A striking example of epigenetic adaptation first reported in 2014 has recently been shown to involve ncRNA1. This work was based on an experimental system in which mice are conditioned to associate an odour with an irritation, a mild electric shock. Short periods of repeated delivery of a distinctive chemical smell followed by a shock resulted in the mice exhibiting anxiety when they smell the odour, even when no shock is administered. The conditioning was very specific for the actual odours being used, rather than exposure to odours in general; mice conditioned with one odour did not become anxious when exposed to another. This experimental system enabled a test of whether such environmentally induced behavioural changes can be inherited. The result was positive; when, subsequent to the conditioning process, conditioned mice were mated, two generations of progeny exhibited the same anxiety response to specific odour seen in their parents.
Not only that, but the inherited phenotype involved morphological changes to odour detection organs. Odour detection involves tissues in the nose and brain that have channels specific for different types of odour. The number and size of anatomical structures comprising the olfactory channel known to detect the conditioning odour used were increased in the affected progeny. The conditioned mice therefore pass to their offspring a state of preparedness for an environmental condition they have encountered. That preparedness comprises two linked but separate phenotypic components: the sensory one and the neurological one controlling and enabling the behavioural (i.e. the anxiety) response.
These observations show that animals can inherit altered behaviour when their recent ancestors experience adverse environmental conditions. It is easy to see that such transgenerationally transmitted behavioural change could be beneficial, increasing survival prospects when there is environmental threat. This research has therefore shown that environmentally induced behavioural change may have evolutionary potential. (It may also hold clues to the biological origins of instinct.)
”This environmentally induced behavioural change is therefore transmitted transgenerationally by RNA in sperm of affected mice.”
The same research group has recently followed up their demonstration of this adaptive epigenetic process with experiments indicating that it has an RNA based mechanism2. They did this by extracting RNA from sperm obtained from conditioned male mice then injecting it into single cell embryos taken from unconditioned females that had been mated with unconditioned males. The only link of these embryos to conditioning was therefore the RNA with which they had been injected, but that was enough; when they became adult the injected embryos showed the odour linked anxiety response and the morphological enhancement of odour detection organs observed previously in progeny of conditioned parents.
This environmentally induced behavioural change is therefore transmitted transgenerationally by RNA in sperm of affected mice. (Note that there is reason to think that this mechanism may not be the only one, but the possibility of other epigenetic mechanisms doesn’t affect the argument.) The research group has not, to date, shown how this phenotype transforming RNA comes to be in the sperm, but it may well have arisen in the somatic tissues (the odour detection organs and brain networks) that provide the conditioned response. The transfer of functional information from cell to cell and organ to organ is what non-coding RNAs do, and other research has shown them to be present in sperm and to generate biological effects in animals sired by those sperms. This, therefore, may well prove to be an example of adaptive change generated by a soma to germline epigenetic process in direct response to environmental conditions.
Research on this epigenetic process is at an early stage and much still remains to be discovered before the phenomenon is fully understood. Nevertheless, these three examples (the experiments involving liver wounding, tumour cell grafts and odour associated anxiety) collectively show how somatic cells with environmentally induced changes to their phenotypes send information to germ cells, thereby making the new phenotype hereditary.
”These three examples … show how somatic cells with environmentally induced changes to their phenotypes send information to germ cells making new phenotypes hereditary”
The theory of a barrier that restricts information flow and influence to a germline to soma direction, thereby preventing phenotypes from specifying heredity3, has been a barrier to thinking about the interaction between environments and animal evolution. The demonstration of hereditary information passing from somatic cells to germ cells and thence to progeny seriously weakens that theoretical barrier. In doing so it allows a potentially powerful way in which animals can adapt reactively and specifically, rather than only randomly, to environmental difficulty and opportunity.
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References
- Dias, Brian G., and Kerry J. Ressler. ‘Parental Olfactory Experience Influences Behavior and Neural Structure in Subsequent Generations’. Nature Neuroscience 17, no. 1 (January 2014): 89–96. https://doi.org/10.1038/nn.3594 [↩]
- Aoued, Hadj S., Soma Sannigrahi, Sarah C. Hunter, Nandini Doshi, Zakia S. Sathi, Anthony W. S. Chan, Hasse Walum, and Brian G. Dias. ‘Proximate Causes and Consequences of Intergenerational Influences of Salient Sensory Experience’. Genes, Brain, and Behavior 19, no. 4 (April 2020): e12638. https://doi.org/10.1111/gbb.12638 [↩]
- August Weismann. Das Keimplasma: Eine Theorie Der Vererbung. Jena: Fisher, 1892 [↩]
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