-
10
(pouched 5 mammals)
genera , over1–4 and placentals, occurred
310 Mesozoic mammaliaform genera are now in the known sification of premammalian mammaliaforms—theexperiments;
tion are mostly dead-end evolutionary extinct relatives the
Repenomamus
Mesozoic
Yanoconodon
to Era . Their ancestors are nested in
science, two-thirds of which were discovered in the last 25 years a great majority of them
outside mammals—during theSinodelphys have no direct ancestor–descendant
Late Triassic and Early Jurassic (Fig. 1,
evolutionary
(Box 1). bush with 25 or so lineages that co-existed relationship to the
node 1), the Middle Jurassic diversificationemergent clades in the succeeding
of docodonts, theriiform
withThe non-avian dinosaurs and other small
rise of mammals from premammaliaform cynodonts is an vertebrates during the episode of diversification, consistent
mammals, and the australosphenidan mammals that with significant taxonomic
are basal suc-
to
Mesozoic. Mammals were not
important transition in vertebrate evolution abundant in the
1,2,6–9 Mesozoic, but
. This already richly cession and turnover between mammaliaform
monotremes (Fig. 1, node 2), the Late Jurassic diversification withinfaunas of different
they were relatively
documented diverse.
transition
Castorocauda
Compared
has been rapidlytore-written
the 547 known by recent discov- geological
dinosaur the extinctepochs.
theriiformThegroups
main episodes
(Fig. 1, node of diversification
3) that are closer are:todiver-
mar-
genera 5
, over 310 Mesozoic mammaliaform 500– genera are now known sification of premammalian mammaliaforms—the extinct relatives
Jurassic

eries of very informative fossils (Box 1), by the increasingly compre- supials and placentals than to monotremes (Fig. 1, node 4), and the
800 g outside mammals—during the
tohensive
science, two-thirdswith
phylogenies of which
whichwere discovered
to infer the pattern in the last 25 years
of diversification Early Cretaceous divergence ofLate Triassic and
the marsupial Early and
lineage Jurassic (Fig. 1,
the placen-
(Box 1).
(Fig. 1), and by a more complex picture of the evolution of key node 1), the Middle Jurassic
tal lineage (Fig. 1, nodes 5 and 6). diversification of docodonts, theriiform
The rise offeatures.
anatomical mammals Thefromnewlypremammaliaform
improved fossil cynodonts
record can is an
recipro- mammals,
Cenozoicand the australosphenidan
placentals and marsupials mammals represent that a newareepisode
basal to of
1,2,6–9
important transition in vertebrate evolution
cally illuminate the molecular evolution of mammals, especially . This already richly monotremes (Fig. 1, node 2), the Late Jurassic diversification
in g diversification in succession to the Cretaceous stem eutherians and within
up to 500
documented
light of the transition
large has
discrepancies been rapidly
between re-written
the molecular by recent
time discov-
estimates the extinct theriiform groups (Fig. 1, node
metatherians.
Fruitafossor Cenozoic marsupials
3) thatasarea closer
are nested, whole,toVolaticotherium
inmar-
the
Morganucodon Haldanodon Sinoconodon Henkelotherium
eries of very informative fossils (Box 1), by the increasingly
and the fossil records for the origins of major marsupial and placental compre- supials and placentals than to monotremes
Cretaceous metatherians, but the emergent Cenozoic marsupial (Fig. 1, node 4), and the
‘Stereotypes’
hensive
super-orderphylogenies with
lineages. which
These new to fossils
infer the and Newly
pattern discovered
of ecomorphological
new Early
diversification
their analyses shed orders diversification
Cretaceous
or families in cannot
Mesozoic
divergence of bemammals
the marsupial lineage and
related directly the placen-
to the known
(Fig. 1), and by a more
light on several controversies: complex picture of the evolution of key tal lineage (Fig. 1, nodes 5 and 6).
Cretaceous metatherian genera by the best available morphological
Figure 2 | Diverse evolutionary
anatomical
. Temporal experiments
features. The newly
evolution: of Mesozoic
improved
is early mammal mammals
fossilevolution
record canbest andchar- (predation
recipro- Cenozoic
data or feeding
sets10–12placentals
. The latestand onmarsupials
analysesother vertebrates)
of all representalso
eutherians in
a newlarge gobiconodontids
episode
strongly favourof
42
and
41
their ecological convergence
acterized by tomajor
cally illuminate modern
the molecular
longmammal
evolution
branches ecomorphotypes.
reaching deep into the large
of mammals, especially in individuals
diversification
placement in succession
of all known eutherians of; d
of Sinoconodon
to the Cretaceous, scratch-digging
the stem eutherians
Cretaceous outside andthe
andfeeding on
metatherians. Cenozoic marsupials 20 are nested, as a whole, in limb
the characteristics
a, Representationlight of the
of the
Mesozoic large
and discrepancies
traditionalby theassumption between
long evolutionary thattheMesozoic
molecular time
fuse that mammals estimates
delayed diver- colonial
Cenozoicinsects
placentalsin 13,14
Fruitafossor
, in contrast ;toe,ascansorial (climbing)
previous analysis 15
. The suc-
were generalizedand smallthe animals
sificationfossilwithin
records
withforgeneralized
long the origins of
branches? major
feeding
Or is this marsupial
and anddominated
terrestrial
evolution placental in Cretaceous metatherians,
basalclusters
cessive eutherians and but
of emergent the and
metatherians,
clades emergent Cenozoic
andturnover
faunal their near marsupial
between the 11,47,48; and
relatives
super-order lineages. These new fossils and their analyses shed new orders or families cannot be related directly to 49the known
Stiassny & Meyer (1999)
http://nature.ca/puijila/fb_e.cfm
 use information from two very different kinds of mammals:
rodents of the mountain beaver family (aplodontoids) and
The Role of Climatic Change Applying those observations to what we might expect in
the future, it seems likely that we will see changes in genotypes

in the Evolution of Mammals

June 2007 / Vol. 57 No. 6 • BioScience 523 horses. Both groups have been well studied, and the fossil
Teaching Biology
and phenotypes at the population level in response to climatic
scales of climatic change. Time is on the vertical
record of both axis. The rich for the time periods of in-
is reasonably change over the next hundred years. But climate-induced
mbolize the periodicity and amplitude of terest temperature
(Hopkins 2005,changes
The Role of Climatic Change
MacFadden 2005). Despite their name,
mountain beavers are digging rodents (figure 5), not true
speciation, if it is a real phenomenon, appears to require cli-
matic events that operate on a much longer timescale than
nces on different timescales. The overall pattern is one of succes-
scillations of climate being nested withinThey lessinclude
rapid more in the Evolution of Mammals
beavers; they are even in a different family than true beavers.
oscillations.
than 30 species that lived during the past
35 million years, but only one surviving species today
those that can cause population-level response. So we would
not expect speciation to regenerate biodiversity in response
to human-induced global warming—especially keeping in
om Ruddiman (2001). © 2001 by W. H. Freeman (Aplodontia and rufa, in Company.
the Pacific Northwest).
ANTHONY D. BARNOSKY AND BRIAN P. KRAATZ mind that the rate of climatic change over the next century
ion. More than 20 of the 30-plus mountain beaver species first is likely to be faster than the rates experienced by mammals
appeared near the beginning of the Mid-Miocene Climatic through much (if not all) of their evolutionary history.
ANTHONY D.
Optimum (Hopkins BARNOSKY AND BRIAN
2005). Likewise, P. KRAATZ
The paleontological record ofamammals burst offers many examples of evolutionary change, which are well documented at many levels of the biological
of new horsehierarchy—at species appeared at about
the level of species (and the above), populations, morphology, and, in ideal cases, even genes. The evolutionary changes developed against
same time (MacFadden a backdrop of 2005).
climatic Such datathat
change agree took place on different scales, from rapid shifts in climate state that took only a few decades, to those that occurred
The paleontological record of mammals offers many examples of evolutionary change, which are well documented at many levels of the biological
with thetheexpectations
hierarchy—at over a millennial
level of species (and of above),
climaticscale, to regular
change
populations, stim- and, in ideal cases,transitions
glacial–interglacial
morphology, even genes. The with cycles ofchanges
evolutionary roughly a hundred
developed againstthousand years, to long-term warming or cooling
a backdrop of climatic change
ulating speciation trends over
that tookhundreds of
place on different
at glacial–interglacial
this geographic thousands
scales, fromto millions
rapid shifts in of years.
climate stateAre
thatthere certain
took only scales
a few decades,
(western cycles of roughly a hundred thousand years, to long-term warming or coolingof
to climatic
those change that accelerate evolution? And what will the
that occurred
over a millennial scale, currentto regularglobal warming transitions
event do with to evolutionary rates? Here we use paleontology—the study of fossils—to illustrate the scientific method behind
trendsUnited States)
over hundreds and tectonic
ofanswering
thousands to
suchmillionsscale
complex (3°C
of years. Areto
questions, 4°C
there certain
and toscales
suggestof climatic change that
that current ratesaccelerate
of global evolution?
warming And are
whatfar will
toothefast to influence evolution much and instead are
current global warming
over 1.5 million event do
years, to evolutionary
followed rates?
by Here
3.5 million we use paleontology—the study of fossils—to illustrate the scientific method behind
answering such complexlikely to accelerate
questions, and to suggest extinctions.
that current rates of global warming are far too fast to influence evolution much and instead are
likelyyears of sustained
to accelerate extinctions. warmth). Therefore, with
this evidence, Keywords:
there is nopaleontology,
reason to reject evolution,
the hy- mammals, scientific method, climate
Keywords: paleontology, evolution, mammals, scientific method, climate
pothesis that speciation requires out-of-the-

D
ordinary climatic changes at the tectonic scale
espite all the3arguments
(hypothesis in table
hypothesis reaches thea fact.
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is a fact. It is a fact in theissense
over
1).
of
status
for example, “something having real, demonstrable exis-
all the arguments
semantics,
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dictionary
It is
ofageneral
evolution
before
definitions—
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thisover semantics,
the limits of the
porary Thomas
sense of dictionary definitions—
evolution
fossil record in this regard,
Huxley recognized
the limits
its power
and hisof
in the
the fossil record in this regard, and his contem-
contem-
evolu-
porary Thomas Huxley recognized its power in the evolu-
tionary debate when he wrote,“Primary and direct evidence
tance,quality
tence...the it would for
of being
example,
be desirable
real or actual”
“something
to have having
additional
(Soukhanov et al.
real, demonstrable exis- tionary debate when he wrote,“Primary and direct evidence
in favour of evolution can be furnished only by palæontol-
tests
1996). And it is a facttence...the
provided bythe
in robustly
scientific quality
constructed
sense—“an of being andreal
observation cal-or actual” ogy.(Soukhanov
The geological et al. so soon asinitfavour
record, approaches of evolution
com- can be furnished only by palæontol-
thatibrated
has beenphylogenies
repeatedly 1996). And
confirmed”
of it (Kennedy
other is mammal
a fact in et the scientific sense—“an
al.groups.
1998). pleteness, must,observation
when properly questioned, ogy. The yieldgeological
either an record, so soon as it approaches com-
This is a bold statement, but it follows directly from
that has been repeatedly confirmed” (Kennedy et al. 1998). in- affirmative or a negative answer: if evolution has taken
pleteness, must, place,when properly questioned, yield either an
controvertible observations. We know what genes are and how there will its mark be left; if it has not taken place, there will
Global
traits warming
are inherited,
This
and that over thethe
is next
avariation
bold century
statement,
we observe be-
but it follows directly from in-
lie its refutation” (Huxley 1880).
affirmative or a negative answer: if evolution has taken place,
tweenTesting the within
individuals controvertible
previous hypotheses
populations observations.
and yielded
between Weisknow whatAlthough
three
species genes aretheand how
paleontological thereis will
record still its
far mark
from be left; if it has not taken place, there will
underlain by genetictraits
new observations, are inherited,
differences.
which We knowlead,
in turn andthose
how thatge-the variation
through we observe
complete—for the same be-reasons Darwin lie and
its refutation”
Huxley recog-(Huxley 1880).
netic differences arisetween and how they
individuals are maintained:
within through
populations nized some 150
and between species is years ago—it now yields a
Although affir-
resounding the paleontological record is still far from
hypotheses, to informed predictions about what
mutation, recombination, random drift, and selection. We can mative answer about evolution. Fossils demonstrate
(andtodo) expect the underlain
induceinwithin-speciesface of evolution by genetic
current global
in
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domesticwarming.
animal
We know how those ge- complete—for the same reasons Darwin and Huxley recog-
overwhelmingly that geologically older species are replaced
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of dogs,we have
cattle, arise
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(including 150 years ago—it now yields a resounding affir-
suc-
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amples as industrial (and melanism in moths (Cook 2003, Rudge
do) induce within-species evolution in domestic animal species typically share certain traits with the older
overwhelmingly ones, butthat geologically older species are replaced
future.
2005) and the reduction of size in snow lotus plants (Law and
The tests
Salick 2005). breeding
On thediscussed
microbial level, programs—think
above yieldedthe
we recognize theof fol-
dogs, cattle,Anthony
reality and racehorses. And by geologically younger descendent species (including the suc-
D. Barnosky (e-mail: barnosky@berkeley.edu) is a professor of
lowing observations:
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it: different selection
As Palumbitempo- (2005) cause evolution in such ex- cession
integrative biology, curator of paleontology at the Museum of species
of Paleontology, and in our own human history). The younger
pointed
ral andout, consumers
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and taxpayers
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Zoology, University ofshare certain traits with the older ones, but
larsmanifest
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2005) and
different evolutionary
the reduction
evolutionary arms race California, Berkeley, CA 94720. His work focuses on understanding the effects
of size in snow lotus plants (Law and
scales—some
between antibiotics and the new bacterial genomes for which of environmental changes on ecosystems, with a particular emphasis on
theyatselect, and toortrySalick
genetic population
to prevent 2005). such On
levels, theothers
potentially microbial at the
disastrous level, wemammalian
recognize the reality Anthony D. Barnosky (e-mail: barnosky@berkeley.edu) is a professor of
communities. Brian P. Kraatz is a PhD candidate and National
species level;
pandemics as avian flu. (b)of evolution
geologically byrapidspending
or cyclical money cli- on it: As Palumbi (2005)
Science Foundation GK–12 fellow in the same integrative
department biology,
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Figure 4. Detail of the last 70 million matic

mechanisms
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cause genetic changes lars to at combat

the populationthe ever-escalating
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Berkeley, CA 94720. rodents),
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long term—which
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genomes
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organized by the American Institute of Biological Sciences, the National
changes on with the Mid-Miocene
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Mid-Miocene Climatic Optimum.events Figure that onlymodified
because isolation they select,
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persist try
a tiny fraction of all the life forms that have to
long prevent
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P. this group
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been
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from the recognized
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and showartist’susrendition,
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and Company. Used with permission. into speciation,mechanisms
www.biosciencemag.org
climatic change must beinunusual
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June 2007 / Vol. 57 No. 6 • BioScience 523
of Hopkins
science to students (2005);
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for example, “something having real, demonstrable exis- tionary debate when he wrote,“Primary and direct eviden
in the Evolution of Mammals
Teaching Biology
tence...the quality of being real or actual” (Soukhanov et al. in favour of evolution can be furnished only by palæont

that has been repeatedly confirmed” (Kennedy et al. 1998).

The Role of Climatic Change
1996). And it is a fact in the scientific sense—“an observation ogy. The geological record, so soon as it approaches co
pleteness, must, when properly questioned, yield either
in the Evolution of Mammals
This is a bold statement, but it follows directly from in- affirmative or a negative answer: if evolution has taken pla
controvertible observations. We know what genes are and how
ANTHONY D. BARNOSKY AND BRIAN P. KRAATZ
there will its mark be left; if it has not taken place, there w
traits are inherited, and that the variation we observe be- lie its refutation” (Huxley 1880).
tween individuals within populations
ANTHONY D. BARNOSKY
andAND between
The paleontological BRIAN Precord
species
. KRAATZ
is Although the paleontological record is still far fro
of mammals offers many examples of evolutionary change, which are well documented at many levels of the biological
underlain by genetic differences. Wehierarchy—at know how the level ofthose
species (and ge-above), populations, complete—for
morphology, and, in ideal the cases,same
even genes. reasons Darwin
The evolutionary changesand Huxley
developed against reco
a backdrop of climatic change that took place on different scales, from rapid shifts in climate state that took only a few decades, to those that occurred
netic differences arise and how they are
The paleontological record ofmaintained:
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millennial scale, to through
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regularof glacial–interglacial some
are well documented
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at many
cycles
hierarchy—at the level of species (and above), populations, morphology, and, in ideal cases, even genes. The evolutionary changes developed against
years
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of the biological
a hundred nowto long-term
thousand years, yields warming
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trends over hundreds of thousands to millions of years. Are there certain scales of climatic change that accelerate evolution? And what will the
mutation, recombination, random
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scale, current global warming transitions
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study evolution.
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(and do) induce within-species evolution
current global warming event doin domestic
to evolutionary
likely to accelerate animal
rates? Here
extinctions. we use paleontology—the studyoverwhelmingly
of fossils—to illustrate the scientificthat geologically older species are replac
method behind
answering such complex questions, and to suggest that current rates of global warming are far too fast to influence evolution much and instead are
breeding programs—think likely of todogs,
acceleratecattle,
extinctions. and racehorses. And
Keywords: paleontology, evolution, mammals, scientific method, climate
by geologically younger descendent species (including the su
we have seen natural selection cause evolution in such ex-
Keywords: paleontology, evolution, mammals, scientific method, climate
cession of species in our own human history). The young
amples as industrial melanismespite
2005) and the reduction of for size
in allmoths
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between antibiotics and thenetic new bacterial
differences arisetween
and how genomes
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Although affir-
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mutation, recombination, random
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evolution in domestic animal overwhelmingly that geologicallycommunities. older species are replaced Brian P. Kraatz a PhDand Huxley recog-
candidate and Natio
netic differences arise
breeding programs—think of dogs, cattle, and racehorses. And and how they are maintained: through nized
by geologically younger descendent species (including the suc- some 150 years ago—it now yields a resounding affir-
pandemics as avian flu. we have seen naturalmutation, selection cause recombination,
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answer
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overwhelmingly that geologically older species are replaced
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reduction of show size in snowus lotus how
plants (Law those
and
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Museum of Paleontology. His work focuses on the evolution of mammals
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Salick 2005). On the microbial level, we recognize the reality
mechanisms we observe in such of evolution a short
by spendingwetermhave
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and taxpayers
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spend billions
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silization process requiresbetween
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of weofmammalian
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recognize organized
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Anthony D. Barnosky
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Institute of Biological Sciences,
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events that only a tiny fraction of all
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between antibiotics and the new bacterial genomes for which of environmental changes on ecosystems, with a particular emphasis on
of those have been discovered. Darwin
silization process requires such
they (1859)
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events that only a tiny fraction of all the life forms that have
sequence of
to prevent such
organized by theTeachers.
potentially
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of those have been discovered.
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Darwin (1859) the fossil record show us how those
Teachers. © 2007 American Institute of Biological Sciences.
Museum of Paleontology. His work focuses on the evolution of mammals and
mechanisms we observe in such a short term play out over the on communicating science to students from K–12 through university levels. This
www.biosciencemag.org www.biosciencemag.orglong term—which is somewhat remarkable, given that the
June 2007 / Vol. 57 No.
fos- 6 • BioScience
article emerged from
June 2007 / Vol. 57 No. 6 • BioScience 5
523a symposium entitled “Evolution and the Environment,”

silization process requires such a complicated sequence of organized by the American Institute of Biological Sciences, the National
events that only a tiny fraction of all the life forms that have Evolutionary Synthesis Center, and the Biological Sciences Curriculum Study
Deriva Continental y la Historia de los Mamíferos
 El Gran Intercambio Americano

Hormigueros
Armadillos
Osos Chiguiros
Camellos Gliptodontos
Gatos Monos
Venados Zarigueyas
Perros Phoruracidos
Elefantes Puercoespines
Caballos Perezosos
Pecaríes Teratomos
Conejos Toxodontos
Mapaches
Zorrillos
Tapires
Musarañas
‘‘ghosts of past mutualisms’’ [7,8]. have serious consequences for plant populations [13–16].

PLoS ONE | www.plosone.org 1 2008 | Volume 3 | Issue 3 | e1745

Seed Dispersal Anachronisms: Rethinking the Fruits

Extinct Megafauna Ate
Paulo R. Guimarães Jr.1,3, Mauro Galetti2, Pedro Jordano3*
1 Departamento de Fı́sica da Matéria Condensada, Instituto de Fı́sica Gleb Wataghin, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil, 2 Laboratório de
Seed Biológica
Biologia da Conservação, Universidade Estadual Paulista (UNESP), Rio Claro, São Paulo, Brazil, 3 Integrative Ecology Group, Estación DispersaldeAnachronisms
Doñana, Consejo Superior
de Investigaciones Cientı́ficas (CSIC), Sevilla, Spain

Abstract
Background: Some neotropical, fleshy-fruited plants have fruits structurally similar to paleotropical fruits dispersed by
megafauna (mammals .103 kg), yet these dispersers were extinct in South America 10–15 Kyr BP. Anachronic dispersal
systems are best explained by interactions with extinct animals and show impaired dispersal resulting in altered seed
dispersal dynamics.

Methodology/Principal Findings: We introduce an operational definition of megafaunal fruits and perform a comparative
analysis of 103 Neotropical fruit species fitting this dispersal mode. We define two megafaunal fruit types based on previous
analyses of elephant fruits: fruits 4–10 cm in diameter with up to five large seeds, and fruits .10 cm diameter with
numerous small seeds. Megafaunal fruits are well represented in unrelated families such as Sapotaceae, Fabaceae,
Solanaceae, Apocynaceae, Malvaceae, Caryocaraceae, and Arecaceae and combine an overbuilt design (large fruit mass and
size) with either a single or few (,3 seeds) extremely large seeds or many small seeds (usually .100 seeds). Within-family
and within-genus contrasts between megafaunal and non-megafaunal groups of species indicate a marked difference in
fruit diameter and fruit mass but less so for individual seed mass, with a significant trend for megafaunal fruits to have larger
seeds and seediness.

Conclusions/Significance: Megafaunal fruits allow plants to circumvent the trade-off between seed size and dispersal by
relying on frugivores able to disperse enormous seed loads over long-distances. Present-day seed dispersal by scatter-
hoarding rodents, introduced livestock, runoff, flooding, gravity, and human-mediated dispersal allowed survival of
megafauna-dependent fruit species after extinction of the major seed dispersers. Megafauna extinction had several
potential consequences, such as a scale shift reducing the seed dispersal distances, increasingly clumped spatial patterns,
reduced geographic ranges and limited genetic variation and increased among-population structuring. These effects could
be extended to other plant species dispersed by large vertebrates in present-day, defaunated communities.
Figure 2. Fleshy fruited megafaunal-dependent species illustrating size, shape, and color variation. a, Attalea speciosa, Arecaceae; b,
Citation:
Mouriri elliptica, Guimarães PR Jr, c,Galetti
Melastomataceae; M, Jordano
Hymenaea P (2008) Seed
stigonocarpa, Dispersal
Fabaceae; Anachronisms:
d, Genipa Rethinking
americana, the Fruits
Rubiaceae; Extinctelliptica,
e, Salacia Megafauna Ate. PLoS ONE
Celastraceae; 3(3): e1745.
f, Annona
doi:10.1371/journal.pone.0001745
dioica, Annonaceae. Black reference line is 2 cm length. Photos from Fazenda Rio Negro, Pantanal, Brazil; by PJ, MG, and Camila I. Donatti.
doi:10.1371/journal.pone.0001745.g002
Editor: Dennis Marinus Hansen, University of Zurich, Switzerland
Received June 8, 2007; Accepted January 15, 2008; Published March 5, 2008
comparable range !for2008non-megafaunal
Copyright: species
Guimarães et al. This is 0.1%–8.9%.
is an open-access There
article distributed underisthe
alsoterms
a similar
of the trend inCommons
Creative fruit design between
Attribution megafaunal
License, which permits
However,unrestricted
this is theuse,
simple result of increasing total fruit mass, not
distribution, and reproduction in any medium, provided and non-megafaunal
the original species
author and source when comparing the allocation of
are credited.
increasingFunding:
the relative seedwas
The study load/fruit
supported(Fig. 4a); thus,
by public fundingthere
fromare
the no seed number/fruit
Spanish Ministerio and individual
de Ciencia y Tecnologı́a seed mass. REN2003-00273,
(BOS2000-1366-C02-01, As expected,CGL2006-
a
differences between
00373) megafaunal
and RNM-305 andAndalucı́a)
(Junta de non-megafaunal
to PJ, CNPqspecies
(Bolsa deinProdutividade),
negativeFAPESP, FUNDUNESP
trend between andvariables
both IFS to MGisand FAPESP
evident in to
thePRG
two(01/1737-3);
groups our
collaborationwhen
seed(s) mass/fruit was also funded by CYTED
accounting and a CNPq-CSIC
for variation in fruitinstitutional
mass agreement.
(Fig. 4b), with individual seed mass decreasing linearly with
P = 0.17, d.f.
(F = 2.11,Competing = 2, 11The
Interests: the a have
forauthors posteriori contrast
declared with
that no fruit interests
competing exist. fruit seediness (F = 126.0, P,0.0001, d.f. = 3, 87). Yet
increasing
mass as the covariate).
* E-mail: jordano@ebd.csic.es megafaunal species have significantly larger seeds when controlling
Mamíferos Modernos

Text
¿Son los Placentarios “Superiores” a los Marsupiales?

a.) Diversidad de Especies: c. 4350 vs. 270 spp.

b.) Diversidad de ambientes y morfología en placentarios

 Reproducción en los Marsupiales

Similitud con Monotremas: mantienen membrana

alrededor del huevo fertilizado, presencia de glándula
de la cáscara.

Cáscara no se mineraliza

Crías nacen sólo después de c. 12-30 días,

pobremente desarrolladas

Crecimiento inicial en útero facilitado por placenta

(coriovitelina)
Reproducción en los Marsupiales
Implantación y Desarrollo del Embrión en Marsupiales
Implantación muy superficial - embrión se acomoda
en depresión panda, muy poca “erosión” de la pared
del útero.

Saco vitelino se expande hasta rodear el embrión,

alantoides se encoge. Da lugar a placenta
coriovitelina.

Embrión bañado por “leche” uterina.

Nutrientes absorbidos de forma muy indirecta -

difusión. No hay contacto con circulación materna.
Implantación y Desarrollo del Embrión en Eutheria
(Eutheria = Verdaderos Placentarios)

Embrión se implanta profundamente en el útero mediante

erosión del endometrio.

Saco vitelino muy importante para nutrición en desarrollo

temprano, luego se absorbe.

Placenta corioalantoica: muy variable entre distintos

eutheria, pero contacto con la madre siempre es más
directo que en marsupiales.Transporte de nutrientes más
eficiente.

Trofoblasto bien desarrollado, recubre al embrión, papel en

la implantación y protección
Coriovitelina
(marsupiales)

Corioalantoica
(Theria)
 Hipótesis del Trofoblasto

Embrión = Organismo Foráneo Respuesta inmune por

la madre

Eutheria: Trofoblasto bien Metatheria: No hay barrera a

desarrollado, gonadotropinas respuesta inmune
coriónicas

Gestación muy corta:

Gestación prolongada: neonatos poco desarrollados
neonatos bien desarrollados

Lactancia Restricciones a
Lactancia corta extendida Morfología de
$ $$$ Extremidades
conflicto evolutivo entre sexos y problemas en gestación
 Hipótesis de las Tasas Metabólicas

Tasas Metabólicas Altas = Sólo posibles cuando hay

Alto Costo Energético calidad o cantidad de
alimento

Eutheria: TMB se relaciona Metatheria: no hay relación

positivamente con capacidad (o muy débil) entre TMB y
reproductiva capacidad reproductiva

En nichos donde TMB altas son posibles

(e.g. ramoneadores, carnívoros),
Eutheria serán competitivamente
superiores
 Hipótesis de Accidentes Históricos
Simplemente, los marsupiales han podido diversificarse
en áreas más pequeñas y en períodos de tiempo más
cortos que los placentarios.
http://bit.ly/jf63x1
Habitat idòneo de la danta de montaña (Tapirus pinchaque)
en los Andes colombianos
C. A. Pedraza (2005)

126  Localidades

56  Variables  ecogeográficas
Lizcano 2008
Felinos Neotropicales
http://www.panthera.org/jaguar_corridor.html
Current Biology Vol 20 No 2
R62

the key finding on which the proposal is
based generalizes over stimulus sets
and methods of achieving invisibility. If
reproducibility does generally correlate
with consciousness, then this could
provide a useful diagnostic criterion.
The hard problem will then be to
demonstrate a causal, mechanistic link
between the reproducibility of a neural
process and its role in consciousness.
References
1. Haynes, J.D. (2009). Decoding visual
consciousness from human brain signals.
Trends Cogn. Sci. 13, 194–202.
2. Owen, A.M., Coleman, M.R., Boly, M.,
Davis, M.H., Laureys, S., and Pickard, J.D.
(2006). Detecting awareness in the vegetative
state. Science 313, 1402.
3. Owen, A.M., Schiff, N.D., and Laureys, S.
(2009). A new era of coma and consciousness
science. Prog. Brain Res. 177, 399–411.
4. Schurger, A., Pereira, F., Treisman, A., and
Cohen, J.D. (2010). Reproducibility
distinguishes conscious from nonconscious
neural representations. Science 327, 97–99.
5. Moutoussis, K., and Zeki, S. (2002). The
relationship between cortical activation and
perception investigated with invisible stimuli.
Proc. Natl. Acad. Sci. USA 99, 9527–9532.
6. Haynes, J.D., and Rees, G. (2006). Decoding
mental states from brain activity in humans.
Nat. Rev. Neurosci. 7, 523–534.
7. Tononi, G., and Edelman, G.M. (1998).
Consciousness and complexity. Science
282, 1846–1851.
8. Dehaene, S., and Naccache, L. (2001). Towards
a cognitive neuroscience of consciousness:
basic evidence and a workspace framework.
Cognition 79, 1–37.
9. Wandell, B.A., Dumoulin, S.O., and Brewer, A.A.
(2007). Visual field maps in human cortex.
Neuron 56, 366–383.
10. Bartels, A., and Zeki, S. (2000). The architecture
of the colour centre in the human visual brain:
new results and a review. Eur. J. Neurosci.
12, 172–193.
11. Jiang, Y., Zhou, K., and He, S. (2007). Human
visual cortex responds to invisible chromatic
flicker. Nat. Neurosci. 10, 657–662.
12. Rao, R.P., and Ballard, D.H. (1999). Predictive
coding in the visual cortex: a functional
interpretation of some extra-classical
receptive-field effects. Nat. Neurosci. 2, 79–87.
13. Murray, S.O., Kersten, D., Olshausen, B.A.,
Schrater, P., and Woods, D.L. (2002). Shape
perception reduces activity in human primary
visual cortex. Proc. Natl. Acad. Sci. USA 99,
15164–15169.
School of Psychology, University of Sydney,
Sydney, NSW 2006, Australia.
E-mail: colinc@psych.usyd.edu.au
DOI: 10.1016/j.cub.2009.12.001

Molecular Evolution: Gene than cellular motor proteins, and its

Convergence in Echolocating contribution to auditory sensitivity in
mammals is immense — a targeted
Mammals deletion of prestin showed a >100-fold
(or 40 dB) loss of auditory sensitivity in
mice [4,5].
A sensory system that places
The motor protein prestin confers sensitive and selective hearing in mammals.
extreme demands on audition
Magazine
Remarkably, prestin amino-acid sequences of echolocating dolphins have
R55 is echolocation. Echolocation
converged to resemble those of distantly related echolocating bats.
involves producing sound — typically,
ultrasound frequencies of >20 kHz —
Gareth Jones Laurasiatheria) [1]. Phylogenies and then receiving and analysing
The hearing gene
Appearances can deceive. Biologists
Rhinolophidae
based
Figure 1Aas
considered —being
and Hipposideridae
on gene sequences
ratherless
than
are often in echoes
susceptible
hadthatto be
phylogenetic
with the cow, Echolocation
removed
return to correct the
from objects.
positionits
has attained of greatest
dolphin,
Prestin unites
are very familiar with examples of its true closest relative
to homoplasy — the possession of
and this unexpected
in our data, sophistication in bats and toothed(referred
and a minimum of five sites
that evolved grouping has a whales to as setasIIIdolphins
in Figureand 1C)porpoises
had to be
echolocating bats
morphological characters that similarities independently such
significant
converge independently in response to in different bootstrap
lineages support
— than (Figure where
are trees removed
it is usedtofor rectify the positions
orientation and of the
and whales
similar selective pressures, resulting in based
the evolution of organisms that are very have
1A). on
Furthermore,
[6],the
morphology,
unlike
asand
the species
potential
recently
tree where
to determine
reported oftentwo
therefore
prey three
microbats.
to detect, Setsand
localise
sites, significantly
[6]. Echolocating
II and III share
classify
animalsexceeding
are
alike in appearance, despite having microbats relationships
evolutionary are paraphyletic in a [7]
more the random
(Figure complex expectation
phenotypically, (P < 0.002,
and show
different ancestry. Such convergent 1B), the
robust andprestin
reliabletree clusters the ten manybinomial
manner. adaptivetest), suggesting that the
specialisations
Ying Li1,2,3can
evolution , Zhen
thenLiu 2,3, Peng
confound Shi2,
the microbats in exclusion
Convergence of gene and of the three misplacements
associated with sound of production
the dolphin and the
reconstruction
and Jianzhi Zhang of evolutionary
1 history. amino-acid
megabatssequences is traditionally
with a moderate bootstrap and hearing. Prestinare
two microbats is unique
in largetopart due to
For example, the hedgehog tenrecs of considered to be rare.
support, resulting inIn
thethis issue of
misplacement mammals,
the same andsites.
its evolution
Madagascar
Echolocationwere long believed
is a sensory to be
mechanism Current
of twoBiology, convergent
purple-labeled research
microbats resultedOurfrom positive
second selection
approach was to