"Darwinian evolution in the light of genomics" by Eugene V. Koonin review

The article "Darwinian evolution in the light of genomics" by Eugene V. Koonin challenges some of the central tenets of the Modern Synthesis of evolutionary biology. The Modern Synthesis is a model of evolution that was developed in the early 20th century and that combines Darwinian natural selection with Mendelian genetics.

Koonin argues that comparative genomics and systems biology have revealed new insights into genome evolution that are not well-explained by the Modern Synthesis. For example, he points out that the genomes of many organisms contain large amounts of non-coding DNA, which is DNA that does not code for proteins. This non-coding DNA is not subject to natural selection and therefore does not contribute to adaptation.

Koonin also argues that horizontal gene transfer, the process of genes being transferred from one organism to another, is a more important force in genome evolution than previously thought. Horizontal gene transfer can occur between closely related organisms, such as bacteria, or between distantly related organisms, such as bacteria and animals. It can result in the rapid acquisition of new genes, which can lead to rapid evolution.

Koonin's work has led to a new understanding of Darwinian evolution that is outside of the Modern Synthesis. This new understanding emphasizes the importance of non-coding DNA and horizontal gene transfer in genome evolution. It also suggests that evolution is a more complex and dynamic process than previously thought.

Here are some of the key points from Koonin's article:

• Natural selection is not the only force that shapes genome evolution.

• Non-coding DNA and horizontal gene transfer are more important forces in genome evolution than previously thought.

• The Tree of Life concept is outdated and needs to be replaced with a more complex model of evolution.

• Evolution is a more complex and dynamic process than previously thought.

Koonin's work has been controversial, but it has also helped to stimulate new research in evolutionary biology. It is likely that his work will continue to shape our understanding of Darwinian evolution for many years to come.

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Article snippets:

Comparative genomics and systems biology offer unprecedented opportunities for testing central tenets of evolutionary biology formulated by Darwin in the Origin of Species in 1859 and expanded in the Modern Synthesis 100 years later.

Evolutionary-genomic studies show that natural selection is only one of the forces that shape genome evolution and is not quantitatively dominant, whereas non-adaptive processes are much more prominent than previously suspected.

Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolution undermine the Tree of Life concept.

An adequate depiction of evolution requires the more complex concept of a network or ‘forest’ of life.

Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.

Of course, Darwin did not discover evolution and did not even offer the first coherent description of evolution—arguably, that honor belongs to Jean-Baptiste Lamarck whose magnum opus Philosophie Zoologique ( 4 ) was, uncannily, published in the year of Darwin's birth

Now, 50 years after the consolidation of the Modern Synthesis, evolutionary biology undoubtedly faces a new major challenge and, at the same time, the prospect of a new conceptual breakthrough

If the Modern Synthesis can be succinctly described as Darwinism in the Light of Genetics (often referred to as neo-Darwinism), then, the new stage is Evolutionary Biology in the Light of Genomics

What the theory actually maintains is that the dominant mode of selection is not the Darwinian positive selection of adaptive mutations, but stabilizing, or purifying selection that eliminates deleterious mutations while allowing fixation of neutral mutations by drift

Although this was rarely stated explicitly, classic genetics certainly implies that (nearly) all parts of the genome (all nucleotides in more modern, molecular terms) have a specific function.

This paradox was conceptually resolved by two related, fundamental ideas, those of selfish genes and junk DNA.

This view of the genome dramatically differs from the picture implied by the selectionist paradigm under which most if not all nucleotides in the genome would be affected by (purifying or positive) selection acting at the level of the organism

Gould and Lewontin sarcastically described the adaptationist worldview as the Panglossian paradigm, after the notorious character in Voltaire's Candide who insisted that ‘everything was to the better in this best of all worlds’ (even major disasters

Gould and Lewontin emphasized that, rather than hastily concoct ‘just so stories’ of plausible adaptations, evolutionary biologists should seek explanations of the observed features of biological organization under a pluralist approach that takes into account not only selection but also intrinsic constraints, random drift and other factors.

Although by 1950s, genetic analysis of bacteriophages and bacteria was well advanced, making it obvious that these life forms had evolving genomes ( 57 ), the Modern Synthesis made no notice of these developments

The fundamental principles of molecular evolution were established, and many specific observations of major importance and impact on the fundamentals of neo-Darwinism were made in the pre-genomic era

fundamental observation supported by the entire body of evidence amassed by evolutionary genomics is that the sequences and structures of genes encoding proteins and structural RNAs are, generally, highly conserved through vast evolutionary spans.

Moreover, deep evolutionary reconstructions suggest that ancestors of hundreds of extant genes were already present in LUCA

Conservative reconstructions of the gene sets of the common ancestors of the two domains of prokaryotes, bacteria and archaea, seem to indicate that these ancestral forms that, probably, existed over 3 billion years ago, were comparable in genetic complexity, at least, to the simpler of modern free-living prokaryotes

From an evolutionary biology perspective, it appears that the sequences of many genes encoding core cellular functions, especially, translation, transcription, replication and central metabolic pathways, are subject to strong purifying selection that remained in place for extended time intervals, on many occasions, throughout the ∼3.5 billion year history of cellular life.

Thus, the dominant factor in the evolution of genome architecture appears to be random, non-adaptive rearrangement rather than purifying or positive selection.

Horizontal gene transfer, the network of evolution and the Forest replacing of the TOL

The observations of extensive, ubiquitous and occurring via multiple routes HGT outlined above lead to a fundamental generalization: the genomes of all life forms are collections of genes with diverse evolutionary histories.

The corollary of this generalization is that the TOL concept must be substantially revised or abandoned because a single tree topology or even congruent topologies of trees for several highly conserved genes cannot possibly represent the history of all or even the majority of the genes

Thus, an adequate representation of life's history is a network of genetic exchanges rather than a single tree, and accordingly, the ‘strong’ TOL hypothesis, namely, the existence of a ‘species tree’ for the entire history of cellular life, is falsified by the results of comparative genomics.

burning question in genome-wide evolutionary studies, especially, for mammals with their huge genomes, what fraction of the non-coding DNA is ‘real’ junk, and how much is subject to yet unknown functional constraints.

The possibility that, despite the lack of detectable evolutionary conservation, a large fraction if not most of the human DNA is, in fact, functionally important and hence maintained by selection is often discussed, especially, in the light of the demonstrations that a very large fraction of the genome is transcribed

the demonstration of the primary evolutionary significance of duplications including duplications of large genome regions and whole genomes is a virtual death knell for Darwinian gradualism: even a single gene duplication hardly qualifies as an infinitesimally small variation whereas WGD qualifies as a bona fide saltatory event.

the primacy of gene duplication with the subsequent (sometimes, rapid) diversification of the paralogs as the route of novel gene origin reinforces the metaphor of evolution as a tinkerer: evolution clearly tends to generate new functional devices by tinkering with the old ones after making a backup copy rather than create novelty from scratch.

The next big question that begs to be asked with regard to complexity, both organizational and genomic, is: was there a consistent trend towards increasing complexity during the ∼3.5 billion years of life evolution on earth?

The most likely answer is, no. Even very conservative reconstructions of ancestral genomes of archaea and bacteria indicate that these genomes were comparable in size and complexity to those of relatively simple modern forms

On the whole, the theoretical and empirical studies on the evolution of genomic complexity suggest that there is no trend for complexification in the history of life and that, when complexity does substantially increase, this occurs not as an adaptation but as a consequence of weak purifying selection, in itself, paradoxical as this might sound, a telltale sign of evolutionary failure. It appears that these findings are sufficient to put to rest the notion of evolutionary ‘progress’, a suggestion that was made previously on more general grounds.

the final decade of the 20th century was the age of genomics when the quantity of genome sequences was transformed into a new quality, allowing novel generalization, such as the ‘uprooting’ the TOL,

Two centuries after Darwin's birth, 150 years after the publication of his ‘Origin of Species’, and 50 years after the consolidation of the Modern Synthesis, comparative analysis of hundreds of genomes from many diverse taxa offers unprecedented opportunities for testing the conjectures of (neo)Darwinism and deciphering the mechanisms of evolution

In addition to point mutations that can be equated with Darwin's ‘infinitesimal changes’, genome evolution involves major contributions from gene and whole genome duplications, large deletions including loss of genes or groups of genes, horizontal transfer of genes and entire genomic regions, various types of genome rearrangements, and interaction between genomes of cellular life forms and diverse selfish genetic elements.

The majority of the sequences in all genomes evolve under the pressure of purifying selection or, in organisms with the largest genomes, neutrally, with only a small fraction of mutations actually being beneficial and fixed by natural selection as envisioned by Darwin.

Evolutionary genomics effectively demolished the straightforward concept of the TOL by revealing the dynamic, reticulated character of evolution where HGT, genome fusion, and interaction between genomes of cellular life forms and diverse selfish genetic elements take the central stage.

So the TOL becomes a network, or perhaps, most appropriately, the Forest of Life that consists of trees, bushes, thickets of lianas, and of course, numerous dead trunks and branches.

the insistence on adaptation being the primary mode of evolution that is apparent in the Origin , but especially in the Modern Synthesis, became deeply suspicious if not outright obsolete, making room for a new worldview that gives much more prominence to non-adaptive processes.