If we make the time animals have Evolutionary History existed to be 1 day, humans have of the Metazoa been around for 61 seconds.

Pushing back the origin of animals Mysteries of ancient animal life Oldest traces of animals: ~ 645 mya: 24- Goals: isopropylcholestane (2009) Consider the central questions Oldest animals sponges, ~650 mya about the origin of Metazoa. (Science Daily, 2010) Review modern evidence about time of origin, patterns of evolution, important processes.

“ ” Outline for History of Life Meteorites bombard the planet 4.6-3.8 bya Making it inhabitable I. Cambrian Explosion Earth formed 4.5 bya 4.6 bya 1st evidence of life 4 bya II. What we knew 15 yrs ago Fossil b-g algae 3.6 bya

III. More Recent Discoveries 3 bya A. New Fossil Discoveries 2.5 bya First cells 2.0 bya 1.5 bya B. Molecular Dating with nucleus First multicelled algae

IV. Some explanations for deep divergence 1.0 bya Cambrian Period V. Why so many body plans in Cambrian? Precambrian, 4.6 bya 543-510 mya To 543 mya

600 mya 543 500 mya 400

Source Newsweek

Biology’s “Big Bang”: The Cambrian Fauna (543-510 mya) In Burgess Shale alone, 15 of the 33 modern phyla are recognized

n = 40,000 Astonishing array of And many Multicellular life. All More! Modern phyla present. 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 Why did the Cambrian Fauna present a challenge to the Darwinian view of Evolution? • Cambrian explosion of body plans

Skeletized How did Darwin and his contemporary evolutionists fauna respond to this criticism? All Modern phyla present and many other types that did not survive. 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 ?

Artist’s rendition of Vendian assemblage Different Views on the Exact Nature as primitive multicelled animals (565 mya) 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” A. Dating Techniques 1995: Groetzinger et. al . (Physical Chemistry) I. Cambrian Explosion

II. What we knew 15 yrs ago Precise lead and zircon dating of Vendian-Cambrian boundaries III. More Recent Discoveries “bridges” the 20 my gap.

A. New Fossil Discoveries Some Vendian species survive to the Cambrian; transitional rocks B. Molecular Dating between Vendian and Cambrian explosion bear traces of Ediacara IV. Some explanations for deep divergence metazoan life gaining momentum. 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 Emphasis is restricted to classical Ediacara fossils that only limits their role in testing hypotheses about the tempo are soft bodied, macroscopic and morphologically diverse. of early animal evolution but also compromises our ability to interpret their ecology using modern analogs. Fortu- The Ediacara biota in space and time nately, ecological inferences can be independently made on Ediacara fossils are mostly restricted between 575 and the basis of trace fossils, functional morphology and taph- 541 Ma (Figure 1; Box 1). Discoid fossils from the onomy. In the past decade, investigation of trace fossils >635 Ma Twitya Formation in northwestern Canada associated with Ediacara body fossils has shed important [12] are similar to some simple forms in the Ediacara biota, light on the autecology of several Ediacara taxa, whereas but the absence of co-occurring complex forms and their recent advances in the paleoecology of Ediacara organisms significantly older age suggest that the Twitya discs are [9] are of close relevance to the evolutionary radiation in possibly simple forerunners rather than parts (e.g. hold- the Ediacaran–Cambrian transition. fasts) of complex Ediacara fossils. A few Cambrian fossils The Ediacaran–Cambrian transition marks a rapid are interpreted as Ediacara survivors or as phyletic des- change in taxonomic diversity, morphological disparity cendants [13,14], but with rare exceptions [14] the most and ecosystem complexity of early animals. Does the early iconic members of the Ediacara biota – the rangeomorphs Downloaded from rstb.royalsocietypublishing.org on 24 August 2009 evolution of the Ediacara biota share similar patterns with and erniettomorphs (Box 2), for example – are unknown in the Cambrian radiation of animals? Only recently have the Cambrian. It has been proposed that the demise of the Earliest fossil record of animals G. E. Budd 1427 paleontologists begun to approach this question using Ediacara biota might be due to the closure of a unique quantitativeClosing methods and a growing databasethe of Ediacara 20taphonomic my window mediatedGap by microbial activities fossils [10,11]. [4,15], and that the Ediacara biota continued to strive after Ordovician (part) The Ediacara fauna bridges the evolution of Promising results from emerging research of the phylo- the Cambrian radiation but were simply not preserved. 490 genic affinities, ecological diversity and evolutionary pat- However, the scarcity of Ediacara fossils in exceptionally Upper terns of theXiao Ediacara biota promptand this review.Laflamme Thus, we preserved Cambrian 2008: biota such as the Burgess Shale [16] 500 Cambrian will begin with a brief description of the spatial–temporal points to a more likely scenario of extinction or at least Middle multicellular life leading to the Cambrian fauna distribution and bodyplan diversity of the Ediacara biota, ecological restriction [2]. 510 Burgess Shale Cambrian Review Trends in Ecology and Evolution Vol.24 No.1 followed by a“On review of recent the advances ineve the phylogenetic, of animalThe restricted temporal radiation..” distribution is in contrast with preservation paleoecological and evolutionary analyses of this biota. a wide spatial distribution of the Ediacara biota. Ediacara 520 8 Lower 530 Cambrian 4 1 6 540 7 3 550

560 5 E 570 Figure 2. The Ediacaran acanthomorphic acritarch Tanarium pluriprotensum from the Tanana Formation, in the Giles 1 580 D drillcore, Officer Basin, Australia; 100!. At least some Gaskiers glaciation Precambrian acanthomorphic acritarchs may be the eggs of 590 animals. Courtesy of S. Willman. Ediacaran interval

formative only in the upper part of the Doushantuo Fm, it ranges 600 2 C down to very close to the base, and thus to 630 Myr ago 610 or so. The claim would be that the oldest animal fossils of the Doushantuo Fm, dating back to just after the 620 Nantuo glaciation (i.e. the Chinese glacial deposits normally correlated with the Marinoan) are of this age, 630 a time that predates the first Ediacaran fossils by some B Marinoan glaciation 60 Myr, as well as the more conservative molecular 640 clock estimates for the divergence of the bilaterians. Despite the obvious uncertainties, the most reason- 650 able interpretation of the data thus is that embryo- forming animals of some sort had evolved by just after 660 A Marinoan time, and that sponges and presumed other animals had started to emerge by 580 Myr ago at the Figure 1. Provisional time scale for events around the latest, and that the Ediacaran biotas are likely to be a Precambrian–Cambrian boundary. 1, range of large, acantho- little younger than the Doushantuo embryos. The morphic‘Ediacaran’acritarchs (a genus thatcontains metazoan- upshot of the new data is that considerably more like embryos is found from close to the bottom of their range just above the Marinoan glaciation rocks); 2, possible range of the convincing evidence exists in the fossil record for an Figure 1. Temporal distribution (bars) and stratigraphic occurrences (black dots) of representative Ediacara genera, plotted against timescale of Ediacaran Period and fossil origin of the animals considerably before the Cambrian 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 Doushantuo embryos and cnidarian-like fossils according to range of the Doushantuo biota, are also marked. Modified from Ref. [58] with permission from the AAAS. Barfod et al. (2002);3,possiblerangeofthesameaccordingto than it did 10 years ago (Budd & Jensen 2000), with an Condon et al. (2005) (which is correct is uncertain, but the inferred documented fossil origin of the entire clade Figure 2. Possible phylogenetic placement of bilateral Ediacara fossils (vendomorphs, parvancorinomorphs, Yorgia, Kimberella and Dickinsonia), tri-, tetra-, penta- and 32 former is favoured here); 4, the ‘Ediacaran’ biota; 5, trace being datable to just after 635 Myr ago—a significant octoradial forms, and rangeomorphs in the metazoan tree. The diverse array of morphological constructions exemplified by the Ediacara biota suggests a greater fossils; 6, Cloudina and Namacalathus;7,classicalsmallshell result (see figure 2 for summary). phylogenetic diversity than typically assumed. Ediacara fossils are represented by dotted lines or triangles, extant animals by gray triangles. Budd, 2009. fossils; 8, trilobites. The alphabets correspond to the key dated If animals had already evolved at this time, why is it points in metazoan evolution in Peterson & Butterfield that the rest of the record does not correlate with it—why To summarize, it is important to realize that the Edia- (half-exposed and half-buried; Ernietta) organisms (2005) based on minimum evolution: A, origin of crown-group no macro body fossils and why no (generally accepted) cara biota consists of an assortment of phylogenetically [44,45]. Additional evidence for epibenthic and endo- Metazoa; B, total-group Eumetazoa; C, crown-group Eume- Philosophical Trans. Of the Royal Soc. trace fossils? The answer to this question, which on tazoa; D, crown-group bilateria (here equivalent to Protosto- diverse taxa, possibly ranging from microbial colonies, benthic activities comes from shallow burrows and sedi- The Earliest Fossil Record of Animals and miaCDeuterostomia); E, crown-group Protostomia. The the face of it seems directly to contradict predictions algae, fungi and protists to animals, including bilaterian ment surface traces [34], but there is no convincing ‘formative interval’ during which distinctive bilaterian features (Budd & Jensen 2000)thatnoanimalsexisted animals [2,39,40]. Just as important, the Ediacara biota evidence for pelagic or deep endobenthic animals. Its Significance were assembled according to this dating is marked by arrows. significantly before the first good trace fossils at ca likely comprises stem-group members of various extant Perhaps the most noticeable ecological difference from 555 Myr ago, may hinge on what sort of organisms these clades. These stem groups might have some, but not all Phanerozoic epibenthic communities is the dominance of Doushantuo Fm would have to be incorrect (Barfod embryos represent. Given their relatively unusual features that collectively define extant crown clades. sessile organisms in the Ediacara biota. All rangeomorphs et al. 2002), but given the care required to interpret the development, with large numbers of cell divisions taking Therefore, extreme approaches to push Ediacara fossils appear to have been nonmotile, typically attached to a whole-rock radiometric dates, this possibility cannot place without the sign of gastrulation or epithelial into the crown-group Metazoa on the basis of plesiomor- holdfast (e.g. Charnia) [46] or lying freely on the seafloor simply be ruled out. formation, it has been suggested that they are from phies, or to relegate them into the phylogenetically distant (e.g. Fractofusus) [47]. Many other Ediacara fossils, in- More recently, the claim has been made that at least stem-group metazoans, i.e. from the organisms more Vendobionta because of the lack of crown-group synapor- cluding Palaeophragmodictya, tri-, tetra-, penta- and octor- one of the enigmatic acanthomorphic (i.e. spinose) basal than any living animals including sponges morphies, are equally undesirable. Given the phylogenetic adial forms, are also likely to have been attached or freely acritarchs (figure 1), which are normally assigned to (Hagadorn et al. 2006). Given that such an organism, uncertainties of many Ediacara fossils, paleoecologists are lying on the seafloor. Although vendomorphs and parvan- protist groups such as the green algae and the lacking muscles and other features of the more derived facing a daunting task to understand the ecological make- corinomorphs were interpreted as relatives of arthropods, dinoflagellates, are actually the hulls of diapause animal bilaterians, would be unlikely readily to form either body up of Ediacara communities using modern analogs. there is no convincing evidence for motility. Yorgia and eggs ( Yin et al. 2004, 2007). Although the fossil in or trace fossils, such an assignment is consistent with the Dickinsonia moved intermittently, facultatively and per- question, Tianzhushania, is known to contain embryos hypothesis that bilaterians emerged later, close to Ecological diversity haps passively. Only Kimberella seems to have actively Phil. Trans. R. Soc. B (2008) Some Ediacara fossils appear to be preserved where they pushed sediments during self-powered movement [8,32]. lived, which offers exceptional opportunities for analysis of The subordinate role of motile animals is also supported by community ecology. Such analyses [41–43] show that most the lower abundance and diversity of trace fossils in Edia- members of the Ediacara biota were epibenthic organisms, caran rocks than in Phanerozoic rocks [34]. with a few possible examples of shallow endobenthic Although Ediacara communities were likely supported (entirely buried; Pteridinium) and semi-endobenthic by cyanobacterial and algal primary producers [48], the

36 3 New fossil discoveries show the presence of complex (but Vertebrates Without Jaws (Extinct) soft-bodied) animal life before the Cambrian (~570 mya) 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 A. Improved Dating Techniques What is the procedure known as “molecular 3. Explain the concept of disparity and what point does the author try to make about dating” andthe disparity how of the Cambrian is it fauna? used to estimate the B. New Fossil Discoveries divergence times for animal phyla? C. Molecular Dating IV. Some explanations for deep divergence V. Why so many body plans in Cambrian?

Genetic Evidence : sequence analyses can provide 1996. Wray et. al. estimate time of information on relatedness AND time of divergence divergence of some phyla at 1 to 1.2 mya Calibrating the molecular clock

Descendant Taxon A Determine % difference Fossil % difference years Ancestor of In mtDNA A & B Descendant Gene sequence Taxon B Molecular years Clock Rate Used vertebrate clock data to estimate divergence times Age Known Extant e.g. nucelotide But, Not all molecular clock rates are the same! From fossil substitutions species Per 10 million years record

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 III. More Recent Discoveries genes might help explain the rapid origin of diverse body plans and skeletal fauna in the A. Improved Dating Techniques Cambrian? B. New Fossil Discoveries C. Molecular Dating * A simple pair of Hox genes is present in modern Cnidaria IV. Some explanations for deep divergence * Basal flatworms have 4 sets V. Why so many body plans in Cambrian? * 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 • miRNAs increase genic precision by turning an imprecise number of (30UTR) of messenger RNA molecules, and once bound to a mRNA transcripts into a more precise number of protein molecules target site ultimately prevent the translation of the messenger RNA. (53) • 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 What are HOX genes? 50 or ‘‘upstream’’ region of the gene, and when bound they regulate the transcription of the target

Is it possible that the evolution of HOX gene. miRNAs, on the other hand, are regulatory RNA molecules genes might help explain the rapid origin of that recognize specific sequences in the 30 untranslated region diverse body plans and skeletal fauna in the (30UTR) of messenger RNA molecules, and once bound to a target site ultimately prevent the Cambrian? 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 Gaskers Ice age

One possibility: Oxygen Post Cambrian Evolution in a Nut-Shell Animal life after the Cambrian

100 80 Angiosperms 50 Invasion of land Reptiles 30 Chordates 10 % of Exoskeletons 400 mya 300 mya 200 mya 100 mya P Present 5 Multicellular organisms Thresholds for oxygen 3 large size? 500-450 mya first land invertebrates 2 Eukaryotes Skeletal body? 438 mya: first vertebrates 1 Aerobic bacteria 400 mya: jawed fishes 360 mya: amphibians, bony fish First life 320-280: conifers, insects, reptiles 144 mya: mammals and birds, giant dinosaurs 4,000 3,000 2,000 1,000 500 250 100 65 mya: dinosaurs extinct Millions of years ago

Annelida Tard. Cheli. Remipedia Five major extinctions of marine animals Onych. Trilob. Crust. Insecta

Quaternary Extinction of

some major Tertiary Cenozoic Cenozoic

groups: Cretaceous

Jurassic

Trilobites Mesozoic Triassic

Permian

Ammonites Carboniferous

extinct with the Devonian

Dinosaurs. Silurian

Paleozoic Paleozoic

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