The concept of organic evolution implies descent of all living and extinct forms from one or more common ancestors in the distant past of earth history. During recent decades, traditional phylogenetic deductions from the anatomy of living and fossil organisms have been supplemented by a vast and growing new body of molecular evidence. Each living creature contains a genome consisting of linear sequences of DNA bases, millions or billions of them, which determine all the developmental, anatomical and physiological characteristics of that species. This DNA is transcribed into messenger RNA (mRNA) which uses the machinery of the cell to make proteins. The sequence of mRNA bases determines the sequence of amino acids of the resultant protein (Lowenstein, 1986).

The fossilization potential of organic molecules is extremely variable. Some organic compounds which are very common in living organisms are extremely rare in the fossil record, and are only preserved under exceptional conditions. For example DNA, despite its abundance in living organisms, is apparently only rarely preserved in recognizable form as fossils, primarily because it is concentrated in vulnerable soft-tissues, and the molecule itself is highly reactive and therefore easily broken down. In contrast the recognizable remains of molecules such as proteins, lipids and certain pigments are extremely abundant in the fossil record, to the extent that a group of fossilized molecules derived from bacterial cell walls is present in quantities which exceed that of the total organic carbon in the present day biosphere. Such preservation reflects the inherent relative stability of the molecular structure, or at least the relative stability of the building blocks of which it is constructed. Even simple biological molecules tend to be constructed from smaller molecular subunits, and their long-term stability, and ultimately their fossilization potential, depends both on the strength of the bonding between these smaller modular building blocks as well as on the durability of the building blocks themselves if they become dissociated during or after fossilization. As would be expected from their geological record, the constituent nucleic acids of DNA are much less stable than the amino acids which make up proteins.

It seems likely that I was invited to contribute to this course because I am a renegade geologist. Many years ago I was lured by the attractions of living animals and switched to zoology. Later I became interested in the possibility of using immunological methods to assess evolutionary relationships among shrews, moles, hedgehogs, tree-shrews, elephant-shrews, otter-shrews, golden-moles and tenrecs, and I set a graduate student onto this project. We also sought to explore the relationships between these so-called ‘Insectivora’ and other orders of mammals, using immunological techniques to estimate crude biochemical distances between the serum proteins of representative species.

Up to the 1960s, geology was the only source of information about the times when common ancestors lived. Since then, molecular genetics has become a major contributor to knowledge of these times. By comparing genetic macromolecules from any two living cells or species, one can now tell roughly when they had a common ancestor. Our contribution aims to trace this development and assess its implications. It is a suitable occasion to offer this perspective because 1987 was the 25th anniversary of the first inkling that genes and their protein products behave as evolutionary clocks (Zuckerkandl and Pauling, 1962). It should be noted that the term “molecular clock” was intended to imply that base substitutions accumulate on surviving molecular lineages at a fairly steady rate, not as steady as the ticking of a metronome but nearly as steady as the process of radioactive decay.

The problems of resolving phylogenetic relationships change with increasing evolutionary distance: very widely separated organisms, which share few phylogenetically helpful morphological features pose the greatest difficulties. Thus, the resolution of relationships between animal phyla and classes present some of the most challenging problems in systematic zoology and paleontology. Traditionally, relationships have been inferred on the basis of comparative anatomy, embryology, and the paleontological record. However, phyla are established on the basis of the unique features of their body plans, and have few shared derived characters to unite them. Even when similar features are available, homology can still be uncertain. The fossil record has been largely unavailable to provide the needed continuity of structure to establish such homologies between phyla and most classes. Generally, the best data for connecting major groups have come from detailed embryological data. But, even there, many ambiguous situations and conflicts of interpretation remain, and these problems are pervasive over a wide range of animal groups, both with and without extensive fossil records.

In 1962 Zuckerkandl & Pauling suggested that the amino acid sequence of proteins might evolve in a clock-like fashion and thus may be useful for phylogenetic reconstruction. Since then, many different molecular approaches to phylogenetic reconstruction have been proposed (Wilson et al., 1977). Enthusiasm for the clock hypothesis was dampened by the discovery that rates of molecular evolution for many macromolecules have been highly variable through time (Romero-Herrera et al., 1979). However, the contribution of molecular characters to the study of phylogeny is not necessarily dependent on the notion of a molecular clock and molecular approaches continue to be an important source of phylogenetic information. One of the more powerful and cost-effective molecular techniques for phylogenetic purposes is DNA-DNA hybridization, which measures the single-copy nuclear DNA sequence divergences between species.

It has become rather widely accepted in recent years that (1) during the geologic past, the Earth's atmosphere evolved from an initial “oxygen deficient” to a later “oxygen-rich” state; that (2) this change was a result chiefly of the cumulative effects of O2-producing “green plant-type” (including cyanobacterial) photosynthesis; and that (3) the transition occurred during the Precambrian, with stable oxygenic conditions having probably become established during the Early Proterozoic (viz., 2.5 to 1.7 Ga). Lines of evidence in support of these suppositions have been drawn from paleobiology, geology, mineralogy, isotopic and organic geochemistry, and comparative planetology – data well familiar to many paleontologists (for detailed discussion including a reference list of some 1,700 entries, see articles in Schopf, 1983). In addition, however, and although it is perhaps not widely recognized, it is of interest to note that the occurrence of such a transition seems also reflected by the nature and structure of the metabolic and biosynthetic pathways of extant living systems. To a paleontologist, this observation should not be surprising. Just as comparative studies of the embryology and structural adult anatomy of extant organisms can provide reliable evidence of phylogenetic relationships, comparative studies of biochemistry –in this case, of evolutionarily conservative, widespread, biochemical pathways – can similarly provide evidence of evolutionary derivation. And just as the structural morphology of currently living systems is a product of, having been influenced by, environments inhabited by evolutionary precursors (e.g., the limb structure of both aquatic and flying mammals reflecting derivation from lineages earlier adapted to the land environment), metabolic and biosynthetic pathways, especially required pathways involved in processes or producing products fundamental to survival, can be expected to provide evidence of past environmental conditions.

Curiosity about the history of life on our planet is a major motivational force for earth scientists. Fossil organic compounds, the components of petroleum and sedimentary organic matter, record aspects of the evolution of the biosphere from as far back as 1.8 billion years and perhaps longer. Elucidation of this record is continually advancing as a result of the concerted interests and efforts of geologists, biologists and chemists. It is also aided by advances in technique and instrumentation. Fascinating new developments and insights abound. In this paper I review some early landmarks and discuss the recent progress made in organic geochemistry, particularly as it applies to biomarker research. The examples of recent work are heavily biased toward my own interests and are not intended to be comprehensive. Because the literature citations are also selective and rely heavily on reviews, readers are advised to seek out the primary literature for accurate detail of specific subjects.

It is conventional to view the origin and early evolution of life as having taken place beneath an atmosphere devoid of free oxygen. Of primary concern is the fact that experiments designed to produce simple prebiotic compounds as precursor “building-blocks” for life are generally successful only if free oxygen is lacking from the starting mixture of gases. Clearly, life could hardly have evolved in the absence of suitable starting materials. Secondly, organic compounds are thermodynamically susceptible to oxygen and, given enough time, will become oxidized, ultimately to carbon dioxide. A centerpiece of biochemical evidence commonly invoked to support early anoxic conditions is the fact that almost all of the metabolic pathways for respiratory electron transfer in aerobic organisms take place anaerobically. Only the last step in the process requires free oxygen. It is easy to argue that this last step was an evolutionary response to the development of oxygenic conditions and was a later addition to the less energy-efficient pathways found in primitive anaerobes. The assumption in arguments of this type is that the present-day descendants of these early, primitive organisms are using similar biochemical pathways today that they used billions of years ago. For paleobiologists the meagre early Precambrian fossil record is of minimal help and such a uniformitarian approach toward deciphering early evolution is, together with the protein and nucleic acid sequence studies, one of the few methodologies available to go on.

Organisms from all five phylogenetic kingdoms form minerals. No less than 60 different mineral types are known, to date, to be formed by organisms and these are located at a wide variety of tissue sites and fulfill a host of different functions (Lowenstam and Weiner, 1989). A prominent and well known function of biogenic minerals is to provide mechanical strength to skeletons and often at the same time to act as a reservoir for the supply of ions necessary for vital metabolic functions. A characteristic of the mineral component of most skeletons is that it is formed under unusually well controlled conditions, such that the mineral form bears no morphological resemblance to its inorganic counterpart. This is, for the most part, achieved by inducing the minerals to precipitate in preformed spaces located by complex assemblies of macromolecules or vesicles or in some cases by combinations of both.

Molecular biology has contributed to the construction of the neoDarwinian synthesis, as it is articulated in the 1980's, in two ways. First, it has provided a nearly complete understanding of the processes of DNA replication and expression, and mutation. We know in detail how genotypes are passed on and how random mutation can provide the variation which must be present in populations if natural selection is to “cause” evolution. (We do not yet understand in detail how genotype determines phenotype in any complex multicellular organism, but there is probably no barrier other than complexity in our way.) Second, molecular biology has provided us with a data base from which to draw conclusions about phylogenetic relationships between species, or between genes, and a powerful way of approaching that data base. Zuckerkandl and Pauling's (1965) contention – that comparisons of amino acid or nucleotide sequences of homologous proteins or nucleic acids from contemporary species should allow measurements of phylogenetic distance – has been amply confirmed. Earlier chapters in this volume provide some details about methods and their application to major groups of organisms. Here I would like to discuss what molecular sequence data, and phylogenetic conclusions drawn from them, might have to say about the very earliest stages of Darwinian evolution, before there were cells.