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. 2011 Sep 1;4(5):521–523. doi: 10.4161/cib.4.5.17702

Evolution in Revolution

A Paradigm shift in our understanding of life and biological evolution

František Baluška 1,✉
PMCID: PMC3204118

Abstract

Biological evolution represents one of the most successful, but also controversial scientific concepts. Ever since Charles Darwin formulated his version of evolution via natural selection, biological sciences experienced explosive development and progress. First of all, although Darwin could not explain how traits of organisms, selected via natural selection, are inherited and passed down along generations; his theory stimulated research in this respect and resulted in the establishment of genetics and still later in the discovery of DNA and genome sequencing some hundred years after his evolutionary theory. Nevertheless, there are several weaknesses in classical Darwinian as well as Neodarwinian gene-centric views of biological evolution. The most serious drawback is its narrow focus: the modern evolutionary synthesis, as formulated in the 20th Century, is based on the concept of gene and on the mathematical/statistical analysis of populations. While Neodarwinism is still generally considered a valid theory of biological evolution, its narrow focus and incompatibility with several new findings and discoveries calls for its update and/or transformation. Either it will be replaced with an updated version or, if not flexible enough, it will be replaced by a new theory. In his book “Evolution — A New View from the 21st Century,”1 James A. Shapiro discusses these problems as well as newly emerging results which are changing our understanding of biological evolution. This new book joins a row of several other recent books highlighting the same issues.2–13

You say you want a revolution
Well, you know
We all want to change the world
You tell me that it's evolution
Well, you know
We all want to change the world
(Revolution 1, The Beatles 1968)

Shapiro's book starts with characterization of cells relying on sensing and signaling for their cognitive life-or-death decisions in response to environmental stress and for their responses to diverse developmental cues and signals. He is stating clearly that all cells, even prokaryotic ones, rely heavily on sensing and decision-making processes in order to survive and reproduce faithfully in ever changing environment. Shapiro concludes that each cell has to make many signal-dependent life-or-death decisions requiring cognitive abilities. This cognitive view of cells, based on their sensory systems and information processing apparatus, changes our understanding of life and requires radical reformulation of the central dogma of molecular biology.1 The Cartesian dualist's view of molecular information transfer, as proposed by Francis Crick, is not able to cope anymore with numerous situations when organisms, ranging from bacteria and protozoa up to higher plants and animals project their sensory and stress experiences on their genomes and epigenomes via their cytoskeleton, endomembranes and integrated information-processing networks.1,10,14–26

There are problems with several concepts on which the Neodarwinistic version of Darwinian evolution relies. First of all, the concept of gene loses its rigorous well-defined status. Instead of the gene, it is necessary to speak about coding sequences which are intermixed with non-coding sequences.1,14,15 Most DNA sequences in eukaryotic nuclei are in fact non-coding sequences but these are important for genome organization. Moreover, these DNA sequences are not fixed in the genome but have been found to be rather fluid and mobile.21 Barbara McClintock received the Nobel Prize for her discovery of mobile DNA elements activated by genomic stress.27–29 This unexpected twist towards fluid and flexible genome1,30 is closely linked with the sensory/cognitive faculties of cells1,14,20,21,25 as well as of their genomes.26,28,31 Importantly, sensory experiences can modify the epigenome.18,31–34

Furthermore, the concept of species in its classical sense is changing also, and there are several examples of interspecies hybridization in both plants and animals.35–38 It is obvious that the gene and species are rather vague concepts which are in need of redefinition. In evolution, merging and fusion of two distant organisms can happen, as evidenced by the composite nature of eukaryotic cells consisting of several cells and chimeric genomes.39–44 Although not mentioned by Charles Darwin in his original version of the evolution theory, and even not being part of the Neodarwinian view of the biological evolution, symbiosis is an essential part of biological evolution.11,39–44 Mitochondria and plastids are symbiotic cells engulfed by still ill-defined host cells. Even the nucleus appears to have an endosymbiotic origin generated by the merging of two or more ancient organisms.40,45–48

Another mystery is the inherent drive of living and evolving systems to associate, or even merge and produce into the higher levels of biological organization.1,11,41–49 This universal tendency for sociality, which is obvious at all levels of biological organization, suggests the existence of a ‘Biological Attraction’ principle49, the nature of which seems to be inherent for any living systems. This ‘Biological Attraction’ manifests itself as co-evolution, convergent evolution, symbiogenesis, lateral DNA transfer, but also as mimicking and manipulation interactions between organisms at a distance.

Besides the gene and species concepts, recent findings start to question another pillar of Neodarwinism—the random nature of evolutionary relevant mutations. James Shapiro applies his new concepts of the genome as a read-write (RW) storage system and of natural genetic engineering.21,22 Instead of representing a ‘blueprint’ (read-only memory subject to accidental changes in form of mutations), in Shapiro's view the genome acts as an active read-write (RW) storage and information-processing system which copes with diverse stress situations actively via rearrangements of DNA sequences.1,15,20,21,25–30 In order to accomplish this task, the genome is integrated with sensory and information processing neuronal intracellular networks built from proteins which act as computational elements.7,10,50–52 Novelty in evolution is inherently linked to the active and cognitive lifestyle of organisms, which continually updates the genome via natural genome editing mechanisms.1,12,54 Random genetic mutations can happen but do not have a decisive role in driving biological evolution.

In conclusion, James A. Shapiro's “Evolution—A New View from the 21st Century” prepares the ground for the next great synthesis in biological evolution.1 This new synthesis should be able to deal with the inherent tendency of biological systems to increase their complexities at all levels of biological organization (from DNA sequences and single proteins up to multicellular organisms and ecological communities) and to associate/merge into larger assemblies.1,39–44 This 21st century synthesis will include our recent understanding of life as a phenomenon supported by knowledge embodied in sentient chemical systems,51 where biocommunication is inherently linked to life as well as to biological evolution.51–55 Sentience, subjectivity, cognition, communication, and intelligence appear to be inherently associated with both life and biological evolution.1,24,50–53 Finally, the active role of viruses and the whole virosphere in shaping and perhaps driving biological macro-evolution is also emerging.4,9,54–58 After all controversies, perhaps a peaceful co-existence of the Darwinian and Lamarckian evolutionary concepts will be possible59–63 under an umbrella of the 21st century evolutionary synthesis encompassing viral infections,4,9,12,39,54–58 symbiogenesis,39,42–44,64 lateral DNA transfer,64,65 and behavior66–68 as essential evolutionary forces. Darwinian competition, predation, and struggle for life are being complemented with cooperation, communication, cognition, learning and behavior;3,59,66 which are also essential ingredients of biological evolution. This paradigm shift in the sense of Thomas Kuhn69 is also transforming the ‘tree of life’ into the ‘network of life’.70

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