11.24.1 The modern evolutionary synthesis

The modern evolutionary synthesis is a union of ideas from several biological specialties which forms a logical account of evolution. The synthesis was produced over about a decade (1936–1947), and the development of population genetics (1918–1932) was the stimulus. This showed that Mendelian genetics was consistent with natural selection and gradual evolution. The synthesis is still, to a large extent, the current paradigm in evolutionary biology.

The modern synthesis solved difficulties and confusions caused by the specialisation and poor communication between biologists in the early years of the 20th century. Discoveries of early geneticists were difficult to reconcile with gradual evolution and the mechanism of natural selection. The synthesis reconciled the two schools of thought, while providing evidence that studies of populations in the field were crucial to evolutionary theory.

11.24.1.1 Developments leading up to the synthesis

Charles Darwin‘s “The Origin of Species” was successful in convincing most biologists that evolution had occurred, but was less successful in convincing them that natural selection was its primary mechanism. In the 19th and early 20th centuries, variations of Lamarckism, orthogenesis (‘progressive’ evolution), and saltationism (evolution by jumps) were discussed as alternatives. As part of the disagreement about whether natural selection alone was sufficient to explain speciation, George Romanes coined the term neo-Darwinism to refer to the version of evolution advocated by Alfred Russel Wallace and August Weismann with its heavy dependence on natural selection.

Weismann’s idea was that the relationship between the hereditary material (the germ plasm) and the rest of the body (the soma) was a one-way relationship: the germ-plasm formed the body, but the body did not influence the germ-plasm, except indirectly in its participation in a population subject to natural selection. Later, after the completion of the modern synthesis, the term neo-Darwinism would come to be associated with its core concept of evolution being driven by natural selection acting on variation produced by genetic mutation and recombination.

11.24.1.2 1900–1915

Gregor Mendel‘s work was re-discovered by Hugo de Vries and Carl Correns in 1900. The early Mendelians viewed hard inheritance as incompatible with natural selection and favoured saltationism (large mutations or jumps) instead. The biometric school, led by Karl Pearson and Walter Weldon, argued vigorously against it, saying that empirical evidence indicated that variation was continuous in most organisms, not discrete as Mendelism predicted.

11.24.1.3 The foundation of population genetics

The first step towards the synthesis was the development of population genetics. In 1918, Fisher’s paper “The Correlation Between Relatives on the Supposition of Mendelian Inheritance“, showed how the continuous variation measured by the biometricians could be the result of the action of many discrete genetic loci. Fisher’s 1930 book “The Genetical Theory of Natural Selection” shows how Mendelian genetics was, contrary to the thinking of many early geneticists, completely consistent with the idea of evolution driven by natural selection. Haldane established that natural selection could work in the real world at a faster rate than even Fisher had assumed.

In a 1932 paper Sewall Wright introduced the concept of an adaptive landscape in which phenomena such as cross breeding and genetic drift in small populations could push them away from adaptive peaks, which would in turn allow natural selection to push them towards new adaptive peaks. The work of Fisher, Haldane and Wright founded the discipline of population genetics. This is the precursor of the modern synthesis, a broader coalition of ideas.

11.24.1.4 The modern synthesis

Theodosius Dobzhansky, a Ukrainian was one of the first to apply genetics to natural populations. His 1937 work “Genetics and the Origin of Species” was a key step in bridging the gap between population geneticists and field naturalists. It presented the conclusions reached by Fisher, Haldane, and especially Wright in their highly mathematical papers in a form that was easily accessible to others. Dobzhansky argued that natural selection worked to maintain genetic diversity as well as driving change

As a result Ford’s work, Dobzhansky changed the emphasis in the third edition of his famous text from drift to selection. Ford was an experimental naturalist who wanted to test natural selection in nature. He virtually invented the field of research known as ecological genetics. Ford was the first to describe and define genetic polymorphism, and to predict that human blood group polymorphisms might be maintained in the population by providing some protection against disease.

Ernst Mayr‘s key contribution to the synthesis was “Systematics and the Origin of Species”, published in 1942. Mayr emphasized the importance of allopatric speciation, where geographically isolated sub-populations diverge so far that reproductive isolation occurs. Mayr also introduced the biological species concept that defined a species as a group of interbreeding or potentially interbreeding populations that were reproductively isolated from all other populations.

In the 1920s Rensch, who like Mayr did field work in Indonesia, analyzed the geographic distribution of polytypic species and complexes of closely related species. In 1947 Rensch wrote a book, under the English title “Evolution above the species level”, that looked at how the same evolutionary mechanisms involved in speciation might be extended to explain the origins of the differences between the higher level taxa.

George Gaylord Simpson was responsible for showing that the modern synthesis was compatible with palaeontology in his book “Tempo and Mode in Evolution” published in 1944. Simpson’s work was crucial because so many palaeontologists had disagreed with the idea that natural selection was the main mechanism of evolution. It showed that the trends of linear progression did not hold up under careful examination. Instead the fossil record was consistent with the irregular, branching, and non-directional pattern predicted by the modern synthesis.

The botanist G. Ledyard Stebbins was another major contributor to the synthesis. His major work, “Variation and Evolution in Plants”, published in 1950, extended the synthesis to encompass botany including the important effects of hybridization and polyploidy in some kinds of plants.

11.24.1.5 Tenets of the modern synthesis

The modern synthesis bridged the gap between experimental geneticists and naturalists. I summary modern syntheses state:

1. All evolutionary phenomena can be explained in a way consistent with known genetic mechanisms and the observational evidence of naturalists.
2. Evolution is gradual: small genetic changes, recombination ordered by natural selection. Discontinuities amongst species are explained as originating gradually through geographical separation and extinction.
3. Selection is overwhelmingly the main mechanism of change; even slight advantages are important when continued.
4. The primacy of population thinking: the genetic diversity carried in natural populations is a key factor in evolution. The strength of natural selection in the wild was greater than expected.
5. In palaeontology, the ability to explain historical observations by extrapolation from micro to macro-evolution is proposed. Gradualism does not mean constant rate of change.

The idea that speciation occurs after populations are reproductively isolated has been much debated. In plants, polyploidy must be included in any view of speciation. Formulations such as ‘evolution consists primarily of changes in the frequencies of alleles between one generation and another’ were proposed rather later. The traditional view is that developmental biology played little part in the synthesis.

There is no doubt that the synthesis was a great landmark in evolutionary biology. It cleared up much confusion, and was directly responsible for stimulating a great deal of research in the post-World War II era.

11.24.1.6 Further advances

The work of W. D. Hamilton, George C. Williams, John Maynard Smith and others led to the development of a gene-centric view of evolution in the 1960s. The synthesis as it exists now has extended the scope of the Darwinian idea of natural selection to include subsequent scientific discoveries and concepts unknown to Darwin, such as DNA and genetics, which allow rigorous, in many cases mathematical, analyses of phenomena such as kin selection, altruism, and speciation.

A particular interpretation most commonly associated with Richard Dawkins asserts that the gene is the only true unit of selection. Dawkins further extended the Darwinian idea to include non-biological systems exhibiting the same type of selective behaviour of the ‘fittest’ such as memes in culture.

11.24.2 Understanding of Earth history

The Earth is the stage on which the evolutionary play is performed. Darwin studied evolution in the context of Charles Lyell‘s geology, but our present understanding of Earth history includes some critical advances made during the last half-century.

• The age of the Earth has been revised upwards. It is now estimated at 4.56 billion years, about one-third of the age of the universe.

• Alfred Wegener‘s idea of continental drift came around 1960. This discovery provides a unifying theory for geology, linking phenomena such as volcanoes, earthquakes, orogeny, and providing data for many paleogeographical questions.

• The substitution of oxygen for carbon dioxide in the atmosphere, which occurred in the Proterozoic, caused probably by cyanobacteria in the form of stromatolites, caused changes leading to the evolution of aerobic organisms.

• The identification of the first generally accepted fossils of microbial life was made by geologists. These rocks have been dated as about 3.465 billion years ago.

• Information about paleoclimates is increasingly available, and being used in paleontology. One example: the discovery of massive ice ages in the Proterozoic, following the great reduction of CO₂ in the atmosphere.

• Catastrophism and mass extinctions. A partial reintegration of catastrophism has occurred, and the importance of mass extinctions in large-scale evolution is now apparent. Causes include meteorite strikes; flood basalt provinces; Siberian traps; and other less dramatic processes.

Our present knowledge of earth history suggests strongly that large-scale geophysical events influenced macroevolution and mega-evolution. These terms refer to evolution above the species level, including such events as mass extinctions, adaptive radiation, and the major transitions in evolution.

11.24.3 Trees of life

The ability to analyse sequence in macromolecules (protein, DNA, RNA) provides evidence of descent, and allows producing genealogical trees covering the whole of life. The tree that results has some unusual features, especially in its roots. Bacteria can pass genetic material to other bacteria; their relationships look more like a web than a tree. Once eukaryotes were established, their sexual reproduction produced the traditional branching tree-like pattern. The last universal common ancestor (LUCA) would be a prokaryotic cell before the split between the bacteria and archaea. LUCA is defined as most recent organism from which all organisms now living on Earth descend (some 3.5 to 3.8 billion years ago, in the Archean era).

Early attempts to identify relationships between major groups were made in the 19th century by Ernst Haeckel, and by comparative anatomists such as Thomas Henry Huxley and E. Ray Lankester.

11.24.4 Evo-devo

What was called once embryology played a modest role in the evolutionary synthesis. Man himself was, according to Bolk, a typical case of evolution by retention of juvenile characteristics (neoteny). He listed many characters where “Man, in his bodily development, is a primate foetus that has become sexually mature”. His list of characters is both interesting and convincing.

Modern interest in Evo-devo springs from clear proof that development is closely controlled by special genetic systems. In a series of experiments with the fruit-fly Drosophila, Edward B. Lewis was able to identify a complex of genes whose proteins bind to the cis-regulatory regions of target genes. The latter then activate, or repress, systems of cellular processes that accomplish the final development of the organism. Each of the genes contains a homeobox, a remarkably conserved DNA sequence. This suggests the complex itself arose by gene duplication.

The term deep homology was coined to describe the common origin of genetic regulatory apparatus used to build morphologically and phylogenetically disparate animal features. It applies when a complex genetic regulatory system is inherited from a common ancestor, as it is in the evolution of vertebrate and invertebrate eyes. The phenomenon is implicated in many cases of parallel evolution.

11.24.5 Fossil discoveries

Many outstanding discoveries have been made, and some of these have implications for evolutionary theory. The discovery of feathered dinosaurs and early birds from the Lower Cretaceous of Liaoning, N.E. China have convinced most students that birds did evolve from coelurosaurian theropod dinosaurs.

A shaft of light has been thrown on the evolution of flatfish (pleuronectiformes), such as plaice, sole, turbot and halibut, by recent work. Their young are perfectly symmetrical, but the head is remodelled during a metamorphosis, which entails the migration of one eye to the other side, close to the other eye. Some species have both eyes on the left (turbot), some on the right (halibut, sole); all living and fossil flatfish to date show an ‘eyed’ side and a ‘blind’ side.

A recent examination of two fossil species from the Eocene has provided the first clear picture of flatfish evolution. The discovery of stem flatfish with incomplete orbital migration refutes Goldschmidt’s ideas, and demonstrates that “the assembly of the flatfish bodyplan occurred in a gradual, stepwise fashion”. The evolution of flatfish falls squarely within the evolutionary synthesis.

11.24.6 Developmental systems theory

In biology the developmental systems theory (DST) is a collection of models of biological development and evolution that argue that the emphasis the modern evolutionary synthesis places on genes and natural selection as explanation of living structures and processes is inadequate. Developmental systems theory embraces a range of positions, from the view that biological explanations need to include more elements than genes and natural selection, to the view that modern evolutionary theory profoundly misconceives the nature of living processes and should be rejected completely.

11.24.6.1 Overview

All versions of developmental systems theory espouse the view that:

• All biological processes operate by continually assembling new structures.

• Each such structure transcends the structures from which it arose and has its own systematic characteristics, information, functions and laws.

• Conversely, each such structure is ultimately irreducible to any lower (or higher) level of structure, and can be described and explained only on its own terms.

• Furthermore, the major processes through which life as a whole operates, including evolution, heredity and the development of particular organisms, can only be accounted for by incorporating many more layers of structure and process than the conventional concepts of ‘gene’ and ‘environment’ normally allow for.

Although it does not claim that all structures are equal, development systems theory is fundamentally opposed to reductionism of all kinds. Developmental systems theory intends to formulate a perspective which does not presume the causal (or ontological) priority of any particular entity and thereby maintains an explanatory openness on all empirical fronts.

11.24.6.2  Developmental systems theory: Topics

– A computing metaphor

To adopt a computing metaphor the reductionists assume that causal factors can be divided into ‘processes’ and ‘data’. Data (inputs, resources, content, and so on) is required by all processes, and must often fall within certain limits if the process in question is to have its ‘normal’ outcome. However, the data alone is helpless to create this outcome, while the process may be ‘satisfied’ with a considerable range of alternative data. Developmental systems theory assumes that the process/data distinction is at best misleading and at worst completely false. In fact, for the proponents of DST, either all structures are both process and data, depending on context, or even more radically, no structure is either.

– Fundamental asymmetry

For reductionists there is a fundamental asymmetry between different causal factors, whereas for DST such asymmetries can only be justified by specific purposes, and argue that many of the (generally unspoken) purposes to which such (generally exaggerated) asymmetries have been put are scientifically illegitimate. Thus, for developmental systems theory, many of the most widely applied, asymmetric and entirely legitimate distinctions biologists draw obtain their legitimacy from the conceptual clarity and specificity with which they are applied, not from their having tapped a profound and irreducible ontological truth about biological causation. One problem might be solved by reversing the direction of causation correctly identified in another.

– DST approach

Developmental systems theory states that what is inherited from generation to generation is a good deal more than simply genes. As a result, much of the conceptual framework that justifies ‘selfish gene’ models is regarded by developmental systems theory as not merely weak but actually false. Not only are major elements of the environment built and inherited as materially as any gene but active modifications to the environment by the organism demonstrably become major environmental factors to which future adaptation is addressed.

This inheritance may take many forms and operate on many scales, with a multiplicity of systems of inheritance complementing the genes. Development systems theory argues that not only inheritance, but evolution as a whole, can be understood only by taking into account a far wider range of ‘reproducers’, or ‘inheritance systems’, than neo-Darwinism’s ‘atomic’ genes and gene-like ‘replicators’. DST regards every level of biological structure as susceptible to influence from all the structures by which they are surrounded.

Developmental systems theory is radically incompatible with both neo-Darwinism and information processing theory. Whereas neo-Darwinism defines evolution in terms of changes in gene distribution, the possibility that an evolutionarily significant change may arise and be sustained without any directly corresponding change in gene frequencies is an elementary assumption of developmental systems theory. Neo-Darwinism’s ‘explanation’ of phenomena in terms of reproductive fitness is regarded as fundamentally shallow.

Likewise, the wholly generic, functional and anti-developmental models offered by information processing theory are comprehensively challenged by DST’s evidence that nothing is explained without an explicit structural and developmental analysis on the appropriate levels. As a result, what qualifies as ‘information’ depends wholly on the content and context out of which that information arises, within which it is translated and to which it is applied.

11.24.7 Evolutionary developmental biology

Evolutionary developmental biology is a field of biology that compares the developmental processes of different animals and plants in an attempt to determine the ancestral relationship between organisms and how developmental processes evolved. It addresses the origin and evolution of embryonic development:

–          How modifications of development and developmental processes lead to the production of novel features.

–          The role of developmental plasticity in evolution.

–          How ecology impacts in development and evolutionary change.

–          The developmental basis of homoplasy and homology.

Although interest in the relationship between ontogeny and phylogeny extends back to the nineteenth century, the contemporary field of evo-devo has gained impetus from the discovery of genes regulating embryonic development in model organisms. General hypotheses remain hard to test because organisms differ so much in shape and form. Just as evolution tends to create new genes from parts of old genes, evo-devo demonstrates that evolution alters developmental processes to create new and novel structures from the old gene networks.

11.24.7.1 Basic principles

At the time that Darwin wrote, the principles underlying heredity and variation were poorly understood. In the 1940s, however, biologists incorporated Gregor Mendel‘s principles of genetics to explain both, resulting in the modern synthesis. It was not until the 1980s and 1990s, however, when more comparative molecular sequence data between different kinds of organisms was amassed and detailed, that an understanding of the molecular basis of the developmental mechanisms has arisen. Currently, it is well understood how genetic mutation occurs.

Evolutionary developmental biology studies how the dynamics of development determine the phenotypic variation arising from genetic variation and how that affects phenotypic evolution. At the same time evolutionary developmental biology also studies how development itself evolves. Some evo-devo researchers see themselves as extending and enhancing the modern synthesis by incorporating into it findings of molecular genetics and developmental biology. Others, drawing on findings of discordances between genotype and phenotype and epigenetic mechanisms of development, are mounting an explicit challenge to neo-Darwinism.

Evo-devo seeks the genetic and evolutionary basis for the division of the embryo into distinct modules, and for the partly independent development of such modules.

Another central idea is that some gene products function as switches whereas others act as diffusible signals. Genes specify proteins, some of which act as structural components of cells and others as enzymes that regulate various biochemical pathways within an organism. Most biologists working within the modern synthesis assumed that an organism is a straightforward reflection of its component genes. The modification of existing, or evolution of new, biochemical pathways depended on specific genetic mutations. In 1961, however, Jacques Monod, Jean-Pierre Changeux and François Jacob discovered within the bacterium Escherichia coli a gene that functioned only when “switched on” by an environmental stimulus. These discoveries drew biologists’ attention to the fact that genes can be selectively turned on and off, rather than being always active, and that highly disparate organisms may use the same genes for embryogenesis, just regulating them differently.

11.24.7.2 History

An early version of recapitulation theory, also called the biogenetic law or embryological parallelism, was put forward by Étienne Serres in 1824–26 as what became known as the “Meckel-Serres Law”. It was supported by Étienne Geoffroy Saint-Hilaire as part of his ideas of idealism, and became a prominent part of his version of Lamarckism leading to disagreements with Georges Cuvier. In the 1850s Owen began to support an evolutionary view that the history of life was the gradual unfolding of a teleological divine plan, in a continuous “ordained becoming”, with new species appearing by natural birth.

11.24.8 Development and the origin of novelty

Among the more surprising and, perhaps, counterintuitive results of recent research in evolutionary developmental biology is that the diversity of body plans and morphology in organisms across many phyla are not necessarily reflected in diversity at the level of the sequences of genes. Indeed, as Gerhart and Kirschner have noted, there is an apparent paradox: “where we most expect to find variation, we find conservation, a lack of change”.

Even within a species, the occurrence of novel forms within a population does not generally correlate with levels of genetic variation sufficient to account for all morphological diversity.