Literature DB >> 23698012

Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse.

Erin D Gleason1, Catherine A Marler.   

Abstract

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.

Entities:  

Keywords:  Peromyscus; biparental; epigenetic; monogamous; paternal; testosterone

Mesh:

Substances:

Year:  2013        PMID: 23698012      PMCID: PMC4043185          DOI: 10.1098/rspb.2013.0824

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  31 in total

1.  Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area.

Authors:  Frances A Champagne; Ian C G Weaver; Josie Diorio; Shakti Sharma; Michael J Meaney
Journal:  Endocrinology       Date:  2003-07-24       Impact factor: 4.736

2.  Variations in maternal care in the rat as a mediating influence for the effects of environment on development.

Authors:  Frances A Champagne; Darlene D Francis; Adam Mar; Michael J Meaney
Journal:  Physiol Behav       Date:  2003-08

3.  Sexual selection and the potential reproductive rates of males and females.

Authors:  T H Clutton-Brock; A C Vincent
Journal:  Nature       Date:  1991-05-02       Impact factor: 49.962

4.  Nongenomic transmission across generations of maternal behavior and stress responses in the rat.

Authors:  D Francis; J Diorio; D Liu; M J Meaney
Journal:  Science       Date:  1999-11-05       Impact factor: 47.728

5.  Vasopressin and aggression in cross-fostered California mice (Peromyscus californicus) and white-footed mice (Peromyscus leucopus).

Authors:  J K Bester-Meredith; C A Marler
Journal:  Horm Behav       Date:  2001-08       Impact factor: 3.587

6.  Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen.

Authors:  Brian C Trainor; Catherine A Marler
Journal:  Proc Biol Sci       Date:  2002-04-22       Impact factor: 5.349

7.  Early experience and cross-generational continuity of mother-infant contact in vervet monkeys.

Authors:  L A Fairbanks
Journal:  Dev Psychobiol       Date:  1989-11       Impact factor: 3.038

8.  Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior.

Authors:  Brian C Trainor; Ian M Bird; Noel A Alday; Barney A Schlinger; Catherine A Marler
Journal:  Neuroendocrinology       Date:  2003-07       Impact factor: 4.914

Review 9.  Plasticity and functions of the orbital frontal cortex.

Authors:  Bryan Kolb; Sergio Pellis; Terry E Robinson
Journal:  Brain Cogn       Date:  2004-06       Impact factor: 2.310

10.  Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice.

Authors:  Janet K Bester-Meredith; Catherine A Marler
Journal:  Behav Neurosci       Date:  2003-06       Impact factor: 1.912

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  11 in total

Review 1.  Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation.

Authors:  Wendy Saltzman; Breanna N Harris; Trynke R De Jong; Juan P Perea-Rodriguez; Nathan D Horrell; Meng Zhao; Jacob R Andrew
Journal:  Integr Comp Biol       Date:  2017-09-01       Impact factor: 3.326

Review 2.  The biology of mammalian parenting and its effect on offspring social development.

Authors:  James K Rilling; Larry J Young
Journal:  Science       Date:  2014-08-14       Impact factor: 47.728

3.  Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety.

Authors:  Katie E McGhee; Alison M Bell
Journal:  Proc Biol Sci       Date:  2014-11-07       Impact factor: 5.349

Review 4.  Early-life experience, epigenetics, and the developing brain.

Authors:  Marija Kundakovic; Frances A Champagne
Journal:  Neuropsychopharmacology       Date:  2014-06-11       Impact factor: 7.853

5.  Sensitive phases in the development of rodent social behavior.

Authors:  Norbert Sachser; Tobias D Zimmermann; Michael B Hennessy; Sylvia Kaiser
Journal:  Curr Opin Behav Sci       Date:  2020-08-26

6.  Chronic variable stress in fathers alters paternal and social behavior but not pup development in the biparental California mouse (Peromyscus californicus).

Authors:  Breanna N Harris; Trynke R de Jong; Vanessa Yang; Wendy Saltzman
Journal:  Horm Behav       Date:  2013-10-22       Impact factor: 3.587

Review 7.  Fathering in rodents: Neurobiological substrates and consequences for offspring.

Authors:  Karen L Bales; Wendy Saltzman
Journal:  Horm Behav       Date:  2015-06-26       Impact factor: 3.587

Review 8.  Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species.

Authors:  Allison M Perkeybile; Karen L Bales
Journal:  J Exp Biol       Date:  2017-01-01       Impact factor: 3.312

9.  Intergenerational transmission of alloparental behavior and oxytocin and vasopressin receptor distribution in the prairie vole.

Authors:  Allison M Perkeybile; Nathanial Delaney-Busch; Sarah Hartman; Kevin J Grimm; Karen L Bales
Journal:  Front Behav Neurosci       Date:  2015-07-23       Impact factor: 3.558

10.  Interactions between parents and parents and pups in the monogamous California mouse (Peromyscus californicus).

Authors:  Cheryl S Rosenfeld; Sarah A Johnson; Mark R Ellersieck; R Michael Roberts
Journal:  PLoS One       Date:  2013-09-19       Impact factor: 3.240

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