Literature DB >> 25232132

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

Katie E McGhee1, Alison M Bell2.   

Abstract

In many animals, including humans, interactions with caring parents can have long-lasting effects on offspring sensitivity to stressors. However, whether these parental effects impact offspring fitness in nature is often unclear. In addition, despite evidence that maternal care can influence offspring behaviour via epigenetic alterations to the genome, it remains unclear whether paternal care has similar effects. Here, we show in three-spined sticklebacks, a fish in which fathers are the sole provider of offspring care, that the direct care provided by fathers affects offspring anxiety and the potential for epigenetic alterations to the offspring genome. We find that families are differentially vulnerable to early stress and fathers can compensate for this differential sensitivity with the quality of their care. This variation in paternal care is also linked to the expression in offspring brains of a DNA methyltransferase (Dnmt3a) responsible for de novo methylation. We show that these paternal effects are potentially adaptive and anxious offspring are unlikely to survive an encounter with a predator. By supplying offspring care, fathers reduce offspring anxiety thereby increasing the survival of their offspring-not in the traditional sense through resource provisioning but through an epigenetic effect on offspring behavioural development.
© 2014 The Author(s) Published by the Royal Society. All rights reserved.

Entities:  

Keywords:  behavioural programming; early life stress; methylation; survival; three-spined stickleback; transgenerational plasticity

Mesh:

Substances:

Year:  2014        PMID: 25232132      PMCID: PMC4211443          DOI: 10.1098/rspb.2014.1146

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


  27 in total

1.  Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks.

Authors:  Genevieve M Kozak; Megan L Head; Janette W Boughman
Journal:  Proc Biol Sci       Date:  2011-01-26       Impact factor: 5.349

Review 2.  Epigenetics and the origins of paternal effects.

Authors:  James P Curley; Rahia Mashoodh; Frances A Champagne
Journal:  Horm Behav       Date:  2010-07-08       Impact factor: 3.587

3.  Paternal social enrichment effects on maternal behavior and offspring growth.

Authors:  Rahia Mashoodh; Becca Franks; James P Curley; Frances A Champagne
Journal:  Proc Natl Acad Sci U S A       Date:  2012-10-08       Impact factor: 11.205

Review 4.  The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome.

Authors:  Nikolaos P Daskalakis; Rosemary C Bagot; Karen J Parker; Christiaan H Vinkers; E R de Kloet
Journal:  Psychoneuroendocrinology       Date:  2013-07-07       Impact factor: 4.905

5.  Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons.

Authors:  Jian Feng; Yu Zhou; Susan L Campbell; Thuc Le; En Li; J David Sweatt; Alcino J Silva; Guoping Fan
Journal:  Nat Neurosci       Date:  2010-03-14       Impact factor: 24.884

Review 6.  Modeling anxiety using adult zebrafish: a conceptual review.

Authors:  Adam Stewart; Siddharth Gaikwad; Evan Kyzar; Jeremy Green; Andrew Roth; Allan V Kalueff
Journal:  Neuropharmacology       Date:  2011-08-09       Impact factor: 5.250

Review 7.  Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans.

Authors:  Tie Yuan Zhang; Benoit Labonté; Xiang Lan Wen; Gustavo Turecki; Michael J Meaney
Journal:  Neuropsychopharmacology       Date:  2012-09-12       Impact factor: 7.853

8.  Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback.

Authors:  Katie E McGhee; Lauren M Pintor; Elissa L Suhr; Alison M Bell
Journal:  Funct Ecol       Date:  2012-06-21       Impact factor: 5.608

9.  Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles.

Authors:  Rui Jia; Fadao Tai; Shucheng An; Xia Zhang; Hugh Broders
Journal:  Behav Processes       Date:  2009-07-25       Impact factor: 1.777

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

Authors:  Erin D Gleason; Catherine A Marler
Journal:  Proc Biol Sci       Date:  2013-05-22       Impact factor: 5.349

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  19 in total

Review 1.  Compassion: From Its Evolution to a Psychotherapy.

Authors:  Paul Gilbert
Journal:  Front Psychol       Date:  2020-12-09

2.  The role of variation and plasticity in parental care during the adaptive radiation of three-spine sticklebacks.

Authors:  Laura R Stein; Alison M Bell
Journal:  Evolution       Date:  2019-03-25       Impact factor: 3.694

3.  A female's past experience with predators affects male courtship and the care her offspring will receive from their father.

Authors:  Katie E McGhee; Sally Feng; Sagan Leasure; Alison M Bell
Journal:  Proc Biol Sci       Date:  2015-11-22       Impact factor: 5.349

Review 4.  Creating a Compassionate World: Addressing the Conflicts Between Sharing and Caring Versus Controlling and Holding Evolved Strategies.

Authors:  Paul Gilbert
Journal:  Front Psychol       Date:  2021-02-10

5.  Integrating Ecological and Evolutionary Context in the Study of Maternal Stress.

Authors:  Michael J Sheriff; Alison Bell; Rudy Boonstra; Ben Dantzer; Sophia G Lavergne; Katie E McGhee; Kirsty J MacLeod; Laurane Winandy; Cedric Zimmer; Oliver P Love
Journal:  Integr Comp Biol       Date:  2017-09-01       Impact factor: 3.326

6.  Looking back and moving forward: Evaluating and advancing translation from animal models to human studies of early life stress and DNA methylation.

Authors:  Sarah Enos Watamura; Tania L Roth
Journal:  Dev Psychobiol       Date:  2018-11-13       Impact factor: 3.038

7.  Effects of mothers' and fathers' experience with predation risk on the behavioral development of their offspring in threespined sticklebacks.

Authors:  Alison M Bell; Katie E McGhee; Laura Stein
Journal:  Curr Opin Behav Sci       Date:  2016-02-01

8.  Larval environmental conditions influence plasticity in resource use by adults in the burying beetle, Nicrophorus vespilloides.

Authors:  Matthew Schrader; Benjamin J M Jarrett; Rebecca M Kilner
Journal:  Evolution       Date:  2021-09-08       Impact factor: 4.171

Review 9.  Don't worry; be informed about the epigenetics of anxiety.

Authors:  Steven J Nieto; Michelle A Patriquin; David A Nielsen; Therese A Kosten
Journal:  Pharmacol Biochem Behav       Date:  2016-05-14       Impact factor: 3.533

Review 10.  Threespine Stickleback: A Model System For Evolutionary Genomics.

Authors:  Kerry Reid; Michael A Bell; Krishna R Veeramah
Journal:  Annu Rev Genomics Hum Genet       Date:  2021-04-28       Impact factor: 9.340

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