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From cells to cities

The evolution of composite individuality - early life leaves its record in the rocks

By Lynn Margulis, Dorion Sagan and Jessica H. Whiteside

Lynn Margulis
Lynn Margulis
Charles Darwin's theory of evolution by natural selection marked a profound change not only in science, but in human thought. Since the Origin it has become obvious that all life is connected by descent to common ancestors and, all life, through energy, is bound to the universe as a whole. These scientific revelations depend on details: barnacle sex, vegetable mold, South America megafossils, steam engines, etc. Yet understanding ofe volution and energy flow in nature, unlike most arcane scientific discoveries, emerged from connected integration rather than divisive specialization.

The Darwinian enjoyed two precedent revolutions: Copernicus' heliocentrism and vitalism's demise. Life, no longer a special substance, is composed of familiar matter of the inorganic world. Animating and body-building energy no longer can be relegated to mysterious spirits: the energy of life comes either from sunlight or chemical oxidation.

We roughly identify four major evolutionary transitions. First, the origin of life (i.e., as bacteria) from carbon compounds. Second, the origin of nucleated cells from bacteria. This transition, enabled by symbiosis, produced protoctists. The third was the evolution ofcells into multicellular bodies. Nucleated cells diverged into three very successful lineages the animals, the plants, and the fungi. The fourth, most recent major evolutionary transition is that from animal populations to superorganisms. Evolution of social superorganisms occurred primarily in insects among the immense colonies of ants, the mound-building termites, and hive-making bees. But the transition from society to superorganism also has a tendency to occur in closely knit collections of mammals. In populations of naked mole rats of Africa, Spalax, not all of the members reproduce. These subterranean mammals are stratified into societies with workers and a huge "queen" who lies on her back producing ugly pink hairless babies most of her life. Human beings, too, with our cities and our now-global populations, seem to be heading toward social stratification in which most members of an interconnected population no longer reproduce.

Fig. 1. Protoctists, a huge group that includes some 250,000 extant species such as the amoebae, phytoplankton, ciliates, water molds, the brown seaweeds and many less familiar organisms are all composed of cells with nuclei. Protoctists, such as Snyderella tabogae here, arose from symbioses among bacteria. Click here for a larger image (Drawing: Christie Lyons).
Our new work shows that symbiosis, the living together of different types of organisms, generates dramatic evolutionary novelty, including new species. Indebted to much international scientific and scholarly labor, symbiogenesis as a source of evolutionary novelty is subsumed by Darwin's revolution. This symbiogenetic view recognizes a crucial fact: the importance of microbes in the evolutionary process. Bacteria, smaller protoctists and other subvisible life forms, exquisitely sensitive to environmental conditions, solve our and Darwin's nagging question: How does hereditary variation originate? A gnawing sense of discomfort is shared by scientists and other readers: the "accumulation of random mutations" does not suffice to explain the appearance of new organs, new tissues, new behaviors or new species either in living beings or their fossil remains.

A huge amount of would-be fine tuning was generated by Darwin's overspecialized successors, the neodarwinists who rationalized Gregor Mendel's genetics with Charles Darwin's natural selection. One inadequacy of neodarwinist explanation can be traced to our profound, nearly invisible, zoological bias: in our perusal of the panoply of life and its record in the sediments we show overwhelming concern with our own size and time scale. We regard evolution as basically a prelude to the appearance of "Man". All earlier life is "primitive" or lower, including the "rise ofbackboned animals". From a broader perspective most biological diversity is not even among animals. The fossil record amply demonstrates that eighty percent oflif e's evolution occurred prior to the origin of any animal of any kind. Indeed, any life visible to the naked eye was preceded by at least 1500 million years of microbial evolution.

Early life leaves its record in the rocks: as kerogen, as microfossils, as strange sedimentary structures made by masses of microbes including stromatolites, microbial laminates, oncolites, radiolarites and diatomaceous earth. Much arcane evidence for the strong interaction of microbes with sediment preceded any evidence for plants, animals and even fungi. Bacteria, with their astounding metabolic virtuosities, appeared very early on Earth's surface. Some bacteria, for example, produce methane from carbon dioxide and hydrogen; they die if fed sugar. Others generate energy by consuming methane. Still others make laughing gas (nitrous oxide) or hydrogen cyanide. A crucial group of bacteria for us are those that pull nitrogen, as N2, out of the air and put it into food. Some take hydrogen out of rocks and others make food by use of carbon dioxide in the air and the energy of sunlight.

Some precipitate metals like manganese, gold or iron. Because of their extraordinary diversity, their genetic systems wildly different from ours and their early appearance on the scene, evolution must be understood by extrapolation from bacteria. Bacteria are neither lower plants nor lower animals. They are not germs; they are our ultimate ancestors. The language of life is chemistry, the energy that drives life is chemical energy. The chemicals of life are organized in cells in ways that yield energy to maintain the identity of living forms all of which evolved, ultimately, from bacteria.

Our animal bias runs deep. Even accepted faulty terminology reinforces it. For example, the term "protozoan" derived from "first-animal" suggests that microbes strove to produce animals. But it is, in a sense, the opposite: animals are one of several outcomes evolved from protoctists (not "protozoans"). Protoctists, a huge group that includes some 250,000 extant species such as the amoebae, phytoplankton, ciliates, water molds, the brown seaweeds and many less familiar organisms are all composed ofcells with nuclei. Protoctists, such as Snyderella tabogae here, arose from symbioses among bacteria (Fig. 1). Three lineages had huge consequences for life on land: the swimming-feeding microbes that led to animals, the green algae that led to plants and the water molds that led to fungi.

Animal-style behavior, animal-style sex, and animal-style speciation first occurred, not in animals but in organisms like the protoctists ofthe termite's intestine. In such warm, wet, food-rich pockets without oxygen, microbes similar to our ancient cell ancestors are still protected. We know they have lived inside termites for at least 20 million years. In Mastotermes darwiniensis, an Australian termite, for example, we recognize the composite individuality of Mixotricha paradoxa (drawing and electron micrograph (Fig. 2). This protoctist is not a tiny "single-celled swiming animal" nor is it the individual organism that it seems to be. Rather, this "single cell" is composed of five distinguishable types of microbes, each with its own genome. Inside the largest microbe dwell many spherical bacteria, while attached to its outside live some 500,000 cilia-like treponemes, spirochetes, that act as oars to propel the protoctist's body through the murky gut. Then, also on the outside are about 200 larger recently described spirochetes and named after a wonderful University of Massachusetts microbiologist, Ercole Canale-Parola: Canaleparolina darwiniensis.

The German literary critic Walter Benjamin argued that it is the extreme, rather than the ordinary, which is exemplary. This is true here. M. paradoxa, despite its monstrous aspect reminiscent of the chimeras, the griffins and medusas of Greek mythology and medieval European bestiaries, turns out to be an obvious example of the tendency of all nucleated cells. The photosynthetic parts of seaweeds and plants (the plastids), and the oxygen-using parts of seaweeds, plants, fungi, and animals (the mitochondria) all originated as bacteria that were ingested but not digested by larger cells. This idea has proved to be correct. There are also tantalizing hints, not yet conclusive, that spirochetes such as those attached to M. paradoxa associated with other bacteria to form cilia very early in the origin of nucleated cells.

Here at the marvelous Hanse-Wissenschaftskolleg in Delmenhorst we continue to work on symbiogenesis in the early record of life with our colleagues: M Dolan, R Guerrero, W Krumbein and A Wier.

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Prof. Dr. Lynn Margulis
Fachgebiet: Paläontologie
Förderprogramm: Humboldt-Forschungspreis
Gastinstitution: Universität Oldenburg
Heimatuniversität: University of Massachusetts at Amherst Dept. of Geosciences Amherst/ USA

co authors Dorion Sagan, Sciencewriters, New York/N.Y./USA, and Jessica H. Whiteside, Lamont Doherty Earth Observatory, Columbia University, New York/N.Y./USA

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