If we make the time animals have
existed to be 1 day, humans have
been around for 61 seconds.
Pushing back the origin of animals
Oldest traces of animals:
~ 645 mya: 24isopropylcholestane (2009)
Oldest animals sponges, ~650 mya
(Science Daily, 2010)
Evolutionary History
of the Metazoa
Mysteries of
ancient animal life
Goals:
Consider the central questions
about the origin of Metazoa.
Review modern evidence about
time of origin, patterns of
evolution, important processes.
Outline for “History of Life”
I.  Cambrian Explosion
II.  What we knew 15 yrs ago
Earth formed
4.6 bya
Meteorites bombard the planet 4.6-3.8 bya
Making it inhabitable
4.5 bya
1st evidence of life
4 bya Fossil b-g algae 3.6 bya
III. More Recent Discoveries
A. New Fossil Discoveries
B. Molecular Dating
IV.  Some explanations for deep divergence
V.  Why so many body plans in Cambrian?
3 bya
2.5 bya
First cells
with nucleus
2.0 bya
1.5 bya
First multicelled algae
1.0 bya
Cambrian Period
543-510 mya
Precambrian, 4.6 bya
To 543 mya
600 mya
543
500 mya
400
Source Newsweek
Biology’s “Big Bang”:
The Cambrian Fauna (543-510 mya)
Astonishing array of
Multicellular life. All
Modern phyla present.
And many
More!
In Burgess Shale alone, 15 of the
33 modern phyla are recognized
n = 40,000
Also 19 unique
body forms of
Unknown affinity
Cambrian Explosion
Cambrian deposits known since 1909 from >34 locations
including the U.S.A., Russia, China, Canada
Morris 1989
1
Summary: ~ 15 years ago
•  Enigmatic Ediacaran assemblage (565 mya), many of
Darwin’s Dilemma
which apparently never survived to the Cambrian
•  A 20 my gap in the fossil record before the Cambrian
•  Cambrian explosion of body plans
All Modern phyla present
and many other types
that did not survive.
Skeletized
fauna
Artist’s rendition of Vendian assemblage
as primitive multicelled animals (565 mya)
Why did the Cambrian Fauna present a challenge to
the Darwinian view of Evolution?
How did Darwin and his contemporary evolutionists
respond to this criticism?
Why does Sukumaran argue that in evaluating the
Cambrian explosion it is important to recognize that
the difference between the concepts of diversity
and disparity ?
Different Views on the Exact Nature
of the Vendian assemblage:
1946: Martin Glaessner, an Australian paleontologist called them
simple soft bodied animals related to jellyfish, corals, segmented
worms
1983: German biologist Adolf Seilacher believed they were
giant single celled organisms; their own kingdom of life; a failed
experiment
1995: Gregory Retalack, Univ. of Oregon, argues they are
ancient lichens (structural expts).
2008: Xiao and Laflamme….biota of protists, fungi, algae, and
metazoa, but there is growing evidence that among the 100 or
so disparate species there were also a few bilateria.
Outline for “History of Life”
I.  Cambrian Explosion
II.  What we knew 15 yrs ago
III. More Recent Discoveries
A. New Fossil Discoveries
B. Molecular Dating
IV.  Some explanations for deep divergence
A. Dating Techniques 1995: Groetzinger et. al .
(Physical Chemistry)
Precise lead and zircon dating of
Vendian-Cambrian boundaries
“bridges” the 20 my gap.
Some Vendian species survive to
the Cambrian; transitional rocks
between Vendian and Cambrian
explosion bear traces of
metazoan life gaining momentum.
Ediacara
Fauna
V.  Why so many body plans in Cambrian?
2
A. New Fossil Discoveries: Diploblasts
Stromatoveris from early Cambrian
Modern Comb Jelly
Is strikingly similar to
Pre-Cambrian Fronds
A. New Fossil Discoveries
Phosphatized remains
1997-98 Li et. al. & Xiao et al.
Report finding
multicellular
sponges, and
embryos of
various phyla
in 570 + 20 mya
formation.
Prof. Shuhai Xiao, Virginia Tech Univ.
Review
Trends in Ecology and Evolution Vol.24 No.1
The phylogenetic uncertainty of Ediacara organisms not
only limits their role in testing hypotheses about the tempo
of early animal evolution but also compromises our ability
to interpret their ecology using modern analogs. Fortunately, ecological inferences can be independently made on
the basis of trace fossils, functional morphology and taphonomy. In the past decade, investigation of trace fossils
associated with Ediacara body fossils has shed important
light on the autecology of several Ediacara taxa, whereas
recent advances in the paleoecology of Ediacara organisms
[9] are of close relevance to the evolutionary radiation in
the Ediacaran–Cambrian transition.
The Ediacaran–Cambrian transition marks a rapid
change in taxonomic diversity, morphological disparity
and ecosystem complexity of early animals. Does the early
evolution of the Ediacara biota share similar patterns with
the Cambrian radiation of animals? Only recently have
paleontologists begun to approach this question using
quantitative methods and a growing database of Ediacara
fossils [10,11].
Promising results from emerging research of the phylogenic affinities, ecological diversity and evolutionary patterns of the Ediacara biota prompt this review. Thus, we
will begin with a brief description of the spatial–temporal
distribution and bodyplan diversity of the Ediacara biota,
followed by a review of recent advances in the phylogenetic,
paleoecological and evolutionary analyses of this biota.
Emphasis is restricted to classical Ediacara fossils that
are soft bodied, macroscopic and morphologically diverse.
The Ediacara biota in space and time
Ediacara fossils are mostly restricted between 575 and
541 Ma (Figure 1; Box 1). Discoid fossils from the
>635 Ma Twitya Formation in northwestern Canada
[12] are similar to some simple forms in the Ediacara biota,
but the absence of co-occurring complex forms and their
significantly older age suggest that the Twitya discs are
possibly simple forerunners rather than parts (e.g. holdfasts) of complex Ediacara fossils. A few Cambrian fossils
are interpreted as Ediacara survivors or as phyletic descendants [13,14], but with rare exceptions [14] the most
iconic members of the Ediacara biota – the rangeomorphs
and erniettomorphs (Box 2), for example – are unknown in
the Cambrian. It has been proposed that the demise of the
Ediacara biota might be due to the closure of a unique
taphonomic window mediated by microbial activities
[4,15], and that the Ediacara biota continued to strive after
the Cambrian radiation but were simply not preserved.
However, the scarcity of Ediacara fossils in exceptionally
preserved Cambrian biota such as the Burgess Shale [16]
points to a more likely scenario of extinction or at least
ecological restriction [2].
The restricted temporal distribution is in contrast with
a wide spatial distribution of the Ediacara biota. Ediacara
Downloaded from rstb.royalsocietypublishing.org on 24 August 2009
Closing the 20 my Gap
Earliest fossil record of animals
Xiao and Laflamme 2008:
“On the eve of animal radiation..”
500
Burgess Shale
preservation
510
520
8
530
540
C
Ediacaran
formative
interval
Gaskiers glaciation
2
620
B
640
Marinoan glaciation
650
660
Figure 1. Temporal distribution (bars) and stratigraphic occurrences (black dots) of representative Ediacara genera, plotted against timescale of Ediacaran Period and fossil
localities or stratigraphic units. The three Ediacara assemblages (Box 1) are indicated by different shades of gray. The Marinoan and Gaskiers glaciations, as well as the age
range of the Doushantuo biota, are also marked. Modified from Ref. [58] with permission from the AAAS.
32
Budd, 2009.
Philosophical Trans. Of the Royal Soc.
The Earliest Fossil Record of Animals and
Its Significance
Trends in Ecology and Evolution Vol.24 No.1
7
610
630
Review
5
E
590
600
The Ediacara fauna bridges the evolution of
multicellular life leading to the Cambrian fauna
Lower
Cambrian
570
580 D
1427
6
3
550
560
4
1
G. E. Budd
Ordovician
(part)
Upper
Cambrian
Middle
Cambrian
490
A
Figure 1. Provisional time scale for events around the
Precambrian–Cambrian boundary. 1, range of large, acanthomorphic ‘Ediacaran’ acritarchs (a genus that contains metazoan like embryos is found from close to the bottom of their range just
above the Marinoan glaciation rocks); 2, possible range of the
Doushantuo embryos and cnidarian-like fossils according to
Barfod et al. (2002); 3, possible range of the same according to
Condon et al. (2005) (which is correct is uncertain, but the
former is favoured here); 4, the ‘Ediacaran’ biota; 5, trace
fossils; 6, Cloudina and Namacalathus; 7, classical small shell
fossils; 8, trilobites. The alphabets correspond to the key dated
points in metazoan evolution in Peterson & Butterfield
(2005) based on minimum evolution: A, origin of crown-group
Metazoa; B, total-group Eumetazoa; C, crown-group Eumetazoa; D, crown-group bilateria (here equivalent to ProtostomiaCDeuterostomia); E, crown-group Protostomia. The
‘formative interval’ during which distinctive bilaterian features
were assembled according to this dating is marked by arrows.
Doushantuo Fm would have to be incorrect (Barfod
et al. 2002), but given the care required to interpret the
whole-rock radiometric dates, this possibility cannot
simply be ruled out.
More recently, the claim has been made that at least
one of the enigmatic acanthomorphic (i.e. spinose)
acritarchs (figure 1), which are normally assigned to
protist groups such as the green algae and the
dinoflagellates, are actually the hulls of diapause animal
eggs ( Yin et al. 2004, 2007). Although the fossil in
question, Tianzhushania, is known to contain embryos
Phil. Trans. R. Soc. B (2008)
Figure 2. The Ediacaran acanthomorphic acritarch Tanarium
pluriprotensum from the Tanana Formation, in the Giles 1
drillcore, Officer Basin, Australia; 100!. At least some
Precambrian acanthomorphic acritarchs may be the eggs of
animals. Courtesy of S. Willman.
only in the upper part of the Doushantuo Fm, it ranges
down to very close to the base, and thus to 630 Myr ago
or so. The claim would be that the oldest animal fossils
of the Doushantuo Fm, dating back to just after the
Nantuo glaciation (i.e. the Chinese glacial deposits
normally correlated with the Marinoan) are of this age,
a time that predates the first Ediacaran fossils by some
60 Myr, as well as the more conservative molecular
clock estimates for the divergence of the bilaterians.
Despite the obvious uncertainties, the most reasonable interpretation of the data thus is that embryoforming animals of some sort had evolved by just after
Marinoan time, and that sponges and presumed other
animals had started to emerge by 580 Myr ago at the
latest, and that the Ediacaran biotas are likely to be a
little younger than the Doushantuo embryos. The
upshot of the new data is that considerably more
convincing evidence exists in the fossil record for an
origin of the animals considerably before the Cambrian
than it did 10 years ago (Budd & Jensen 2000), with an
inferred documented fossil origin of the entire clade
being datable to just after 635 Myr ago—a significant
result (see figure 2 for summary).
If animals had already evolved at this time, why is it
that the rest of the record does not correlate with it—why
no macro body fossils and why no (generally accepted)
trace fossils? The answer to this question, which on
the face of it seems directly to contradict predictions
(Budd & Jensen 2000) that no animals existed
significantly before the first good trace fossils at ca
555 Myr ago, may hinge on what sort of organisms these
embryos represent. Given their relatively unusual
development, with large numbers of cell divisions taking
place without the sign of gastrulation or epithelial
formation, it has been suggested that they are from
stem-group metazoans, i.e. from the organisms more
basal than any living animals including sponges
(Hagadorn et al. 2006). Given that such an organism,
lacking muscles and other features of the more derived
bilaterians, would be unlikely readily to form either body
or trace fossils, such an assignment is consistent with the
hypothesis that bilaterians emerged later, close to
Figure 2. Possible phylogenetic placement of bilateral Ediacara fossils (vendomorphs, parvancorinomorphs, Yorgia, Kimberella and Dickinsonia), tri-, tetra-, penta- and
octoradial forms, and rangeomorphs in the metazoan tree. The diverse array of morphological constructions exemplified by the Ediacara biota suggests a greater
phylogenetic diversity than typically assumed. Ediacara fossils are represented by dotted lines or triangles, extant animals by gray triangles.
To summarize, it is important to realize that the Ediacara biota consists of an assortment of phylogenetically
diverse taxa, possibly ranging from microbial colonies,
algae, fungi and protists to animals, including bilaterian
animals [2,39,40]. Just as important, the Ediacara biota
likely comprises stem-group members of various extant
clades. These stem groups might have some, but not all
features that collectively define extant crown clades.
Therefore, extreme approaches to push Ediacara fossils
into the crown-group Metazoa on the basis of plesiomorphies, or to relegate them into the phylogenetically distant
Vendobionta because of the lack of crown-group synapormorphies, are equally undesirable. Given the phylogenetic
uncertainties of many Ediacara fossils, paleoecologists are
facing a daunting task to understand the ecological makeup of Ediacara communities using modern analogs.
Ecological diversity
Some Ediacara fossils appear to be preserved where they
lived, which offers exceptional opportunities for analysis of
community ecology. Such analyses [41–43] show that most
members of the Ediacara biota were epibenthic organisms,
with a few possible examples of shallow endobenthic
(entirely buried; Pteridinium) and semi-endobenthic
36
(half-exposed and half-buried; Ernietta) organisms
[44,45]. Additional evidence for epibenthic and endobenthic activities comes from shallow burrows and sediment surface traces [34], but there is no convincing
evidence for pelagic or deep endobenthic animals.
Perhaps the most noticeable ecological difference from
Phanerozoic epibenthic communities is the dominance of
sessile organisms in the Ediacara biota. All rangeomorphs
appear to have been nonmotile, typically attached to a
holdfast (e.g. Charnia) [46] or lying freely on the seafloor
(e.g. Fractofusus) [47]. Many other Ediacara fossils, including Palaeophragmodictya, tri-, tetra-, penta- and octoradial forms, are also likely to have been attached or freely
lying on the seafloor. Although vendomorphs and parvancorinomorphs were interpreted as relatives of arthropods,
there is no convincing evidence for motility. Yorgia and
Dickinsonia moved intermittently, facultatively and perhaps passively. Only Kimberella seems to have actively
pushed sediments during self-powered movement [8,32].
The subordinate role of motile animals is also supported by
the lower abundance and diversity of trace fossils in Ediacaran rocks than in Phanerozoic rocks [34].
Although Ediacara communities were likely supported
by cyanobacterial and algal primary producers [48], the
3
New fossil discoveries show the presence of complex (but
soft-bodied) animal life before the Cambrian (~570 mya)
Vertebrates Without Jaws (Extinct)
The first Craniates Ca. 530 mya
Yunnanozoon
Myllokunmingia
Haikouella
Ca. 530 mya
Outline for “History of Life”
I.  Cambrian Explosion
What does Sukumaran mean by the term
“deep divergence” ?
II.  What we knew 15 yrs ago
III. More Recent Discoveries
What is the procedure known as “molecular
3. Explain the concept of disparity and what point does the author try to make about
dating” and
how
is itfauna?used to estimate the
the disparity
of the Cambrian
divergence times for animal phyla?
A. Improved Dating Techniques
B. New Fossil Discoveries
C. Molecular Dating
IV.  Some explanations for deep divergence
V.  Why so many body plans in Cambrian?
Genetic Evidence : sequence analyses can provide
information on relatedness AND time of divergence
Calibrating the molecular clock
Descendant
Taxon A
Determine
% difference
In mtDNA
Descendant Gene sequence
Taxon B
Fossil
Ancestor of
A & B
Age Known
From fossil
record
% difference
years
Molecular
Clock Rate
years
Extant
species
1996. Wray et. al. estimate time of
divergence of some phyla at 1 to 1.2 mya
e.g. nucelotide
substitutions
Per 10 million years
Used vertebrate clock data to estimate divergence times
But, Not all molecular clock rates are the same!
4
Fig. 2. ML tree of the seven concatenated protein sequences from 18 in-group taxa
by using Arabidopsis as the outgroup. Shows a slower molecular clock for 8 genes among the
vertebrates, and a faster rate among invertebrates that is consistent between groups
1998 Ayala et al.
Added Many genes to the
analysis and discard
genes that show variable
molecular clock rates
Peterson, Kevin J. et al. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541
Copyright ©2004 by the National Academy of Sciences
Fig. 4. Metazoan divergence estimates with metazoan diversity and phylogeny
(7 different a.a. sequences from 23 taxa)
§  What were the ancestors of the Cambrian Fauna?
(Ediacaran fauna? 20 my gap?)
§  When did the major lineages appear?
(support for cryptic pre-Cambrian history > 600 mya,
unique and skeletized body plans appear later.... Referred
to as “deep divergence”)
§  Why was there a burst of body plan diversity
starting in the middle Cambrian?
Peterson, Kevin J. et al. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541
Copyright ©2004 by the National Academy of Sciences
Outline for “History of Life”
I.  Cambrian Explosion
What are HOX genes?
II.  What we knew 15 yrs ago
Is it possible that the evolution of HOX
genes might help explain the rapid origin of
diverse body plans and skeletal fauna in the
Cambrian?
III. More Recent Discoveries
A. Improved Dating Techniques
B. New Fossil Discoveries
C. Molecular Dating
IV.  Some explanations for deep divergence
V.  Why so many body plans in Cambrian?
* A simple pair of Hox genes is present in
modern Cnidaria
* Basal flatworms have 4 sets
* Other Bilateria have 9-11 hox genes
5
Transcription factors, like Hox
proteins or Fox
proteins, recognize specific
sequences in the regulatory
regions of downstream target
genes, usually motifs present in the
50 or ‘‘upstream’’ region of the
gene, and when bound they regulate
the transcription of the target
,
gene. miRNAs
on the other
hand, are regulatory RNA molecules
that recognize specific sequences
in the 30 untranslated region
(30UTR) of messenger RNA
molecules, and once bound to a
target site ultimately prevent the
translation of the messenger RNA.
(53)
•  miRNAs increase genic precision by turning an imprecise number of
mRNA transcripts into a more precise number of protein molecules
•  By reducing gene expression variability they also increase heritability
and allow natural selection to elaborate morphological
complexity
•  More complex animals have more miRNAs
•  Origin and elaboration of miRNA systems may have contributed to the
high rate of morphological diversification in the Cambrian Explosion
Transcription factors, like Hox
proteins or Fox
proteins, recognize specific
sequences in the regulatory
regions of downstream target
genes, usually motifs present in the
50 or ‘‘upstream’’ region of the
gene, and when bound they regulate
the transcription of the target
What are HOX genes?
,
Is it possible that the evolution of HOX
genes might help explain the rapid origin of
diverse body plans and skeletal fauna in the
Cambrian?
gene. miRNAs
on the other
hand, are regulatory RNA molecules
that recognize specific sequences
in the 30 untranslated region
(30UTR) of messenger RNA
molecules, and once bound to a
target site ultimately prevent the
translation of the messenger RNA.
(53)
What evidence indicates that the evolution
of miRNAs may have played a role in the
early evolution of animal life?
Conclusions:
• Vendian fauna includes representatives of some modern
phyla. They and others that apparently did not leave
many fossils contributed to the Cambrian fauna.
• Ancestors of Metazoa were around at least 30-80 million
years before the Cambrian. ‘Explosion’ may be a more
gradual radiation.
• Did the evolution of genetic and developmental complexity
contribute to the origin of so many body plans?
Why so many species in the Cambrian? Why a
surge of organisms with a skeleton?
warm
Ghaub/Nantuo
Ice Age
Gaskers Ice age
6
warm
Ghaub/Nantuo
Ice Age
Post Cambrian Evolution in a Nut-Shell
One possibility: Oxygen
100
80
50
30
10
Gaskers Ice age
Animal life after the Cambrian
Angiosperms
Invasion of land
Reptiles
Chordates
% of
Present 5
oxygen 3
Exoskeletons
Thresholds for
large size?
Skeletal body?
Multicellular organisms
2
1
Aerobic
bacteria
Eukaryotes
First life
4,000
3,000
2,000 1,000
500
250
Millions of years ago
100
400 mya
300 mya
200 mya
100 mya
P
500-450 mya first land invertebrates
438 mya: first vertebrates
400 mya: jawed fishes
360 mya: amphibians, bony fish
320-280: conifers, insects, reptiles
144 mya: mammals and birds, giant dinosaurs
65 mya: dinosaurs extinct
Five major extinctions of marine animals
Ammonites
extinct with the
Dinosaurs.
Mesozoic
Trilobites
Paleozoic
Extinction of
some major
groups:
Cenozoic
Annelida
Tard. Cheli. Remipedia
Onych. Trilob. Crust. Insecta
Quaternary Tertiary Cretaceous Jurassic Triassic Permian Carboniferous Devonian Silurian Ordovician Cambrian Precambrian 7
Great Mysteries of Early Animal Life
1. What were the ~30 forms in the Ediacara?
2. Gap of 20 my real? Or were Vendian animals
precursors to the Cambrian fauna?
3. Where are the ancestors of the Cambrian Phyla?
4. What conditions (ecological, evolutionary) contributed
to great surge of life forms?
Much has been learned in the past 10 years!!
8