Article - Darwinian evolution in the light of genomics

Article - Darwinian evolution in the light of genomics -...

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Published online 12 February 2009 Nucleic Acids Research, 2009, Vol. 37, No. 4 1011–1034 doi:10.1093/nar/gkp089 SURVEY AND SUMMARY Darwinian evolution in the light of genomics Eugene V. Koonin* National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA Received January 9, 2009; Revised January 30, 2009; Accepted February 4, 2009 ABSTRACT Comparative genomics and systems biology offer unprecedented opportunities for testing cen- tral 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 domi- nant, whereas non-adaptive processes are much more prominent than previously suspected. Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolu- tion undermine the Tree of Life concept. An ade- quate depiction of evolution requires the more complex concept of a network or ‘forest’ of life. There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non- adaptive consequence of evolution under weak pur- ifying selection rather than an adaptation. Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse gen- omes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate. Simple, non-adaptive models of evolution explain some of these univer- sals, suggesting that a new synthesis of evolution- ary biology might become feasible in a not so remote future. INTRODUCTION Charles Darwin’s book On the Origin of Species that appeared in London in 1859 (1) was the frst plausible, detailed account oF biological evolution ever published, along with the simultaneous and independent brieF out- lines by Darwin and AlFred Russell Wallace published the previous year (2–3). OF course, Darwin did not dis- cover evolution and did not even o±er the frst 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. However, Lamarck’s picture oF evolution was based on an innate drive oF evolving organisms toward perFection, an idea that cannot be acceptable to a rationalist mind. Besides, Lamarck did not proclaim the universal character oF evolution: he postulated multi- ple acts oF creation, apparently, one For each species. Darwin was the frst to present a rational, mechanistic, and arguably, magnifcent picture oF the origin oF the entire diversity oF liFe Forms ‘From so simple a beginning’, probably, From a single common ancestor (1). Darwin’s vision oF the evolution oF liFe was sufficiently complete and powerFul to win over or, at least, deeply a±ect the minds oF
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Article - Darwinian evolution in the light of genomics -...

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