Maternal care affects the development of maternal behavior in inbred mice

Shoji, Hirotaka; Kato, Katsunori

doi:10.1002/dev.20375

Cited by 25 publications

(22 citation statements)

References 55 publications

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“…3 Graph illustrating the relationship between litter size and mortality for litters of F1 dams: B6D2 dams (dashed line) and D2B6 dams (solid line). Minor lines display 95% confidence intervals have been passed from mother to daughter by early environmental experience as has been reported for several maternal behaviour traits (Meaney 2001;Carola et al 2006;Shoji and Kato 2009;Curley and Mashoodh 2010). However, instead of being similar to their mothers in terms of offspring mortality rates, the hybrid daughters clearly showed the opposite pattern.…”

Section: Discussionmentioning

confidence: 67%

Genetic and Maternal Effects on Offspring Mortality in Mice

et al. 2011

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Trade-offs occur when two traits have opposing fitness effects such that positive selection on one trait is constrained by the negative fitness consequences of the other trait. To understand why trade-off may arise we need to study the genetic and non-genetic factors that influence associated traits because these may respond differently to selective pressure. Research into trade-offs has largely focused on the genetic basis of associated traits, yet both maternal effects and epigenetic effects have recently been shown to affect life history traits that play a role in tradeoffs. In this study, we analyze genetic, epigenetic and lifehistory predictors of one of the most important trade-offs, that between offspring number and offspring mortality. Using a large-scale 3-generational intercross between two divergent mouse lines C57BL/6J and DBA/2J, we show that litter size differences between these lines, although significant, are surprisingly not the most important predictors of mortality. Offspring genotype, maternal effects and their interactions are the most influential factors determining mortality. We found significant paternal effects suggesting an important influence of paternal care or potentially the role of imprinted genes. Perhaps contrary to expectations our results further show that the trade-off between offspring number and mortality is not just a simple function of the two factors yielding, on average, an 'optimal' litter size at weaning. Indeed if one focused on litter size and mortality alone, the slope of relationship is the same for the two lines, yet they differ in the number of young at weaning. Our study reveals that a perceived tradeoff between two traits is governed by a more complex set of interactions between genetic and non-genetic effects.

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Section: Discussionmentioning

confidence: 67%

Genetic and Maternal Effects on Offspring Mortality in Mice

et al. 2011

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“…This was based upon the knowledge that when mouse pups are cross-fostered to adoptive lactating dams, they are usually well accepted and nurtured [39], and on the fact that an adoption procedure carried out in the first postnatal days has a low impact on offspring's HPA functioning [40].…”

Section: Methodsmentioning

confidence: 99%

Unstable Maternal Environment, Separation Anxiety, and Heightened CO2 Sensitivity Induced by Gene-by-Environment Interplay

et al. 2011

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BackgroundIn man, many different events implying childhood separation from caregivers/unstable parental environment are associated with heightened risk for panic disorder in adulthood. Twin data show that the occurrence of such events in childhood contributes to explaining the covariation between separation anxiety disorder, panic, and the related psychobiological trait of CO2 hypersensitivity. We hypothesized that early interference with infant-mother interaction could moderate the interspecific trait of response to CO2 through genetic control of sensitivity to the environment.MethodologyHaving spent the first 24 hours after birth with their biological mother, outbred NMRI mice were cross-fostered to adoptive mothers for the following 4 post-natal days. They were successively compared to normally-reared individuals for: number of ultrasonic vocalizations during isolation, respiratory physiology responses to normal air (20%O2), CO2-enriched air (6% CO2), hypoxic air (10%O2), and avoidance of CO2-enriched environments.ResultsCross-fostered pups showed significantly more ultrasonic vocalizations, more pronounced hyperventilatory responses (larger tidal volume and minute volume increments) to CO2-enriched air and heightened aversion towards CO2-enriched environments, than normally-reared individuals. Enhanced tidal volume increment response to 6%CO2 was present at 16–20, and 75–90 postnatal days, implying the trait's stability. Quantitative genetic analyses of unrelated individuals, sibs and half-sibs, showed that the genetic variance for tidal volume increment during 6%CO2 breathing was significantly higher (Bartlett χ = 8.3, p = 0.004) among the cross-fostered than the normally-reared individuals, yielding heritability of 0.37 and 0.21 respectively. These results support a stress-diathesis model whereby the genetic influences underlying the response to 6%CO2 increase their contribution in the presence of an environmental adversity. Maternal grooming/licking behaviour, and corticosterone basal levels were similar among cross-fostered and normally-reared individuals.ConclusionsA mechanism of gene-by-environment interplay connects this form of early perturbation of infant-mother interaction, heightened CO2 sensitivity and anxiety. Some non-inferential physiological measurements can enhance animal models of human neurodevelopmental anxiety disorders.

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“…Behavioral changes have also been observed in hybrids, such as the temperament differences commonly reported between hinnies (donkey mother and horse father) and mules (horse mother and donkey father) (Gray, 1972). In the laboratory, the reciprocal breeding of various inbred and outbred rodent strains and species has been extremely useful in screening for parent-of-origin effects on behavioral and physiological phenotypes such as emotional reactivity (Calatayud & Belzung, 2001;Carola, Frazzetto, & Gross, 2006;Roy, Merali, Poulter, & Anisman, 2007), maternal care (Calatayud, Coubard, & Belzung, 2004;Carola et al, 2008;Shoji & Kato, 2009), infanticide (Perrigo et al, 1993), aggression (Carlier, Roubertoux, & Pastoret, 1991;Platt & Maxson, 1989), sex (McGill & Manning, 1976), forced ethanol intake (Gabriel & Cunningham, 2008), calcium taste preference (Tordoff, Reed, & Shao, 2008), activity (Dohm, Richardson, & Garland, 1994;Massett & Berk, 2005;Price & Loomis, 1973), cerebellar development (Cooper, Benno, Hahn, & Hewitt, 1991), peripheral nerve conductivity (Hegmann & White, 1973), central estrogen receptor a distribution (Kramer, Carr, Schmidt, & Cushing, 2006), and puberty onset (Zhou et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Parent‐of‐origin and trans‐generational germline influences on behavioral development: The interacting roles of mothers, fathers, and grandparents

Curley

Mashoodh

2010

Developmental Psychobiology

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Mothers and fathers do not contribute equally to the development of their offspring. In addition to the differential investment of mothers versus fathers in the rearing of offspring, there are also a number of germline factors that are transmitted unequally from one parent or the other that contribute significantly to offspring development. This article shall review four major sources of such parent-of-origin effects. Firstly, there is increasing evidence that genes inherited on the sex chromosomes including the nonpseudoautosomal part of the Y chromosome that is only inherited from fathers to sons, contribute to brain development and behavior independently of the organizing effects of sex hormones. Secondly, recent work has demonstrated that mitochondrial DNA that is primarily inherited only from mothers may play a much greater than anticipated role in neurobehavioral development. Thirdly, there exists a class of genes known as imprinted genes that are epigenetically silenced when passed on in a parent-of-origin specific manner and have been shown to regulate brain development and a variety of behaviors. Finally, there is converging evidence from several disciplines that environmental variations experienced by mothers and fathers may lead to plasticity in the development and behavior of offspring and that this phenotypic inheritance can be solely transmitted through the germline. Mechanistically, this may be achieved through altered programming within germ cells of the epigenetic status of particular genes such as retrotransposons and imprinted genes or potentially through altered expression of RNAs within gametes.

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Maternal care affects the development of maternal behavior in inbred mice

Cited by 25 publications

References 55 publications

Genetic and Maternal Effects on Offspring Mortality in Mice

Genetic and Maternal Effects on Offspring Mortality in Mice

Unstable Maternal Environment, Separation Anxiety, and Heightened CO2 Sensitivity Induced by Gene-by-Environment Interplay

Parent‐of‐origin and trans‐generational germline influences on behavioral development: The interacting roles of mothers, fathers, and grandparents

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