“Transgeneration Effects of Social Environment on Variations in Maternal Care and Behavioral Response to Novelty

Columbia University, Department of Psychology, New York, NY 10027, USA.
Behavioral Neuroscience (Impact Factor: 2.73). 04/2008; 121(6):1353-63. DOI: 10.1037/0735-7044.121.6.1353
Source: PubMed


Cross-fostering studies in the rat have illustrated the importance of the postnatal environment in mediating the transmission of maternal licking/grooming (LG) from mother to offspring. The authors addressed the question of how postweaning social conditions can alter the patterns of maternal behavior. Juvenile female offspring of high LG and low LG mothers were placed in either standard, enriched, or impoverished postweaning environments for 50 consecutive days and then mated and observed with their own litters. Analysis of LG behavior indicated that the effect of postweaning environment was dependent on the level of postnatal mother-infant interaction. Postweaning isolation reduced exploratory behavior, maternal LG, and oxytocin receptor binding in the offspring of high LG mothers, whereas social enrichment enhanced exploration, LG behavior, and oxytocin receptor binding of low LG offspring. These effects were also transmitted to the next generation of offspring. Thus, maternal LG and the neural mechanisms that regulate this behavior exhibited a high degree of plasticity in response to changes in environment both within and beyond the postnatal period, with implications for the transmission of behavioral response to novelty and maternal care across generations.

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    • "Although the machinery of empathy for recognizing distress may be genetically transmitted, the behavior of consoling others may possibly be culturally transmitted. For example, maternal behavior is often influenced by the early experience of being cared for by the mother and observing the maternal behaviors of others (Gonzalez et al. 2001; Champagne and Meaney 2007), although in mammals mothers may also take care of their offspring through instinct. In other words, consolation behavior may remain in the population even when consolation is costly because the behaviors of empathetic consolers are more likely to be transmitted culturally. "
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    Learning Strategies and Cultural Evolution during the Palaeolithic, Edited by Alex Mesoudi, Kenichi Aoki, 05/2015: chapter 3: pages 23-33; Springer Japan., ISBN: 978-4-431-55362-5
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    • "Phenotypic modifications can be transmitted across generations through various mechanisms like parental behavior, transfer of physical substances, hormonal effects that influence gene expression, or epigenetic inheritance of environmental variation (West-Eberhard 2003; Jablonka and Lamb 2005; Badyaev 2005; Champagne and Meaney 2007). Parental behavior during the lactation period is rather unlikely to have caused the observed differences in phenotypes and reproductive strategy in this study because guinea pig young are born in a state of advanced maturation. "
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    ABSTRACT: The prenatal social environment affects offspring development in most studied taxa with potentially lifelong consequences. To understand the adaptive significance of such maternal influences on offspring development, it is important to study their effects on fitness. In guinea pigs, social instability during pregnancy leads to delayed development of male offspring. This has been interpreted as an adaptation to high social densities, where young males need to queue for reproductive opportunities since they cannot out-compete older dominant males. The consequences for male reproductive success are, however, so far unknown. To study the effects of different prenatal social densities on offspring reproductive performance, we housed females individually or in small groups during late pregnancy. Offspring from both treatments were reared together in large groups until independence and thereafter housed in same-sex pairs of the same treatment. We then observed courtship, aggressive behavior, and reproductive success in a low-density context with one male from each treatment competing over access to two females. Sons born to individually housed females initiated more fights, had more social contacts, courted females more, and had a higher reproductive success than sons of group-housed females. Sons born to mothers experiencing low social densities before birth therefore perform better at low social group sizes, suggesting that male development may be adaptively adjusted to anticipated social densities, although performance under high densities still needs to be compared.
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    • "Recent data also demonstrate that non-gametic inheritance occurs via parental hormones, immune molecules and even microorganisms (Howerton and Bale, 2012) (Fig. 1). Still other non-gametic mechanisms of inheritance are social or behavioral transmission of phenotypes, a topic extensively covered in previous reviews (Meaney, 2001; Champagne and Meaney, 2007; Cameron et al., 2008), as well as in this issue (xxxx). "
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    ABSTRACT: Inheritance is typically associated with the Mendelian transmission of information from parents to offspring by alleles (DNA sequence). However, empirical data clearly suggest that traits can be acquired from ancestors by mechanisms that do not involve genetic alleles, referred to as non-genetic-inheritance. Information that is non-genetically transmitted across generations includes parental experience and exposure to certain environments, but also parental mutations and polymorphisms, because they can change the parental "intrinsic' environment. Non-genetic inheritance is not limited to the first generation of the progeny, but can involve the grandchildren and even further generations. Non-genetic inheritance has been observed for multiple traits including overall development, cardiovascular risk and metabolic symptoms, but this review will focus on inheritance of behavioral abnormalities pertinent to psychiatric disorders. Multigenerational non-genetic inheritance is often interpreted as the transmission of epigenetic marks, such as DNA methylation and chromatin modifications, via the gametes (transgenerational epigenetic inheritance). However, information can be carried across generations by a large number of bioactive substances, including hormones, cytokines and even microorganisms, without the involvement of the gametes. We reason that this broader definition of non-genetic inheritance is more appropriate, especially in the context of psychiatric disorders, because of the well-recognized role of parental and early life environmental factors in later life psychopathology. Here we discuss the various forms of non-genetic inheritance in human and animals, as well as rodent models of psychiatric conditions to illustrate possible mechanisms.Neuropsychopharmacology Reviews accepted article preview online, 03 June 2014; doi:10.1038/npp.2014.127.
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