An article in the journal Experimental Physiology by the distinguished British biologist Denis Noble has the provocative title, “Physiology is rocking the foundations of evolutionary biology.” He argues that “[t]he ‘Modern Synthesis’ (Neo-Darwinism) is a mid-20th century gene-centric view of evolution, based on random mutations accumulating to produce gradual change through natural selection” but we now know that view is wrong because “genetic change is far from random and often not gradual.” Regarding the neo-Darwinian viewpoint, Noble doesn’t mince words:
It is not only the standard 20th century views of molecular genetics that are in question. Evolutionary theory itself is already in a state of flux (Jablonka & Lamb, 2005; Noble, 2006, 2011; Beurton et al. 2008; Pigliucci & Muller, 2010; Gissis & Jablonka, 2011; Shapiro, 2011). In this article, I will show that all the central assumptions of the Modern Synthesis (often also called Neo-Darwinism) have been disproved.
Noble then recounts those assumptions: (1) that “genetic change is random,” (2) that “genetic change is gradual,” (3) that “following genetic change, natural selection leads to particular gene variants (alleles) increasing in frequency within the population,” and (4) that “inheritance of acquired characteristics is impossible.” He then cites examples that refute each of those assumptions, focusing specifically on newly discovered examples of inheritance of acquired characteristics. About that last assumption, he notes:
An endocrine disruptor compound can “induce transgenerational disease states or abnormalities that are inherited for at least four generations in rats.” The mechanism is probably “marking of the genome or transmission of RNA” in the germ line.
“A study done in Scandinavia clearly shows the transgenerational effect of food availability to human grandparents influencing the longevity of grandchildren.”
Behaviorally induced, heritable epigenetic changes, such as “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.”
In C. elegans, an infection induced the formation of an RNA silencer that “is robust for over 100 generations.”
Paramutations that are “the interaction between two alleles at a single locus” can “induce permanent epigenetic changes in organisms from maize to mice.”
After reviewing these and other examples, Noble concludes:
The flow of papers during the last 5 years showing non-Mendelian inheritance is, however, now becoming a flood of evidence. … These examples of robust inheritance of acquired characteristics reveal a wide array of mechanisms by which such inheritance can be achieved. Nature seems to work through the cracks, as it were, of the gene-centric view. Those cracks have now been discovered to be great fissures, through which functionally significant inherited changes occur. Such mechanisms could not have been foreseen at the time when the Modern Synthesis was formulated, or even a decade ago. To Maynard Smith’s comment (‘it is hard to conceive of a mechanism whereby it could occur’), the reply must be that some of those mechanisms have now been found and they are robust.