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Proc Natl Acad Sci U S A. Jun 20, 2000; 97(13): 6947–6953.
PMCID: PMC34368
Colloquium Paper

Solution to Darwin's dilemma: Discovery of the missing Precambrian record of life

Abstract

In 1859, in On the Origin of Species, Darwin broached what he regarded to be the most vexing problem facing his theory of evolution—the lack of a rich fossil record predating the rise of shelly invertebrates that marks the beginning of the Cambrian Period of geologic time (≈550 million years ago), an “inexplicable” absence that could be “truly urged as a valid argument” against his all embracing synthesis. For more than 100 years, the “missing Precambrian history of life” stood out as one of the greatest unsolved mysteries in natural science. But in recent decades, understanding of life's history has changed markedly as the documented fossil record has been extended seven-fold to some 3,500 million years ago, an age more than three-quarters that of the planet itself. This long-sought solution to Darwin's dilemma was set in motion by a small vanguard of workers who blazed the trail in the 1950s and 1960s, just as their course was charted by a few pioneering pathfinders of the previous century, a history of bold pronouncements, dashed dreams, search, and final discovery.

In 1950, when Ledyard Stebbins' Variation and Evolution in Plants (1) first appeared, the known history of life—the familiar progression from spore-producing to seed-producing to flowering plants, from marine invertebrates to fish, amphibians, then reptiles, birds, and mammals—extended only to the beginning of the Cambrian Period of the Phanerozoic Eon, roughly 550 million years ago. Now, after a half-century of discoveries, life's history looks strikingly different—an immense early fossil record, unknown and assumed unknowable, has been uncovered to reveal an evolutionary progression dominated by microbes that stretches seven times farther into the geologic past than previously was known. This essay is an abbreviated history of how and by whom the known antiquity of life has been steadily extended, and of lessons learned in this still ongoing hunt for life's beginnings.

Pioneering Pathfinders

Darwin's Dilemma.

Like so many aspects of natural science, the beginnings of the search for life's earliest history date from the mid-1800s and the writings of Charles Darwin (1809–1882), who in On the Origin of Species first focused attention on the missing Precambrian fossil record and the problem it posed to his theory of evolution: “There is another … difficulty, which is much more serious. I allude to the manner in which species belonging to several of the main divisions of the animal kingdom suddenly appear in the lowest known [Cambrian-age] fossiliferous rocks … If the theory be true, it is indisputable that before the lowest Cambrian stratum was deposited, long periods elapsed … and that during these vast periods, the world swarmed with living creatures … [But] to the question why we do not find rich fossiliferous deposits belonging to these assumed earliest periods before the Cambrian system, I can give no satisfactory answer. The case at present must remain inexplicable; and may be truly urged as a valid argument against the views here entertained” (ref. 2, Chapter X).

Darwin's dilemma begged for solution. And although this problem was to remain unsolved—the case “inexplicable”—for more than 100 years, the intervening century was not without bold pronouncements, dashed dreams, and more than little acid acrimony.

J. W. Dawson and the “Dawn Animal of Canada.”

Among the first to take up the challenge of Darwin's theory and its most vexing problem, the missing early fossil record, was John William Dawson (1820–1899), Principal of McGill University and a giant in the history of North American geology. Schooled chiefly in Edinburgh, Scotland, the son of strict Scottish Presbyterians, Dawson was a staunch Calvinist and devout antievolutionist (3).

In 1858, a year before publication of Darwin's opus, specimens of distinctively green- and white-layered limestone collected along the Ottawa River to the west of Montreal were brought to the attention of William E. Logan, Director of the Geological Survey of Canada. Because the samples were known to be ancient (from “Laurentian” strata, now dated at about 1,100 million years) and exhibited layering that Logan supposed too regular to be purely inorganic (Fig. (Fig.1),1), he displayed them as possible “pre-Cambrian fossils” at various scientific conferences, where they elicited spirited discussion but gained little acceptance as remnants of early life.

Figure 1
Eozoon canadense, the “dawn animal of Canada,” as illustrated in Dawson's The Dawn of Life (4) (A) and shown by the holotype specimen archived in the U.S. National Museum of Natural History, Washington, DC (B). (Bars = 1 cm.)

In 1864, however, Logan brought specimens to Dawson who not only confirmed their biologic origin but identified them as fossilized shells of giant foraminiferans, huge oversized versions of tiny calcareous protozoal tests. So convinced was Dawson of their biologic origin that a year later, in 1865, he formally named the putative fossils Eozoon canadense, the “dawn animal of Canada.” Dawson's interpretation was questioned almost immediately (5), the opening shot of a fractious debate that raged on until 1894 when specimens of Eozoon were found near Mt. Vesuvius and shown to be geologically young ejected blocks of limestone, their “fossil-like” appearance the result of inorganic alteration and veining by the green metamorphic mineral serpentine (6).

Yet despite the overwhelming evidence, Dawson continued to press his case for the rest of his life, spurred by his deeply held belief that discovery of his “dawn animal” had exposed the greatest missing link in the entire fossil record, a gap so enormous that it served to unmask the myth of evolution's claimed continuity and left Biblical creation as the only answer: “There is no link whatever in geological fact to connect Eozoon with the Mollusks, Radiates, or Crustaceans of the succeeding [rock record] … these stand before us as distinct creations. [A] gap … yawns in our imperfect geological record. Of actual facts [with which to fill this gap], therefore, we have none; and those evolutionists who have regarded the dawn-animal as an evidence in their favour, have been obliged to have recourse to supposition and assumption” (ref. 4, p. 227). (In part, Dawson was right. In the fourth and all later editions of The Origin, Darwin cited the great age and primitive protozoal relations of Eozoon as consistent with his theory of evolution, just the sort of “supposition and assumption” that Dawson found so distressing.)

C. D. Walcott: Founder of Precambrian Paleobiology.

Fortunately, Dawson's debacle would ultimately prove to be little more than a distracting detour on the path to progress, a redirection spurred initially by the prescient contributions of the American paleontologist Charles Doolittle Walcott (1850–1927).

Like Dawson before him, Walcott was enormously energetic and highly influential (7, 8). He spent most of his adult life in Washington, DC, where he served as the CEO of powerful scientific organizations—first, as Director of the U.S. Geological Survey (1894–1907), then Secretary of the Smithsonian Institution (1907–1927) and President of the National Academy of Sciences (1917–1923). Surprisingly, however, Walcott had little formal education. As a youth in northern New York State he received but 10 years of schooling, first in public schools and, later, at Utica Academy (from which he did not graduate). He never attended college and had no formally earned advanced degrees (a deficiency more than made up for in later life when he was awarded honorary doctorates by a dozen academic institutions).

In 1878, as a 28-year-old apprentice to James Hall, Chief Geologist of the state of New York and acknowledged dean of American paleontology, Walcott was first introduced to stromatolites—wavy layered mound-shaped rock masses laid down by ancient communities of mat-building microbes—Cambrian-age structures near the town of Saratoga in eastern New York State. Named Cryptozoon (meaning “hidden life”), these cabbagelike structures (Fig. (Fig.2)2) would in later years form the basis of Walcott's side of a nasty argument known as the “Cryptozoon controversy.“

Figure 2
Cryptozoon reefs near Saratoga, NY. (Photo by E. S. Barghoorn, November, 1964.)

A year later, in July, 1879, Walcott was appointed to the newly formed U.S. Geological Survey. Over the next several field seasons, he and his comrades charted the geology of sizable segments of Arizona, Utah, and Nevada, including unexplored parts of the Grand Canyon, where in 1883 he first reported discovery of Precambrian specimens of Cryptozoon (9). Other finds soon followed, with the most startling in 1899—small, millimeter-sized black coaly discs that Walcott named Chuaria and interpreted to be “the remains of … compressed conical shell[s],” possibly of primitive brachiopods (10). Although Chuaria is now known to be a large single-celled alga, rather than a shelly invertebrate, Walcott's specimens were indeed authentic fossils, the first true cellularly preserved Precambrian organisms ever recorded.

After the turn of the century, Walcott moved his field work northward along the spine of the Rocky Mountains, focusing first in the Lewis Range of northwestern Montana, from which he reported diverse stromatolitelike structures (11) and, later, chains of minute cell-like bodies he identified as fossil bacteria (12). His studies in the Canadian Rockies, from 1907 to 1925, were even more rewarding, resulting in discovery of an amazingly well preserved assemblage of Cambrian algae and marine invertebrates—the famous Burgess Shale Fauna that to this day remains among the finest and most complete samples of Cambrian life known to science (13, 14).

Walcott's contributions are legendary—he was the first discoverer in Precambrian rocks of Cryptozoon stromatolites, of cellularly preserved algal plankton (Chuaria), and of possible fossil bacteria, all capped by his pioneering investigations of the benchmark Burgess Shale fossils. The acknowledged founder of Precambrian paleobiology (15), Walcott was first to show, nearly a century ago and contrary to accepted wisdom, that a substantial fossil record of Precambrian life actually exists.

A. C. Seward and the Cryptozoon Controversy.

The rising tide in the development of the field brought on by Walcott's discoveries was not yet ready to give way to a flood. Precambrian fossils continued to be regarded as suspect, a view no doubt bolstered by Dawson's Eozoon debacle but justified almost as easily by the scrappy nature of the available evidence. Foremost among the critics was Albert Charles Seward (1863–1941), Professor of Botany at the University of Cambridge and the most widely known and influential paleobotanist of his generation. Because practically all claimed Precambrian fossils fell within the purview of paleobotany—whether supposed to be algal, like Cryptozoon stromatolites, or even bacterial—Seward's opinion had special impact.

In 1931, in Plant Life Through the Ages, the paleobotanical text used worldwide, Seward assessed the “algal” (that is, cyanobacterial) origin of Cryptozoon as follows: “The general belief among American geologists and several European authors in the organic origin of Cryptozoon is … not justified by the facts. [Cyanobacteria] or similar primitive algae may have flourished in Pre-Cambrian seas and inland lakes; but to regard these hypothetical plants as the creators of reefs of Cryptozoon and allied structures is to make a demand upon imagination inconsistent with Wordsworth's definition of that quality as ‘reason in its most exalted mood”’ (ref. 16, pp. 86–87).

Seward was even more categorical in his rejection of Walcott's report of fossil bacteria: “It is claimed that sections of a Pre-Cambrian limestone from Montana show minute bodies similar in form and size to cells and cell-chains of existing [bacteria]  . These and similar contributions … are by no means convincing  . We can hardly expect to find in Pre-Cambrian rocks any actual proof of the existence of bacteria  ” (ref. 16, p. 92).

Seward's 1931 assessment of the science was mostly on the mark. Mistakes had been made. Mineralic, purely inorganic objects had been misinterpreted as fossil. Better and more evidence, carefully gathered and dispassionately considered, was much needed. But his dismissive rejection of Cryptozoon and his bold assertion that “we can hardly expect to find in Pre-Cambrian rocks any actual proof of the existence of bacteria” turned out to be misguided. Yet his influence was pervasive. It took another 30 years and a bit of serendipity to put the field back on track.

Emergence of a New Field of Science

In the mid-1960s—a full century after Darwin broached the problem of the missing early fossil record—the hunt for early life began to stir, and in the following two decades the flood-gates would finally swing wide open. But this surge, too, had harbingers, now dating from the 1950s.

A Benchmark Discovery by an Unsung Hero.

The worker who above all others set the course for modern studies of ancient life was Stanley A. Tyler (1906–1963) of the University of Wisconsin, the geologist who in 1953 discovered the now famous mid-Precambrian (2,100-million-year-old) microbial assemblage petrified in carbonaceous cherts of the Gunflint Formation of Ontario, Canada. A year later, together with Harvard paleobotanist Elso S. Barghoorn (1915–1984), Tyler published a short note announcing the discovery (17), a rather sketchy report that on the basis of study of petrographic thin sections documents that the fossils are indigenousness to the deposit but fails to note either the exact provenance of the find or that the fossils are present within, and were actually the microbial builders of, large Cryptozoon-like stromatolites (an association that, once recognized, would prove key to the development of the field). Substantive, full-fledged reports would come later—although not until after Tyler's untimely death, an event that cheated him from receiving the great credit he deserved—but this initial short article on “the oldest structurally preserved organisms that clearly exhibit cellular differentiation and original carbon complexes which have yet been discovered in pre-Cambrian sediments” (17) was a benchmark, a monumental “first.”

Contributions of Soviet Science.

At about the same time, in the mid-1950s, a series of articles by Boris Vasil'evich Timofeev (1916–1982) and his colleagues at the Institute of Precambrian Geochronology in Leningrad (St. Petersburg) reported discovery of microscopic fossil spores in Precambrian siltstones of the Soviet Union. In thin sections, like those studied by Tyler and Barghoorn, fossils are detected within the rock, entombed in the mineral matrix, so the possibility of laboratory contamination can be ruled out. But preparation of thin sections requires special equipment, and their microscopic study is tedious and time-consuming. A faster technique, pioneered for Precambrian studies in Timofeev's lab, is to dissolve a rock in mineral acid and concentrate the organic-walled microfossils in the resulting sludgelike residue. This maceration technique, however, is notoriously subject to error-causing contamination—and because during these years there was as yet no established early fossil record with which to compare new finds, mistakes were easy to make. Although Timofeev's laboratory was not immune, much of his work has since proved sound (18), and the technique he pioneered to ferret-out microfossils in Precambrian shaley rocks is now in use worldwide.

Famous Figures Enter the Field.

Early in the 1960s, the fledgling field was joined by two geologic heavyweights, an American, Preston Cloud (1912–1991), and an Australian, Martin Glaessner (1906–1989), both attracted by questions posed by the abrupt appearance and explosive evolution of shelly invertebrate animals that marks the start of the Phanerozoic Eon.

A feisty leader in the development of Precambrian paleobiology, Cloud was full of energy, ideas, opinions, and good hard work. His Precambrian interests were first evident in the late-1940s, when he argued in print that although the known Early Cambrian fossil record is woefully incomplete it is the court of last resort and, ultimately, the only court that matters (19). By the 1960s, he had become active in the field, authoring a paper that to many certified the authenticity of the Tyler-Barghoorn Gunflint microfossils (20) and, later, a series of reports adding new knowledge of the early microbial fossil record (2123). But above all, he was a gifted synthesist, showing his mettle in a masterful article of 1972 that set the stage for modern understanding of the interrelated atmospheric-geologic-biologic history of the Precambrian planet (24).

In the early 1960s, a second prime player entered this now fast-unfolding field, Martin Glaessner (1906–1989), of the University of Adelaide in South Australia. A scholarly, courtly, old-school professor, Glaessner was the first to make major inroads toward understanding the (very latest) Precambrian record of multicelled animal life (25, 26).

In 1947, three years before Glaessner joined the faculty at Adelaide, Reginald C. Sprigg announced his discovery of fossils of primitive soft-bodied animals, chiefly imprints of saucer-sized jellyfish, at Ediacara, South Australia (27). Although Sprigg thought the fossil-bearing beds were Cambrian in age, Glaessner showed them to be Precambrian (albeit marginally so), making the Ediacaran fossils the oldest animals known. Together with his colleague, Mary Wade, Glaessner spent much of the rest of his life working on this benchmark fauna (see, e.g., refs. 28 and 29), bringing it to international attention in the early 1960s (30) and, later, in a splendid monograph (31).

With Glaessner in the fold, the stage was set. Like a small jazz band—Tyler and Barghoorn trumpeting microfossils in cherts, Timofeev beating on fossils in siltstones, Cloud strumming the early environment, Glaessner the earliest animals—great music was about to be played. At long last, the curtain was to rise on the missing record of Precambrian life.

Breakthrough to the Present.

My own involvement dates from 1960, when as a sophomore in college I became enamored with the problem of the missing Precambrian fossil record, an interest that was to become firmly rooted during the following few years, when I was the first of Barghoorn's graduate students to focus on early life. I have recently recounted in some detail my recollections of those heady days (32) and need not reiterate the story here. Suffice it to note that virtually nothing had been published on the now-famous Gunflint fossils (Fig. (Fig.3)3) in the nearly 10 years that had passed between the Tyler-Barghoorn 1954 announcement of the find and my entry into graduate school in June, 1963. Then, quite unexpectedly, in October of that year, Stanley Tyler passed away at the age of 57, never to see the ripened fruits of his long-term labor reach the published page. Within a year thereafter, a series of events that would shape the field began to unfold, set off first by a squabble between Barghoorn and Cloud as to who would scoop whom in a battle for credit over the Gunflint fossils (32). By late 1964 this spat had been settled, with Cloud electing to hold off publication of his paper “illustrating some conspicuous Gunflint nannofossils and discussing their implications until Barghoorn could complete his part of a descriptive paper with the by-then deceased Tyler” (ref. 33, p. 23). The two articles appeared in Science in 1965, first Barghoorn and Tyler's “Microorganisms from the Gunflint chert” (34), followed a few weeks later by Cloud's contribution, “Significance of the Gunflint (Precambrian) microflora” (20). Landmark papers they were!

Figure 3
Microfossils of the Paleoproterozoic (≈2,100-million-year-old) Gunflint chert of southern Canada. (A and B) Eosphaera, in B shown in two views of the same specimen. (C and D) Eoastrion. (EG) Huroniospora. (HK) Gunflintia ...

Unlike the 1954 Tyler-Barghoorn announcement of discovery of the Gunflint fossils, which had gone largely unnoticed, the Barghoorn-Tyler 1965 article—backed by Cloud's affirmation of its significance—generated enormous interest. Yet it soon became apparent that acceptance of ancient life would come only grudgingly. The well had been poisoned by Dawson's debacle, the Cryptozoon controversy, Seward's criticism—object lessons that had been handed down from professor to student, generation to generation, to become part of accepted academic lore. Moreover, it was all too obvious that the Gunflint organisms stood alone. Marooned in the remote Precambrian, they were isolated by nearly a billion and half years from all other fossils known to science, a gap in the known fossil record nearly three times longer than the entire previously documented history of life. Skepticism abounded. Conventional wisdom was not to be easily dissuaded. The question was asked repeatedly: “Couldn't this whole business be some sort of fluke, some hugely embarrassing awful mistake?”

As luck would have it, the doubts soon could be laid to rest. During field work the previous year (and stemming from a chance conversation with a local oil company geologist by the name of Helmut Wopfner), Barghoorn had collected a few hand-sized specimens of Precambrian stromatolitic black chert in the vicinity of Alice Springs, deep in the Australian outback. Once the Gunflint paper had been completed, I was assigned to work on the samples, which quite fortunately contained a remarkable cache of new microscopic fossils, most nearly indistinguishable from extant cyanobacteria and almost all decidedly better preserved than the Gunflint microbes (Fig. (Fig.4).4). Although the age of the deposit (the Bitter Springs Formation) was known only approximately, it seemed likely to be about 1,000 million years, roughly half as old as the Gunflint chert.

Figure 4
Filamentous microfossils of the Neoproterozoic (≈850-million-year-old) Bitter Springs chert of central Australia. Because the petrified microbes are three-dimensional and sinuous, composite photos have been used to show the specimens A ...

Barghoorn and I soon sent a short report to Science (35), publication of which—viewed in light of the earlier articles on the Gunflint organisms—not only served to dispell lingering doubts about whether Precambrian fossils might be some sort of fluke, but seemed to show that the early fossil record was surprisingly richer and easier to unearth than anyone had dared imagine. Indeed, it now appears that the only truly odd thing about the Gunflint and Bitter Springs fossils is that similar finds had not been made even earlier. Walcott had started the train down the right track only for it to be derailed by the conventional wisdom that the early history of life was unknown and evidently unknowable, a view founded on the assumption that the tried and true techniques of the Phanerozoic hunt for large fossils would prove equally rewarding in the Precambrian. Plainly put, this was wrong.

Lessons from the Hunt

The Gunflint and Bitter Springs articles of 1965 charted a new course, showing for the first time that a search strategy centered on the peculiarities of the Precambrian fossil record would pay off. The four keys of the strategy, as valid today as they were three decades ago, are to search for (i) microscopic fossils in (ii) black cherts that are (iii) fine-grained and (iv) associated with Cryptozoon-like structures. Each part plays a role.

(i) Megascopic eukaryotes, the large organisms of the Phanerozoic, are now known not to have appeared until shortly before the beginning of the Cambrian—except in immediately sub-Cambrian strata, the hunt for large body fossils in Precambrian rocks was doomed from the outset.

(ii) The blackness of a chert commonly gives a good indication of its organic carbon content—like fossil-bearing coal deposits, cherts rich in petrified organic-walled microfossils are usually a deep jet black color.

(iii) The fineness of the quartz grains making up a chert provides another hint of its fossil-bearing potential—cherts subjected to the heat and pressure of geologic metamorphism are often composed of recrystallized large grains that give them a sugary appearance whereas cherts that have escaped fossil-destroying processes are made up of cryptocrystalline quartz and have a waxy glasslike luster.

(iv) Cryptozoon-like structures (stromatolites) are now known to have been produced by flourishing microbial communities, layer upon layer of microscopic organisms that make up localized biocoenoses. Stromatolites permineralized by fine-grained chert early during diagenesis represent promising hunting grounds for the fossilized remnants of the microorganisms that built them.

Measured by virtually any criterion one might propose (Fig. (Fig.5),5), studies of Precambrian life have burst forth since the mid-1960s to culminate in recent years in discovery of the oldest fossils known, petrified cellular microbes nearly 3,500 million years old, more than three-quarters the age of the Earth (36). Precambrian paleobiology is thriving—the vast majority of all scientists who have ever investigated the early fossil record are alive and working today; new discoveries are being made at an ever quickening clip—progress set in motion by the few bold scientists who blazed this trail in the 1950s and 1960s, just as their course was charted by the Dawsons, Walcotts, and Sewards, the pioneering pathfinders of the field. And the collective legacy of all who have played a role dates to Darwin and the dilemma of the missing Precambrian fossil record he first posed. After more than a century of trial and error, of search and final discovery, those of us who wonder about life's early history can be thankful that what was once “inexplicable” to Darwin is no longer so to us.

Figure 5
Birth and growth of Precambrian paleobiology.

Footnotes

This paper was presented at the National Academy of Sciences colloquium “Variation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins,” held January 27–29, 2000, at the Arnold and Mabel Beckman Center in Irvine, CA.

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