Transmission of Stress-Induced Learning Impairment and Associated Brain Gene Expression from Parents to Offspring in Chickens

Abstract

BackgroundStress influences many aspects of animal behaviour and is a major factor driving populations to adapt to changing living conditions, such as during domestication. Stress can affect offspring through non-genetic mechanisms, but recent research indicates that inherited epigenetic modifications of the genome could possibly also be involved.Methodology/Principal FindingsRed junglefowl (RJF, ancestors of modern chickens) and domesticated White Leghorn (WL) chickens were raised in a stressful environment (unpredictable light-dark rhythm) and control animals in similar pens, but on a 12/12 h light-dark rhythm. WL in both treatments had poorer spatial learning ability than RJF, and in both populations, stress caused a reduced ability to solve a spatial learning task. Offspring of stressed WL, but not RJF, raised without parental contact, had a reduced spatial learning ability compared to offspring of non-stressed animals in a similar test as that used for their parents. Offspring of stressed WL were also more competitive and grew faster than offspring of non-stressed parents. Using a whole-genome cDNA microarray, we found that in WL, the same changes in hypothalamic gene expression profile caused by stress in the parents were also found in the offspring. In offspring of stressed WL, at least 31 genes were up- or down-regulated in the hypothalamus and pituitary compared to offspring of non-stressed parents.Conclusions/SignificanceOur results suggest that, in WL the gene expression response to stress, as well as some behavioural stress responses, were transmitted across generations. The ability to transmit epigenetic information and behaviour modifications between generations may therefore have been favoured by domestication. The mechanisms involved remain to be investigated; epigenetic modifications could either have been inherited or acquired de novo in the specific egg environment. In both cases, this would offer a novel explanation to rapid evolutionary adaptation of a population.

Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution

“…We also excluded a similar case in mice which showed that tumor risk was increased following chromium III chloride exposure and that this risk was then transmitted from father to son (Shiao et al 2005). Other cases of single-generation inheritance, such as protection against type I diabetes in humans (where a paramutation-like process has been reported) (Bennett et al 1997), hydrostatic pressure-induced alterations in DNA methylation in Japonica rice (Long et al 2006), and parallel alterations in gene expression profiles in White Leghorn chickens and their offspring following stress in the parental generation (Lindqvist et al 2007), were also excluded, although epigenetic inheritance may well have occurred and may be revealed when subsequent generations are studied. However, within the limitations imposed by the research designs of the studies we reviewed and the qualifications we have mentioned, we believe that the table provides a fairly exhaustive overview of the recognized cases of cellular transgenerational epigenetic inheritance that have been described in English-language journals, although, inevitably, we likely missed some cases.…”

Observational field studies reveal wild birds responding to early-life stresses with resilience, plasticity, and intergenerational effects

“…Although seldom sought, these have been documented in diverse taxa (Burton and Metcalfe 2014), including 4 species of birds. Application of experimental stresses to captive nestlings or juveniles induced deficits in their offspring: diminished size, hatching success, and nest success in female Zebra Finches (Naguib and Gil 2005, Naguib et al 2006, Alonso-Alvarez et al 2007); reduced spatial learning or corticosterone responsiveness in breeds of Domestic Fowl (Lindqvist et al 2007, Goerlich et al 2012; and increased fearfulness in Japanese Quail (Guibert et al 2012). In nature, however, intergenerational effects are unlikely to be just a matter of imposed deficits and, on present evidence, sometimes reflect adaptive plasticity.…”

“…In nature, however, intergenerational effects are unlikely to be just a matter of imposed deficits and, on present evidence, sometimes reflect adaptive plasticity. A hint of such potential comes from the offspring of white leghorn chicks exposed to unpredictable light-dark rhythms (Lindqvist et al 2007) which, despite their poor spatial learning, were more competitive and grew faster than controls. More persuasive, perhaps, are the 2 intergenerational effects so far observed in free-living birds that can be interpreted as strategic deferral of costs or compensatory adjustment for them.…”

Transgenerational epigenetic effects on animal behaviour

“…A corresponding transgenerational effect of early maternal separation has also been found in female mice (Weiss, Franklin, & Vizi, 2011). My group has demonstrated transgenerational, epigenetically mediated changes in behaviour in chickens as a result of both chronic stress (Lindqvist et al, 2007) and brief events of early social isolation (Goerlich, Nätt, Elfwing, Macdonald, & Jensen, 2012). Also "positive" experiences may transmit across generations.…”

“…Most of the studies referred to here have not examined the possible epigenetic mechanisms involved, even though it appears evident that such mechanisms must play an important role. For example, although the exact mechanisms are unknown, my group has shown that stress induced modifications in hypothalamic gene expression profiles are significantly mirrored in the offspring of the affected animals (Goerlich et al, 2012;Lindqvist et al, 2007;Nätt et al, 2009). …”