B orn more than three and a half billion years ago, life remained unicellular during more than two and a half billion years, more than two-thirds of its existence on Earth. During all that time, microbes, organisms visible only with a microscope, were the only ones present on our planet. They are still abundant, occupying a wide variety of sites and revealing their presence by many effects, such as producing diverse chemical substances, causing many infectious diseases, and putrefying dead organisms (a function they share with certain molds).
Very few fossil remains landmark the history of microbes on Earth, but many other signs of their passage have been left. They remodeled their habitat, leaving many traces found in geological structures and in the atmosphere today. And they have undergone a number of changes that have become known to us through the study of the genomes of extant organisms. Three major events highlight this long history.
First, the initial lineage soon split into two major groups, known today as Archaea and Bacteria or, more commonly, as archaebacteria and eubacteria, which, together, make up what much of the world still calls “bacteria” and experts designate as “prokaryotes,” organisms that do not possess a true nucleus (karyon in Greek).
Archaebacteria, so named because they were believed, perhaps wrongly, to be the more ancient of the two groups, include, among many others, two particularly fascinating classes of extant microorganisms, the methanogens and the extremophiles.
Methanogens are present wherever oxygen is absent and hydrogen is produced. There they survive by converting carbon dioxide (CO2) and hydrogen (H2) to methane gas (CH4) and water (H2O), a reaction that supplies them with enough energy to build their substance entirely from simple mineral building blocks. The mud at the bottom of ponds is one of their favorite habitats. The methane they produce in those murky depths creates the bubbles that break the silence of swamps by their muffled plopping; it fuels the will-o’-the-wisps that flit on the surface of marshes at night. Methanogens also thrive in the digestive tract of cattle and other ruminants. Methane is a greenhouse gas, which joins with carbon dioxide in the formation of the atmospheric shield that prevents heat from escaping and thereby contributes significantly to the warming of the global climate.
Extremophiles, the other remarkable class of archaebacteria, include organisms that are, as their name indicates, adapted to extreme physical conditions: elevated temperature, up to more than 110°C (230°F), icy cold, high pressure, burning acidity, caustic alkalinity, concentrated brine, not counting the innumerable human-made pollutants. Extremophiles illustrate, more than any other living beings, the amazing ability of life to respond to environmental challenges.
Eubacteria, the second group of prokaryotes, include most of the pathogenic varieties that cause such infectious diseases as tuberculosis, diphtheria, plague, leprosy, meningitis, pneumonia, and many others. They also comprise a large number of harmless varieties found in many natural niches, including the human gut, whose main inhabitant, E. coli (short for Escherichia coli, also known as colibacillus), has been the object of much of the seminal research leading to modern molecular biology.
A second major event that took place during the “microbial era” is the appearance of molecular oxygen in the Earth’s atmosphere. Oxygen, the life-giving gas par excellence, was absent in the early atmosphere, as attested by multiple evidence in ancient rocks. LUCA and its descendants for more than one billion years were all “anaerobic,” which means that they lived without air, as many microorganisms still do today, for example, those that accomplish some of the fermentations on which we rely for the manufacturing of alcoholic beverages and cheeses. The early organisms, never having been exposed to oxygen, may even have been strict anaerobes, which are killed by this gas, as is the case for the bacillus of gangrene, which infects poorly aerated wounds and is readily killed by the simple device of incising the wounds and exposing them to air.
What introduced oxygen into the Earth’s atmosphere was life itself, through the appearance of a special kind of photosynthetic bacteria called cyanobacteria (from the Greek kyanos, blue). These organisms use sunlight energy to split water (H2O) into hydrogen (H2) and oxygen (O2). The hydrogen is used to convert CO2 into sugar, from which, in turn, all the other organic cell constituents are formed, whereas oxygen is released in gaseous form.
According to the geochemical evidence, the atmospheric oxygen level started rising about 2.4 billion years ago, up to, first, a value of 1 percent of the terrestrial atmosphere, reached some 2.2 billion years ago. It stayed at that level until a second upward move lifted it to its present value of 21 percent of the atmosphere, about 1.6 billion years later.
The appearance of oxygen had a profound influence on the anaerobic forms of life that had been exclusively present until that time. Many disappeared, victims of oxygen toxicity, like the gangrene bacillus exposed to air. This extinction is sometimes referred to as the “oxygen holocaust,” a misleading term that suggests a sudden catastrophe that took place almost overnight. In fact, the process was exceedingly slow, with the oxygen content of the atmosphere rising by much less than one-ten-thousandth of a percent per millennium. There was plenty of time for life to adapt to the changing conditions.
This adaptation probably took place first by the acquisition of enzymes capable of disabling oxygen. Such enzymes are present in all aero-tolerant organisms today. Eventually, some organisms not only protected themselves against oxygen but also acquired ways to take advantage of it. They developed chemical mechanisms whereby the energy released by the reaction of foodstuffs with oxygen could serve to support various kinds of biological work, much like fuel combustion supports motor-car engines and other heat-powered machines. The biological machineries, however, are “cold” engines; they convert oxidation energy into work without the mediation of heat. Most of life today is powered entirely (animals, fungi, many bacteria) or partly (plants and other photosynthetic organisms in the dark) by such engines, to the point that oxygen, from being a deathly menace, has become an indispensable condition of survival for much of life on Earth. The most sophisticated biological “combustion engines” are found in certain bacteria and in mitochondria, about which more soon.
The third major biological event that happened in those early days was the epoch-making birth of a new type of cells of much larger size and more complex structural and functional organization than their bacterial predecessors, conspicuously including a central nucleus containing the genome. Called “eukaryotic” (which is Greek for “having a good nucleus”), as opposed to the prokaryotic bacteria, these cells gave rise to a wide variety of unicellular organisms, known as protists, and also to all multicellular organisms, including plants, fungi, animals, and humans. So the prokaryote-eukaryote transition represents a watershed in the history of life on Earth, a key event on the way to our own appearance. Without it, our planet would still harbor only bacteria.
Eukaryotic cells are so different from prokaryotic cells that one finds it difficult to imagine how one type could ever have arisen from the other. Yet, this is undoubtedly what happened, given the many indisputable signs of kinship between the two. Although the problem is far from solved, a number of telling clues are already available. Particularly revealing is the astonishing fact, now solidly established, that two key, granule-shaped organelles (small organs) of eukaryotic cells were once free-living bacteria that, at some time in the distant past, were taken up by other cells within which they underwent a progressive process of enslavement, turning into “endosymbionts” (literally meaning “living together inside”) and, eventually, evolving into fully integrated organelles.
First to be adopted in this way were the mitochondria, which are the main sites of oxidative energy production, the central “power plants,” in the vast majority of eukaryotic cells. These organelles are derived from bacterial ancestors that must have ranked among the most efficient prokaryotic oxygen utilizers at the time they were adopted and have left similarly endowed, present-day descendants showing many signs of kinship with mitochondria.
The second eukaryotic organelles of established endosymbiont origin are the chloroplasts, which harbor the light-utilizing systems of all photosynthetic eukaryotic cells, to wit, all unicellular algae and green plants. The bacterial ancestors of these organelles have been identified as belonging to the group of cyanobacteria, encountered above as the “inventors” of oxygen-generating photosynthesis. These ancestral organisms were first adopted by cells that already possessed mitochondria, which are thus present in all photosynthetic eukaryotes (except when lost in the course of evolution).
For endosymbiosis to take place, there must first have existed cells with a size and functional properties that allowed them to harbor the bacteria that gave rise to the organelles. This question has been a fertile ground for all kinds of hypotheses, one more ingenious than the other. For my part, I stick to the simplest possibility, directly inspired by what we know and using a common cellular function, called “phagocytosis,” whereby, for example, white blood cells capture infectious bacteria that invade an organism. We need merely to suppose that a “primitive phagocyte” possessing this property already existed at the time we are talking about and that, exceptionally, the bacterial ancestors of the endosymbionts captured by this organism were not killed and destroyed, as happens in white blood cells, but survived to become the endosymbionts. Such a phenomenon would hardly be surprising, as several present-day instances of it are known. According to the hypothesis I propose, this phenomenon would have happened at least twice, first to the ancestors of mitochondria and then, again, to the cyanobacteria that evolved inside the host cell to become the chloroplasts.
According to this scenario, formation of the “primitive phagocyte” from a prokaryotic ancestor appears as a crucial step in the development of eukaryotic cells. A detailed discussion of the manner in which this key transition could have occurred would take us too far. Let me simply emphasize the important role that may have been played by the passage from extracellular to intracellular digestion. All living beings that feed on nutrients provided by other living beings must start by digesting their foodstuffs, that is, cutting the big molecules of which these are made into small molecules that can be assimilated. This is what happens in our stomach and intestines. For single cells, this function is carried out in two different ways, depending on whether they are prokaryotic (bacteria) or eukaryotic. The former universally digest their foodstuffs with the help of enzymes that they discharge into their immediate surroundings, a process that requires prokaryotes to reside within their food source, like worms inside an apple or a piece of cheese. Eukaryotic cells, on the other hand, almost all feed by phagocytosis and digest their food within small intracellular pockets called “lysosomes”; they are thereby freed from the residential constraints to which bacteria are subjected. Thus, the development of the phagocytic mode of cellular feeding probably represents one of the key events in the birth of eukaryotic cells, the source of their emancipation and their ability to adopt endosymbionts.
We lack reliable fossil traces and thus do not know for sure when eukaryotic cells first arose. But we do know they have given rise to a multitude of unicellular organisms, or protists, which have gone on evolving up to the present day and exploiting the potentialities of unicellularity to their utmost, spreading into an extraordinary variety of organisms. These include the most elaborate and remarkable unicellular forms known, which have fascinated their observers by the multiplicity of their specializations, the elaborateness of their adaptations, and the beauty of their structures.
There is a limit, however, to what can be accomplished by a single cell, obliged to carry out all the functions needed for independent life. At some stage, the advantages of a “division of labor” must have favored the emergence of organisms genetically predisposed to form multicellular associations. Many mutually advantageous associations among members of the same or of different species no doubt formed, as they do today. But true multicellular organisms were apparently late in appearing. Possibly accounting for this delay is the fact that true multicellular organisms are derived from a single egg cell, which gives rise to two or more distinct cell types by division and differentiation. Here is the key word: “differentiation.” Starting with a single genome, different cells are generated by a process dependent on certain genes being expressed and others silenced, in a manner different for each cell type. Mechanisms for turning genes on and off are already present in the simplest of prokaryotes. But it probably took special circumstances to convert such primitive mechanisms into a developmental pattern. There will be more on this subject in chapter 6.
According to presently available evidence, multicellular forms of life appeared only about one billion years ago. Plants came first, soon followed by the fungi, or molds. Animals arose much later, about six hundred million years ago—that is, at the time when the atmospheric oxygen level went through its second rise, from 1 percent to 21 percent of the atmosphere. This is probably more than a coincidence, considering the absolute dependence of animals on oxygen. The three lines evolved in parallel, following comparable courses within the constraints imposed by their respective modes of life.
One common trend was a progressive rise in complexity, a quality that, to avoid the accusation of subjectivity and personal value judgment made by some philosophers, can be defined objectively by the number of different cell types of which organisms are made. This number increased from an original two to several tens in plants and fungi, and up to some 220 in animals. This rise in cellular diversity went together with increasingly elaborate arrangements of tissues and organs. Particularly intricate body plans were achieved in the animal line, with, among others, the appearance of neurons and their association into increasingly complex polyneuronal systems, of which the human brain is the most highly developed extant form.
A second feature common to the evolution of the three lines is that they all started in water and eventually invaded land, thanks to a variety of adaptations. Plants led the way, as they had to, since only they could do without other living organisms, being capable of constructing all their substance from water, carbon dioxide, and a few minerals, using light as energy source. The other two lines, being dependent, directly or indirectly, on the plants for food, could only invade land that had already been colonized by plants. I leave out here prokaryotes that could have served to feed very primitive forms of life.
Inaugurated in water by simple seaweeds, plants started to move out of their birthplace by way of coastal varieties periodically exposed to dryness at low tide and thus likely to benefit from traits favoring survival under dry conditions. These acquired attributes included rootlets capable of drawing water and minerals from the soil and coverings that both protected the plants against desiccation and allowed them to draw carbon dioxide from the surrounding air. Thus were born primitive mosses, the first multicellular organisms to invade land.
The mosses further evolved into the first vascularized plants, fitted with roots and leaves linked by a double set of conduits. One set of conduits, leading upward, served to bring to the leaves the water and mineral nutrients taken up from the soil by the roots. In the leaves, these nutrients were then combined with atmospheric carbon dioxide into various organic compounds with the help of sunlight energy. The other set of conduits served to convey the products of these syntheses from the leaves to the roots and other nonphotosynthetic parts, to be used for metabolism and growth. This basic design has been preserved in the entire further evolution of plants, leading, largely by way of improvements in reproductive strategies (see chapter 5), first to organisms represented today by ferns, then to organisms related to conifers, and, finally, to flowering plants, which make up much of the plant world today. An important development in this history was the “invention” of lignin, the hard substance of wood to which trees owe their remarkable strength.
The plants were soon followed on land by the fungi (mushrooms and molds), which, though being both dependent on other living organisms for their food supply and unable to move and hunt for food, have acquired the means to survive by utilizing whatever organic support, whether living or dead, they can stick to, deriving nutrients from it with the help of powerful digestive enzymes that they secrete in contact with their support.
The story of animals is more complicated. Being obliged, like the fungi, to obtain their food from other living organisms, animals developed, like these organisms, around the indispensable functions of feeding and digestion, but in a different way. Their first ancestors, born in water, initially arose by exploiting the primeval phagocytic mechanism of feeding common to all protists. From first serving to support individual cells, as in sponges, this mechanism became communal in the digestive pouches of polyps and jellyfish, using enzymes secreted by the cells surrounding the pouch. Conversion of the pouch with a single opening—serving both for the entry of food and for the exit of waste—into a one-way canal, fitted with a mouth at one end and an anus at the other, completed the basic design of the animal alimentary tract, which has been maintained in all the forms that followed.
All other animal functions developed around this central alimentary core, in relation with the presence of cells that were increasingly distant from the digestive tract, while remaining dependent on it for their feeding. Thus were born circulation and, with it, respiration and excretion. Circulation served for bringing to the cells the foodstuffs and oxygen they needed and for clearing them of waste products. Respiration acted as a means, by way of gills and other organs, to capture oxygen and introduce it into the circulation for delivery to all cells. The function of excretion was to discharge, by organs such as kidneys, cellular waste carried by the circulation.
Another characteristic animal acquisition was motility, which was ensured by a variety of mechanisms, mostly dependent on the operation of special organs, the muscles. Organisms were thereby provided with all sorts of ways to seek food, find mates, join in groups, escape or fight predators, and soon. With motility came the neurons and the beginnings of a nervous system, serving first to adapt motile responses to sensory influxes and developing further into increasingly complex regulatory networks, thanks to the ability of neurons to establish connections (synapses) with each other. Chemical transmitters evolved as a means to use these connections to transmit signals from neuron to neuron, and these transmitters eventually developed into hormonal systems. Finally, all kinds of specializations were built around the all-important function of reproduction (see chapter 5).
These events gave rise first to the rich world of marine invertebrates, which include the sponges and jellyfish already mentioned, corals, sea anemones, different kinds of worms, mollusks—characterized by a great variety of solid outer shells—arthropods, such as lobsters, crabs, and other crustaceans—distinguished by an articulated outer skeleton made of a very tough substance called chitin—and, characterized by a peculiar fivefold symmetry, echinoderms, of which starfish and sea urchins are the best-known representatives.
A key event that occurred at some early stage of this development was the repeated duplication of a central set of genes (see chapter 6), which led to segmentation, the building of bodies made of a large number of similar units. Almost identical at first, as in the familiar earthworms, these units later evolved into a wide variety, illustrated, for example, by the antennae, claws, and other appendages of crustaceans. Eventually, the units produced the characteristic segments of vertebrates, starting with primitive fish, which further evolved into more advanced fish and, from these, into all the forms that followed.
Adaptation of animals to living on land involved several key acquisitions: a skin capable of protecting against desiccation, a mechanism for deriving oxygen from air instead of from water, and a motor system allowing movement on land. Ability to reproduce on land, as we shall see in chapter 5, was another essential requisite. Remarkably, several distinct such adaptations developed at different stages of animal evolution. For example, marine worms turned into nematodes and, in a later, segmented line, into earthworms; aquatic mollusks evolved into snails; and arthropods gave rise to the vast group of insects and arachnids (spiders, scorpions, and the like). As to vertebrates, their transition from water to land probably took place in shallow tropical lakes that periodically evaporated during the dry season and regained water during the rainy season. Some fish, known as lungfish, of which species still exist today, became able to survive on land thanks to a dryness-resistant skin, rudimentary lungs derived from the swim bladder, and modified fins converted into primitive limbs. Thus arose, some 400 million years ago, the first amphibians, represented today by animals such as frogs, salamanders, and toads, which still depend on water for their early development. Then, about 350 million years ago, some amphibians evolved into the first vertebrates fully adapted to live and reproduce on land, the reptiles, made famous by the giant dinosaurs, which fill museums with their spectacular remains and have inspired innumerable works of fiction.
Further vertebrate evolution took place on land. Some dinosaurs acquired feathers, perhaps serving initially as a protection against a cold climate, and eventually turning into primitive wings that allowed the animals to glide and, later, to fly. First revealed by archaeopteryx, the fossil of a feathered, presumably flying dinosaur, discovered in 1864 in a Bavarian schist quarry, this story has since received confirmation from a number of fossils found in China. Its outcome is the appearance of birds, about 150 million years ago.
Other dinosaurs became covered with hair and acquired milk-secreting glands on their chest, allowing females to feed their young. This acquisition led, some 225 million years ago, to the first mammals. These creatures remained small, enjoying a relatively modest existence in the shadow of the monstrous dinosaurs, until some 65 million years ago, when a planetary catastrophe, probably initiated by the fall of a large meteorite on the Yucatán Peninsula in Mexico, precipitated the massive extinction of dinosaurs and many other animal and plant species. Subsequent to this cataclysm, mammals underwent an extraordinary development and came to occupy all environments, even returning to the sea in some cases, as happened to the ancestors of seals and whales. Mammals gave rise, some 70 million years ago, to the primate group, out of which a line detached, some 6–7 million years ago, that was to lead to the human species.
Viewing this grand history (fig. 3.1), or rather its present outcome, through the eyes of the prophets who wrote the Bible or of medieval scholars, who didn’t even know about microbes, one can readily understand how this whole pageantry was viewed as given once and for all, brought into being by a Creator for the sole benefit of humankind. Even the eighteenth-century Swedish naturalist Carl von Linné (1707–1778), who did know about microbes and who spent his entire career observing and describing living organisms, patiently classifying them into species, genera, families, orders, classes, phyla, and kingdoms, failed to see that the kinships he was recognizing rested, like those of human families, on a vast genealogical tree springing from a single root. Linné remained all his life an unconditional defender of “fixism” and adhered staunchly to the biblical story. Even his later French successor Georges Cuvier (1769–1832), the founder of comparative anatomy and paleontology, adamantly refused to accept the transformist hypothesis proposed by his rival Lamarck, even though he was hardly influenced by biblical creationism. We don’t have their excuses today. Evolution, as we have seen, no longer calls for demonstration.
Fig. 3.1. The main steps in the history of life, in particular of animals. Note that life remained exclusively unicellular during 2.5 billion years. The first animals appeared 600 million years ago, after life had already accomplished five-sixths of its history. The human species dates back a mere 200,000 years, the equivalent of the last half-hour if life had started one year earlier (and animals two months earlier).