Towards a postmodern synthesis of evolutionary biology

Abstract

In 2009, we are celebrating the 200th anniversary of Charles Darwin and the 150th jubilee of his masterpiece, the Origin of Species. Darwin developed the first coherent and compelling narrative of biological evolution and thus founded evolutionary biology—and modern biology in general, remembering the famous dictum of Dobzhansky. It is, however, counter-productive, and ultimately, a disservice to Darwin’s legacy, to define modern evolutionary biology as neo-Darwinism. The current picture of evolution, informed, in particular, by results of comparative genomics and systems biology, is by far more complex than that presented in the Origin of Species, so that Darwinian principles, including natural selection, are incorporated into the evolving new synthesis as important but certainly not all-embracing tenets. This expansion of evolutionary biology does not denigrate Darwin in the least but rather emphasizes the fertility of his ideas.

The year 2009 is marked by great anniversaries of evolutionary biology: 200 years since Charles Darwin’s birth, 150 years since the publication of On the Origin of Species¹ and 200 years of Jean-Baptiste Lamarck’s early evolutionary synthesis Philosophie Zoologique.² Moreover, the 100th anniversary of the Origin was marked by the generally recognized consolidation of the Modern Synthesis of evolutionary biology, so neo-Darwinism is celebrating its 50th anniversary.^3,4

I am typing these words on Darwin’s actual birthday, February 12, so a brief reflection on the current status of “Darwinism” seems appropriate. Darwin’s achievement is genuinely monumental. Although the fact of evolution was asserted earlier, in the most systematic form by Lamarck, Darwin was the first to postulate that evolution was responsible for the emergence of the entire diversity of life on earth and to buttress this postulate by proposing and elaborating a plausible underlying mechanism. At the conceptual level, Darwin’s principal feat is that he was the first to introduce the interplay of chance, in the form of random, undirected variation and necessity, epitomized by natural selection, as the basis of the evolutionary process. For obvious reasons, Darwin’s vision of evolution lacked the essential foundation in genetics. This major shortcoming was remedied with the development of population genetics in the first half of the 20th century, and the new, genetically-founded interpretation of Darwinian evolution was codified in the Modern Synthesis (neo-Darwinism).

Fifty years after the consolidation of the Modern Synthesis, comparative genomics that came of age in the 1990s and systems biology, a signature development of the first decade of the new millenium, present evolutionary biology both with a new challenge and with an unprecedented opportunity for new conceptual break-throughs.⁵ How do Darwinian principles, amended but essentially unchanged by the Modern Synthesis, fare in the age of genomics? In the rest of this essay, I discuss six major tenets of neo-Darwinism and their reappraisal informed by the results of genome analysis. Of course, it is impossible to present the evidence in a short note; a much more detailed discussion appears elsewhere.⁶

1. Random, undirected variation is the primary process that provides the material for evolution. Darwin was the first to realize the crucial importance of chance in the history of life, a truly revolutionary idea.

   Post-genomic view: Darwinian vision holds but the repertoire of random changes that are important for evolution is greatly expanded to include duplication of genes, genome regions, and entire genomes, loss of genetic material, horizontal gene transfer, invasion of mobile selfish elements into genomes, and other types of events.

2. The principal driving force of evolution according to Darwin and the Modern Synthesis evolution is natural selection, that is, fixation of the rare beneficial variations and elimination of deleterious variations. Natural selection is the deterministic component of Darwin’s dyad and the first simple and plausible mechanism of evolution ever proposed. In the early days of population genetics, it was proposed by Sewall Wright that chance could be important not only for the origination of the material for evolution but also for the fixation of changes, owing to genetic drift, that is, random fixation of neutral or even moderately deleterious changes. Drift is particularly common in small populations that go through bottlenecks.^7,8 However, the “hardened” form of the Modern Synthesis⁹ rejected drift as an important evolutionary force, and adopted a purely adaptationist model of evolution.¹⁰ This model implies continuous “progress” in evolution, a concept that Darwin embraced as a general trend, despite his understanding that organisms are less than perfectly adapted, as exemplified, in particular, by rudimentary organs.

   Post-genomic view: The new picture of evolution is incomparably more pluralistic. Natural selection of beneficial mutations is an important factor of evolution but is only one of several major forces and not the quantitatively dominant one; on the contrary, genome evolution appears to be dominated by neutral processes combined with purifying selection. Genomic complexity that is particularly prominent in animals and plants is, probably, not originally adaptive but rather evolved, primarily, as a “genomic syndrome” owing to the low intensity of purifying selection in small populations.¹¹ There is no consistent trend towards increasing complexity in evolution, and the notion of evolutionary progress is unwarranted.^6,12

3. Darwin insisted on strict gradualism of evolution: the beneficial changes that are fixed by natural selection are “infinitesimally” small, and all evolution proceeds via the gradual accumulation of these tiny modifications.¹ Although even some contemporary supporters of Darwin, in particular Thomas Huxley,¹³ believed that gradualism was an unnecessary stricture on the theory, this concept was inherited by the Modern Synthesis.

   Post-genomic view: Gradualism is unsustainable as a general principle of evolution. Gene duplications and horizontal gene transfer that are among the principal driving forces of evolution are substantial genomic changes, certainly, not “infinitesimally small” ones. Furthermore, rare catastrophic events, such as endosymbiosis accompanied by massive horizontal transfer of genes and whole genome duplication, play a pivotal role in evolution.

4. In addition to gradualism, Darwin emphasized that the evolutionary processes remained, essentially, the same throughout the history of life—evolution followed the principle of uniformitarianism borrowed from the classic geological work of Charles Lyell.

   Post-genomic view: The fundamental unity of evolutionary processes observed in extremely diverse organisms suggests that uniformitarianism is, in general, a valid concept. However, the earliest stages of evolution probably involved processes distinct from those that operate in the course of subsequent “normal” evolution. Major transitions in evolution like the origin of eukaryotes appear to be triggered by (nearly) unique events such as endosymbiosis.^14,15

5. Evolution of life is adequately depicted as a “great tree” that is shown on the single, famous illustration of the Origin (reference 1, Chapter 4).

   Post-genomic view: The discovery of the crucial contributions of horizontal gene transfer and mobile genetic elements to genome evolution invalidate the concept of a Tree of Life (TOL) in its original, strong sense.¹⁶ It became clear that evolution of life can only be represented by a more complex graph, with tree-like phases interspersed with those where only a network representation is adequate.¹⁷ Nevertheless, trees remain essential tools to describe evolution of individual genes and many intervals in of evolution of groups of relatively close organisms where large sets of genes evolve congruently. The possibility of salvaging the TOL as a central trend of evolution remains open and merits careful investigation.

6. A crucial corollary of the TOL concept is the existence of a single common ancestor (or very few ancestral forms, under Darwin’s cautious formula 1 in reference 1, chapter 14) of all extant life forms for which the name Last Universal Common (Cellular) Ancestor (LUCA) was coined much later.¹⁸

   Post-genomic view: the results of comparative genomics leave no doubt of the common ancestry of all modern cellular life forms. However, there is also evidence that LUCA might have been dramatically different from modern cells, possibly, a loose conglomerate of virus-like genetic elements that more appropriately would be denoted LUCAS, a Last Universal Common Ancestral State.⁶

The revision of these fundamental concepts indicates that the Modern Synthesis is no longer a viable framework for evolutionary biology, and a “postmodern synthesis” will have to replace it. Is such a new framework in sight? Not in its entirety but some key components of the new edifice are clear and include the new, not necessarily adaptive evolutionary concepts outlined above along with novel insights into evolution derived from systems biology results. This burgeoning discipline yields vast amounts of genome-wide data from which universal patterns can be extracted such as (to give just one prominent example) the strong inverse correlation between a gene’s sequence evolution rate and expression level¹⁹ that gave rise to a new theory of gene evolution that does not directly invoke biological functions of genes.^20,21

Very often these days, discussions on evolution, especially those that involve the public, and in particular, attacks on evolution from the standpoint of Intelligent Design and similar lines of “creative thought” revolve around the validity of Darwinism, or more bluntly put, the notorious question: Was Darwin right or wrong? I hope that the above brief recapitulation of the main propositions of neo-Darwinism in light of genomics shows that this type of discussion is either misunderstanding or demagoguery. Today’s evolutionary biology is not “neo-Darwinism” but rather a much more complex scientific framework to which neo-Darwinian concepts make an important but limited contribution.^5,22,23 In that sense, the fate of Darwin’s theory is the same as that of other major scientific theories of old that become approximations, sometimes, applicable under special circumstances, within new, more comprehensive theoretical constructs (fortunately, the validity of modern physics is not often questioned on the basis of claims that “Newton was wrong”). What seems unusual, given the state of science in the middle of the 19th century, is on how many important issues Darwin was actually close to the truth, most importantly, on the groundbreaking integration of chance and necessity in his account of evolution.

The new developments in evolutionary biology by no account should be viewed as refutation of Darwin. On the contrary, they are widening the trails that Darwin blazed 150 years ago and reveal the extraordinary fertility of his thinking.