Transgenerational epigenetic effects on animal behaviour

Abstract

Over the last decade a shift in paradigm has occurred with respect to the interaction between environment and genes. It is now clear that animal genomes are regulated to a large extent as a result of input from environmental events and experiences, which cause short-and long-term modifications in epigenetic markings of DNA and histones. In this review, the evidence that such epigenetic modifications can affect the behaviour of animals is explored, and whether such acquired behaviour alterations can transfer across generation borders. First, the mechanisms by which experiences cause epigenetic modifications are examined.This includes, for example, methylation of cytosine in CpG-positions and acetylation of histones, and studies showing that this can be modified by early experiences. Secondly, the evidence that specific modifications in the epigenome can be the cause of behaviour variation is reviewed. Thirdly, the extent to which this phenotypically active epigenetic variants can be inherited either through the germline or through reoccurring environmental conditions is examined. A particularly interesting observation is that epigenetic modifications are often linked to stress, and may possibly be mediated by steroid effects. Finally, the idea that transgenerationally stable epigenetic variants may serve as substrates for natural selection is explored, and it is speculated that they may even predispose for directed, non-random mutations.3

Evidence from pyrosequencing indicates that natural variation in animal personality is associated with DRD4 DNA methylation

“…Personality traits typically show long-term consistency within individuals, still there is adaptive significance in a considerable degree of plasticity in response to early developmental conditions (Groothuis & Trillmich 2011). A popular idea is that through environmental effects on DNA methylation, behavioural phenotypes can be controlled in concert with environmental demands (Kappeler & Meaney 2010;Jensen 2013), and may be effectuated via maternal effects, via for example maternal hormones, during embryonic development. The case of DRD4 in great tits, whose methylation may be partly under trans-genetic control, may offer an opportunity to investigate whether and how genetic and environmental control of DRD4 methylation may be balanced to jointly determine the behavioural phenotype.…”

Adding ‘epi-’ to behaviour genetics: implications for animal domestication

“…I have elaborated in detail on these aspects in previous reviews (Jensen, 2013;Jensen, 2014), and will expand on some of the aspects in the rest of this paper as well, but, mostly, it appears that all these processes do in fact occur: epigenomes respond in a nonrandom, often adaptive way to environmental signals, they cause behavioural changes and they are often inherited. This means that the interaction between the genome and the environment is far more dynamic and complex than previously thought and our view on domestication and evolution may have to be rather drastically revised.…”

Definition of Epigenetic Transgenerational Inheritance and Biological Impacts

“…The information available can now be used to design more efficient studies to determine the environmental hazards of these exposures. A number of other laboratories have now shown transgenerational inheritance of disease induced by a variety of environmental factors including nutrition, 34 stress, 35 and other toxicants. 36 Combined observations suggest that epigenetic biomarkers for ancestral exposures and adult-onset disease exist and require future investigation.…”