Physiology is rocking the foundations of evolutionary biology
Denis Noble
Article first published online: 17 MAY 2013
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In this article, I will show that all the central assumptions of the Modern Synthesis (often also called Neo-Darwinism) have been disproved.
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Summary of the Modern Synthesis
The central assumptions of the Modern Synthesis that are relevant to this article are fourfold (see also the summary by
Koonin, 2011).
First, genetic change is random.
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Second, genetic change is gradual. Since random events are best thought of as arising from microscopic stochasticity, it will generally be the case that many such events would have to accumulate to generate a major change in genome and phenotype.
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Third, following genetic change, natural selection leads to particular gene variants (alleles) increasing in frequency within the population.
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Fourth, the inheritance of acquired characteristics is impossible.
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All these assumptions have been disproved in various ways and to varying degrees, and it is also important to note that a substantial proportion of the experimental work that has revealed these breaks has come from within molecular biology itself. Molecular biology can now be seen to have systematically deconstructed its own dogmas.
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Are mutations random?
All careful studies of mutagenesis find statistically significant non-random patterns of change, and genome sequence studies confirm distinct biases in location of different mobile genetic elements’
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Is genetic change gradual?
It was the Nobel Prize-winner Barbara McClintock who introduced the idea that the genome is ‘an organ of the cell’ (McClintock, 1984). She won her prize for physiology or medicine in 1983 over 40 years after she had made the ground-breaking discovery of chromosome transposition (now called mobile genetic elements).
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Nature 2001 report (International Human Genome Mapping Consortium, 2001) compared protein-template regions for several classes of proteins from yeast, nematode worms, Drosophila, mice and humans. In the case of transcription factors (Figure 45 of the Nature report) and chromatin-binding proteins (Figure 42 of the Nature report)
the evidence shows that whole domains up to hundreds of amino acids in length have been amplified and shifted around among different genetic loci in the genome.
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A genome consists largely of semi-stable genetic elements that may be rearranged or even moved around in the genome thus modifying the information content of DNA.’ The central dogma of the 1950s, as a general principle of biology, has therefore been progressively undermined until it has become useless as support for the Modern Synthesis (Werner, 2005; Mattick, 2007; Shapiro, 2009) or indeed as an accurate description of what happens in cells. As Mattick (2012) says,
‘the belief that the soma and germ line do not communicate is patently incorrect.’
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Horizontal transfer of DNA is ubiquitous in the prokaryote world, but also far from absent amongst eukaryotes (Shapiro, 2011). Other forms of mobile DNA include plasmids, viruses and group II introns, which are all prokaryotic elements. To these we can add group I introns and inteins (Raghavan & Minnick, 2009), multiple classes of transposons (Curcio & Derbyshire, 2003), multiple classes of retrotransposons (Volff & Brosius, 2007) and various forms of genomic DNA derived from reverse transcription (Baertsch et al. 2008).
One of the major developments of Darwin's concept of a ‘tree of life’ is that the analogy should be more that of a ‘network of life’ (Doolittle, 1999; Woese & Goldenfeld, 2009). As with other breaks from the Modern Synthesis, that synthesis emerges as only part of the evolutionary story.
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The inheritance of acquired characteristics
In 1998, the great contributor to the development of the Modern Synthesis, John Maynard Smith, made a very significant and even prophetic admission when he wrote ‘it [Lamarckism] is not so obviously false as is sometimes made out’ (Maynard Smith, 1998), a statement that is all the more important from being made by someone working within the Modern Synthesis framework.
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So why, given his extraordinary (but completely correct) admission, did Maynard Smith not revise his view of the mechanisms of evolution? The reason he gave in 1999 was that ‘it is hard to conceive of a mechanism whereby it could occur; this is a problem’ (Maynard Smith, 1999).
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But the evidence for the inheritance of acquired characteristics has now moved right into the zoological domain. All the remaining examples I shall quote here are on multicellular organisms, including mammals, and they refer to pioneering work done in the last 7 years.
Anway et al. (2006a,b) demonstrated that an endocrine disruptor, vinclozolin (an anti-androgenic compound), can induce transgenerational disease states or abnormalities that are inherited for at least four generations in rats.
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An alternative approach to determining how the organism as a whole may influence the genome and whether such influences can be transmitted transgenerationally is to study cross-species clones, e.g. by inserting the nucleus of one species into the fertilized but enucleated egg cell of another species. Following the gene-centric view of the Modern Synthesis, the result should be an organism determined by the species from which the genome was taken. In the great majority of cases, this does not happen. Incompatibility between the egg cytoplasm and the transferred nuclear genome usually results in development freezing or completely failing at an early stage. That fact already tells us how important the egg cell expression patterns are. The genome does not succeed in completely dictating development regardless of the cytoplasmic state. Moreover, in the only case where this process has resulted in a full adult, the results also do not support the prediction.
Sun et al. (2005) performed this experiment using the nucleus of a carp inserted into the fertilized but enucleated egg cell of a goldfish. The adult has some of the characteristics of the goldfish. In particular, the number of vertebrae is closer to that of the goldfish than to that of a carp.
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Epigenetic effects can even be transmitted independently of the germ line. Weaver and co-workers showed this phenomenon
in rat colonies, where stroking and licking behaviour by adults towards their young results in epigenetic marking of the relevant genes in the hippocampus that predispose the young to showing the same behaviour when they become adults (Weaver et al. 2004; Weaver, 2009).
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Molecular mechanisms
The results I have described so far establish the existence of transgenerational non-Mendelian inheritance. This section describes recent studies that demonstrate the molecular biological mechanisms and that the transmission can be robust for many generations.
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Rechavi et al. (2011) worked on Caenorhabditis elegans and the non-Mendelian inheritance of the worm's response to viral infection. This is achieved by the infection inducing the formation of an RNA silencer. They crossed worms with this response with worms that do not have it and followed the generations until they obtained worms that did not have the DNA required to produce the silencing RNA but which nevertheless had inherited the acquired resistance.
The mechanism is that transmission of RNA occurs through the germ line and is then amplified by using RNA polymerase. The inheritance of the acquired characteristic is robust for over 100 generations.
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