The great naturalhistory museums of the world, in Paris, London, New York, Chicago, and Cleveland, boast of magnificenthalls of ancientlife. Dioramasface the corridor,beginning with the oldest layers of rock in which huge numbers of invertebrate animal The "Sudden skeletons have been found. Simple trilobites, segmented worms, brachiopods, and solitary corals (fig. 1) inhabited ancient seas some 580 million years E I *nt ago during Cambriantimes (fig. 2). By the Ordovician Period, beginning about 480 million years ago, new groups of animals appeared:cephalopods, graptolites, Animal Fossils colonial bryozoans, and primitive fishes made their debut, as reconstructedby, for example, fossiliferous limestones underlying what is now Cincinnati. Later, Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021 About 600 Million by the Devonian Period, which began 400 millionyears ago, huge reef-likecomplexes extended for kilometers across shallow seas. These calcareous mounds were Years Ago: Why? formed by coralsand cemented by "stromatoporoids," tiny, rectangular skeletalized animals. Most paleon- tologists believe stromatoporoids were colonial sponges with calcium carbonate spicules. The museumgoer delights in undersea worlds which are Sharon Kaveski now entirely extinct. What was the scenario before the Cambrian?The Lynn Margulis rocks underlying those from Cambriantimes in many parts of the world are folded and metamorphosed by high temperaturesand pressures. Yet, some sedimen- tary rocks as old as 3,500 million years, far more an- cient than those of the Cambrian Period, have also been found which seem to be devoid of animal fossils. Why? The "sudden appearance" of invertebrate fossil skeletons in different sediments from many parts of the world about 600 million years ago (at the base of the Cambrian)has been referred to, for example, by Princeton paleontologist A. Fischer and many others as the "most vexing" of all paleontological problems. What happened between 3,500 and 600 million years ago? Why do the many older rocks lack clear evidence of animal remains?Does the sudden appearanceof in- vertebratessupport a contention that all animals were Sharon Kaveski received her B.A. degree in biology from Boston University,where she concentratedin evolutionarybiology. She has created simultaneously? Did it take most of Earth also studied marinescience at the Universityof Miami-CoralGables, history for life itself to emerge from non-life? Did Florida,and participatedin an intensive shipboard oceanography shocking catastrophes in the form of worldwide programat OccidentalCollege in Los Angeles. Lynn Margulisis a professor of biology at the Boston University Biological Science volcanoes and earthquakespreclude life from gaining Center, Boston, MA 02215, where she has taught since 1967. She a foothold among the chaos? received her A.B. degree from the University of Chicago, her M.S. Many attempts have been made to explain the degree fromthe Universityof Wisconsin,and her Ph.D. degree from the University of California-Berkeley.Her research interests have Precambrian boundary problem, the comparative taken her to Mexico, Ghana, Brazil, and Spain. She worked on paucity of Precambrian animal fossils, and their elementary school science curriculumreform for the U.S., Colom- remarkableabundance in the PhanerozoicAeon, in all bia, and Africa.She has receivedmany awardsincluding the Boston UniversityFaculty Publication Merit Award (1967)and the Sherman marine fossiliferous strata since the base of the Cam- FairchildFellowship at the CalifomiaInstitute of Technology(1977). brian. Perhaps the most satisfactoryexplanation is the Dr. Margulisis a fellow of AAAS, and a Guggenheim Foundation one we present here: there is no "Precambrianbound- Fellow. She has publishedextensively (see ABT43(9):482).Her most recent book is EarlyLife, Science Books International,Boston, MA ary problem" at all. It depends on how you look at (1982). evolution.

76 THE AMERICAN BIOLOGY TEACHER, VOLUME 45, NO. 2, FEBRUARY 1983 9K ~9 , t-g ~ ~ ~ ~ 4~

FIGURE 1. Cambrian scene, Cambrian fauna. The beginning of the Phanerozoic Aeon: a marinelandscape of the Cambrian Periodnearly 600 million years ago. (Draw- ing by Laszlo Meszoly, reprinted from M7 ~ B Margulis,Early Life, 1982, with permission of ScienceBooks International, Boston MA.) Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021

At Ediacara remarkable animal fossils have been The Boundary and the EdiacaranFauna found in rocks beneath those harboring Cambrian When we examine the nature of the famous Precam- trilobitesand brachiopods. As imprints in sandstones brian/Cambrian boundary, we find that nearly or casts of bodies, these animals have been identified everywhere that it has been studied there lies an un- as part of a rich marinefauna by MartinGlaessner and conformity,or missing sequence of rocklayers between his colleagues of the University of Adelaide. Six ex- the barrenPrecambrian and the overlying fossiliferous tinct genera of jellyfish as well as soft corals related Cambrian-for example in Wales (the ancientname for to today's sea pens have been identified. Segmented which was Cambria),or in the Grand Canyon of nor- annelid worms with strong head shields and odd, thern Arizona (fig. 3). This unconformity really does bilaterally symmetrical, worm-like fossils are also not occur everywhere in the world; there are places among the collectionof crawling, free-floating,sessile, where the entire unbroken sequence of Precam- and swimming animals (fig. 5). These animals, it is brian/Cambrian rock surfaces. Unfortunately for thought, were preserved as molds or casts in sand- western geologists, most of the continuous rock se- stone when they became stranded in mud flats in quences occur in remote, inaccessible places such as shallow waters, and were subsequentlyburied by shift- the Alden River formation in Siberia (fig. 4; see ing sands that washed over the flats (Glaessner 1961). Rosanov 1975.) However, there is one readily accessi- The key factorin explaining this great and beautiful ble site where the relation between Precambrianand collectionof Precambriananimals is the realizationthat Cambrianrocks can be seen in the field. This site is all the animals were soft-bodied. They lacked the hard the Ediacarahills of southwest Australia,near Sydney. calcareous skeletons of the later Cambrian animals.

0 Millions of , years ago P P

c~~~~~~~~ j 30 Periods 2 E

Uu i7n n0 u C u - I- C Eras Paleozoic Mesozoic enozoic Pre-Phanerozoic

Eras Aphebian Riphsean Vendian _ Aeons J Hadean Archaen Proterozoic Paarzi Milliotns of 400f0 3900 3000 2600 2)000 1000 580) years ago

Origin Oldest Oldest strotmatolitesand Abundant Oldest OldEst Oldest plant of Earth Earth rocks moneran microfossils stromatolites protoctist animal and fungus fossils fossils fosils

FIGURE2. A chronologyof Earthhistory showing the majortime-rock divisions. (Reprintedfrom Margulis,Early Life, 1982, with permission of Science Books International,Boston MA.)

SUDDEN EXPLOSION 77 FIGURE 3. Cambrian boundary: United States, Grand Canyon. The boundary between prePhanerozoic rocks in the Monument Creek Xi7- =area of the Grand Canyon of Arizona. The discontinuity (unconfor- ._ :; ~ ~mity) here is profound. Because no obvious signs of life are found here below the arrow, and fossils are abundant above in the Cam- brian strata, it was thought that this boundary represented some major change in the history of the Earth. (Photograph by Bradford Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021 4U ~~~~~~~~~~Washburn,Boston Museum of Science, reprinted from Margulis, Early Life, 1982, with permission of Science Books International, Boston MA.)

Since the early '60s, the Ediacaranfauna has been iden- bacteriain the process of reproducingby division. An- tified at 14 other locations worldwide, including Great cient microfossils seen in rocks dated to be about the Britain,Canada, Sweden, and the Soviet Union. Thus, same age, 3,400 million years old, have also been the idea that there were no animals before the Cam- reported from the Warrawoona rock formation at brian has now been entirely dispelled. During the late North Pole, Western Australia (one of the warmest Precambrian,a period of time which is better called places on Earth). the prePhanerozoic (see fig. 2), there were perfectly Another amazing and diverse assemblage of well-developed metazoanforms belonging to recogniz- microfossils has been found in the 2 billion-year-old able phyla. But, since they bore no hard parts, relative Gunflint Iron formation of Northern Minnesota and to theirCambrian successors, they were preservedonly Southern Ontario (fig. 6.) Still another remarkably very poorly. well-preserved collection of fossils comes from Cen- tralAustralia, near Alice Springs. This fossil find, from And Before the Ediacaran Fauna? the BitterSprings formation,is about 900 million years Did other forms of life precede the Ediacaranfauna, old. These and many other findings confirm that life or did all of evolution begin with these soft-bodied, was already well established at least 3.4 billion years late prePhanerozoic metazoans? ago, a mere billion years after the formation of the Amazingly enough, there has been a revolution in Earth itself as a solid planet replete with its satellite, our thinking about early life in the last 30 years. The the moon, in orbit around the sun. firstfossil evidence for life extends backat least 2 billion What sorts of environments existed on the Earthin years before the Ediacarananimals. such ancient times? Most geologists agree that from The oldest reported fossils have been identified in the beginning of the ArcheanAeon, 3,900 millionyears fine, dark, quartzrocks called flints or cherts. Spherical ago, there was very little oxygen in the atmosphere of bodies that can be seen with the light microscopehave the Earth. Ultraviolet light irradiated the surface been identified as microfossils of bacteria. Some, for waters. Bacterialived in shallow seas where the light example those taken from the Swaziland rock forma- penetrated sufficiently to insure that producers could tion in the BarbertonMountainland of South Africa make a living by photosynthesis. On shallow shores, near the tiny village of Fig Tree, even seem to be communities of bacteria, often dominated by

78 THE AMERICAN BIOLOGY TEACHER, VOLUME 45, NO. 2, FEBRUARY 1983 FIGURE4. Cambrianboundary: USSR, Alden River. The lower t boundaryof the Cambrianrocks on the Alden Riverin Siberia.The arrowpoints to the lowermost layer that contains fossils of skeleta- lized animals. The layersabove the one numbered"9" containfossils it of more than 60 species of animals. The lower layers, which, like the upper ones, are composed primarilyof the mineral dolomite, lack animal remains but contain stromatolitesand traces of soft- bodied Edicaranfauna. The absence of any discontinuitybetween these layers supports the concept that the Cambrianboundary . ; Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021 representsa change in the preservabilityof fossils, an evolutionary ir toA sequence, rather than a geological, atmospheric, extraterrestrial, or other external event. (Courtesy of Max and FrancoiseDebrenne, Li Mus&ede HistoireNaturelle, Paris. Reproduced from Margulis, Early i L . Life, 1982, with permissionof Science Books International,Boston MA.)

z & h r +ti tp bt .s t r r iJ, j #AV7 A __ w * * s ~~4ISAl, ; Rv <

cyanobacteria(organisms that used to be called blue- microbes, amoeboflagellates, dinoflagellates, green green algae) formed layered structurescalled mats. In algae, and probably many others appeared. In these these microbialmats the ensheathed, sticky, filamen- organisms mitosis evolved as a new mechanism of cell tous and coccoid bacteriatrapped and bound particles division. This process and the meiotic sexualityrelated of sediment to their surfaces. Layerupon layer of these to it was a precursor to the many multicellular alternatingorganic-rich and sediment-richstrata built microorganismsof which the majorityare animals and up, sometimes hardening into rock to form limestones plants. Such multicellular protists, or protoctists as or chert structurescalled "stromatolites" (fig. 7.) The they are now called, include water molds, slime molds, Great Slave Lake stromatolitesof the Northwest Ter- slime nets, various colonial algae, and other nucleated ritories, Canada are a good example of these fossil aquatic, sexual beings that are neither animals nor structures (fig. 8.) Modem live mats that form plants (Margulis1981). Since most protoctistsare soft- stromatolitescontinue to exist in the hypersalinebasins bodied, they left no clear fossil record-yet enough of Hamilin Pool at Shark Bay, Western Australia (fig. enigmatic fossil structures have been found for us to 9.) It is remarkablethat one still finds filamentous and feel that well before the Cambrian, invertebrates, coccoid bacteria trapping sediments much as their unicellular microbes, and their multicellulardescen- ancestors did over 2 billion years ago. dants did flourish.

Protoctists About a billion years ago new kinds of communities Skeletalization of bacteria emerged. Some were close alliances of Before the Cambrian, microbes and animals had bacteriato form symbioses of various sorts. By a com- flourished for years. Why then, did skeletalization plicatedseries of events involving microbesof different abruptlyappear with the Cambrianinvertebrates? Was species living together, the nucleated, or eukaryotic, this skeletalizationcorrelated with drastic early Cam- cells with their specialized organelles for respiration brian environmental changes as has been proposed? (mitochondria)and photosynthesis (plastids)evolved. Skeletalization is in part a consequence of the During the late prePhanerozoicphase new groups of requirementin an animal body for the external extru-

SUDDEN EXPLOSION 79 r~~~~7 A

7. FIGURE5. The Ediacaranfauna. A scene ia from the end of the ProterozoicAeon: an Ediacaran sea bottom with soft-bodied animalsreconstructed from impressions they a ~~~leftin sandstone and mud some 700 million IL ~~~~yearsago. Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021

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FIGURE 6. PrePhanerozoic microfossils. Thin sections of chertrocks viewed with the light microscopefrom the 2,000 million-year- old GunflintIron Formation of western On- 46 tario.(A). A micrographmagnified 300 times 41 _ ^ _ ^ =[. 4 "showing the diversityand abundanceof the Gunflintmicrobiota. (B). Gunflintiagrandis Barghoorn, a filamentous microorganism Ii ^ Wveryabundant in certain Gunflint facies (magnified 750 times). (C). Leptoteichus _ { ^ .. t. _ golubicii Barghoorn, a newly identified ...... spherical microorganism abundant in the Gunflint chert.

a~~~~~~~~~~ ~~~~~~~~...... ;...tZ

0. TH A B ,, U sion of soluble calcium ions. Indeed, regulation of left evidence of its activities for 3 billion years before calciumis crucialto the function of all eukaryoticcells. the Phanerozoic Aeon (and its first period, the Cam- Whereas the sea has high concentrations of calcium brian)ever began. However, the preservationof com- (0.1 mM,) inside the eukaryoticcell the concentration plete animal skeletons dramaticallyincreased at the must be less than 0.001 mM. Calcium is intrinsic to base of the Cambrian.Examination of the missing se- many functions, specificallyrequired for amoeboid cell quence between Precambrian/Cambrianstrata, studies movement, cell secretion,and adhesion, and especially of the late PrecambrianEdiacaran fauna, and evidence for muscle contraction. Many of the members of the pointing to the fact that early skeletalization actually Ediacaran faunal assemblage were free-swimming; originated with this fossil assemblage-all dispel the thus they must have possessed relatively complex muscle systems. Since intracellularcalcium-regulating mechanisms must have preceded skeletalization, the potential for forming skeletons must have existed by Ediacarantimes. Was calcium skeletalization present before the early Cambrianfauna-i.e., in the Ediacaran fauna? Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021 The mineralized skeletons of Cambriananimals are found in strata with unequivocal evidence of preda- I!_~~~~~~~ tion. This does not seem to be a mere coincidence. In the course of evolution, prey developed more highly efficient motor and muscle systems to escape more ef- fective predators. Since muscle contractionresponds A directlyto calciumrelease, the co-evolutionof prey and predatoris thought to have led to greaterphysiological control over intracellularcalcium release. In muscle tissue, one can see electron microscopicalevidence for the differentiation of calcium storage sites. Certain animals extruding excess intracellular calcium developed calcium excretion mechanisms on newly developed cuticles and other surface tissues...... ~~~~~~~~..3 ...... ; These differentiated in response to the immediate needs of the fine-tuning of intracellularcalcium con- centrations. Hence early skeletons most likely ap- peared with the Ediacaranfauna, and were not uni- que to the Cambrianinvertebrates. Why then do we not see at first glance evidence of calcified hard parts in the Ediacaran fossils? Early skeletons were probably poorly consolidated and on- ly locally mineralized. After death, the intervening organic material that held together early skeletons would degrade, leaving behind only rather scattered calcified constituents for preser- '1_N )! . remains of the hard, ly340mio 1 ear -1-old R igtlaintducsoiaesdmns1 1 S= vation (Lowenstam and Margulis 1980). Recognition of such discontinuous,bio-inorganic deposits as former frmamcoilmt at LauaFgeoa_aaCl_rnadlNre n skeletal material would be difficult, but not impossi- Mexco Comnte fbcei, ohpooytei ble to accomplish. Indeed, Martin Glaessner has heeorpi,fomtefb. o h aiae sdmn ()h. reportedbody depressions on certainEdiacaran fossils saesmle,si (A., bu.a.hgermanfiato. Scl1hw to be remnants of organic hard parts reinforced by milmee itras carbonate. B FIGURE7. Modem microbialmats comparedwith ancientlaminated Summary chertinterpreted to be fossil microbialmats. (A). Left:Archean band- ed chert from the Swaziland System of South Africa,approximate- The traditional "problem" of explaining the "sud- den" appearance of Cambrian skeletalized fossil in- vertebrates, supposedly lacking Precambrianprecur- sors, is no longer a paradox. Life, as microbial life, originated in the early Archean Aeon or before, and

SUDDEN EXPLOSION 81 '@: Downloaded from http://online.ucpress.edu/abt/article-pdf/45/2/76/40171/4447635.pdf by guest on 29 September 2021 l ~ ~~ ~ ~ ~ - -

FIGURE 8. Ancient stromatolites. Proterozoic carbonate FIGURE9. Recent stromatolites. Carbonatestromatolites forming stromatolites, remains of bacterialcommunities, from The Great today in a warm hypersaline evaporate basin in tropical western Slave Lake, Northwest Territory,Canada. The hammer is about a Australia,Hamelin Pool, SharkBay. (Photographby Paul Hoffman, foot long. (Photograph by Paul Hoffman, Geological Survey of GeologicalSurvey of Canada.Reproduced by permissionfrom W.H. Canada. Reproduced by permission from W.H. Freeman Co., in FreemanCo., in Margulis, 1982, Symbiosis in Cell Evolution, San Margulis, 1982, Symbiosis in Cell Evolution, San Francisco.) Francisco.)

idea that the skeletalizedCambrian invertebrates were Acknowledgment-We acknowledge the support of without Precambrian metazoan antecedents. Early NASA, NGR, 004-025 and the Boston University Graduate stages of skeletalization preserved only poorly in the School in support of this work and the aid of Isobel Taylor in preparation of the manuscript. fossil record, so it is difficult to identify exactly when calcium biomineralization of animals began; but it References originated with the Ediacarananimals during the late GLAESSNER,M.F. 1961.Pre-Cambrian animals. In Laporte, ProterozoicAeon. As more and more evidence begins L.F. (ed.) Evolution and the fossil record. San Francisco: to accumulate, it becomes clear that the Cambrianin- W.H. Freeman and Company. vertebrate "explosion" is simply a result of organic LOWENSTAM,H.A., and MARGULIS, L. 1980. Evolu- evolution, leading to remarkably preservable tionary prerequisites for early Phanerozoic calcereous calcareous skeletons. Indeed, the Cambrian "explo- skeletons. Biosystems 12:27-41. MARGULIS,L. 1981. How many kingdoms?:Current views sion" bang is more of a whimper, representing only of biological classification. American Biology Teacher a matter-of-factchapter in the overall evolutionary 43:482-489. history of life. ROZANOV,A.Y. 1975. The problem of the lower boundary of the Cambrian. In Cowie, J.W., and Glaessner, M.F. (eds.) The Precambrian-Cambrianboundary: A sym- posium. Earth Science Reviews 11:209-251.

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82 THE AMERICANBIOLOGY TEACHER, VOLUME 45, NO. 2, FEBRUARY1983