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Title: Intragenomic conflict over bet-hedging

Abstract

Genomic imprinting, where an allele’s expression pattern depends on its parental origin, is thought to result primarily from an intragenomic evolutionary conflict. Imprinted genes are widely expressed in the brain and have been linked to various phenotypes, including behaviours related to risk tolerance.Here, we analyse a model of evolutionary bet-hedging in a system with imprinted gene expression. Previous analyses of bet-hedging have shown that natural selection may favour alleles and traits that reduce reproductive variance, even at the expense of reducing mean reproductive success, with the trade-off between mean and variance depending on the population size. In species where the sexes have different reproductive variances, this bet-hedging trade-off differs between maternally and paternally inherited alleles. Where males have the higher reproductive variance, alleles are more strongly selected to reduce variance when paternally inherited than when maternally inherited. We connect this result to phenotypes connected with specific imprinted genes, including delay discounting and social dominance. The empirical patterns are consistent with paternally expressed imprinted genes promoting risk-averse behaviours that reduce reproductive variance. Conversely, maternally expressed imprinted genes promote risk-tolerant, variance-increasing behaviours. Finally, we indicate how future research might further test the hypotheses suggested by our analysis.

Authors:
ORCiD logo [1]; ORCiD logo [2]
  1. Ronin Institute, Montclair, NJ (United States); Santa Fe Institute, NM (United States)
  2. Santa Fe Institute, NM (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1530782
Report Number(s):
LA-UR-18-25754
Journal ID: ISSN 0962-8436
Grant/Contract Number:  
89233218CNA000001
Resource Type:
Accepted Manuscript
Journal Name:
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
Additional Journal Information:
Journal Volume: 374; Journal Issue: 1766; Journal ID: ISSN 0962-8436
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wilkins, Jon F., and Bhattacharya, Tanmoy. Intragenomic conflict over bet-hedging. United States: N. p., 2018. Web. doi:10.1098/rstb.2018.0142.
Wilkins, Jon F., & Bhattacharya, Tanmoy. Intragenomic conflict over bet-hedging. United States. doi:10.1098/rstb.2018.0142.
Wilkins, Jon F., and Bhattacharya, Tanmoy. Mon . "Intragenomic conflict over bet-hedging". United States. doi:10.1098/rstb.2018.0142. https://www.osti.gov/servlets/purl/1530782.
@article{osti_1530782,
title = {Intragenomic conflict over bet-hedging},
author = {Wilkins, Jon F. and Bhattacharya, Tanmoy},
abstractNote = {Genomic imprinting, where an allele’s expression pattern depends on its parental origin, is thought to result primarily from an intragenomic evolutionary conflict. Imprinted genes are widely expressed in the brain and have been linked to various phenotypes, including behaviours related to risk tolerance.Here, we analyse a model of evolutionary bet-hedging in a system with imprinted gene expression. Previous analyses of bet-hedging have shown that natural selection may favour alleles and traits that reduce reproductive variance, even at the expense of reducing mean reproductive success, with the trade-off between mean and variance depending on the population size. In species where the sexes have different reproductive variances, this bet-hedging trade-off differs between maternally and paternally inherited alleles. Where males have the higher reproductive variance, alleles are more strongly selected to reduce variance when paternally inherited than when maternally inherited. We connect this result to phenotypes connected with specific imprinted genes, including delay discounting and social dominance. The empirical patterns are consistent with paternally expressed imprinted genes promoting risk-averse behaviours that reduce reproductive variance. Conversely, maternally expressed imprinted genes promote risk-tolerant, variance-increasing behaviours. Finally, we indicate how future research might further test the hypotheses suggested by our analysis.},
doi = {10.1098/rstb.2018.0142},
journal = {Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences},
number = 1766,
volume = 374,
place = {United States},
year = {2018},
month = {12}
}

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Works referenced in this record:

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    Works referencing / citing this record:

    Is there a genomically imprinted social brain?
    journal, August 2011


    The evolving landscape of imprinted genes in humans and mice: Conflict among alleles, genes, tissues, and kin
    journal, March 2016

    • Wilkins, Jon F.; Úbeda, Francisco; Van Cleve, Jeremy
    • BioEssays, Vol. 38, Issue 5
    • DOI: 10.1002/bies.201500198

    The coadaptation theory for genomic imprinting: THE COADAPTATION THEORY FOR GENOMIC IMPRINTING
    journal, May 2017

    • O'Brien, Eleanor K.; Wolf, Jason B.
    • Evolution Letters, Vol. 1, Issue 1
    • DOI: 10.1002/evl3.5

    Inbreeding, Maternal Care and Genomic Imprinting
    journal, April 2003


    Imprinted gene expression in the brain
    journal, May 2005


    Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest
    journal, October 1998

    • Lefebvre, Louis; Viville, Stéphane; Barton, Sheila C.
    • Nature Genetics, Vol. 20, Issue 2
    • DOI: 10.1038/2464

    Distinct physiological and behavioural functions for parental alleles of imprinted Grb10
    journal, January 2011

    • Garfield, Alastair S.; Cowley, Michael; Smith, Florentia M.
    • Nature, Vol. 469, Issue 7331
    • DOI: 10.1038/nature09651

    What good is genomic imprinting: the function of parent-specific gene expression
    journal, May 2003

    • Wilkins, Jon F.; Haig, David
    • Nature Reviews Genetics, Vol. 4, Issue 5
    • DOI: 10.1038/nrg1062

    Genomic imprinting: the emergence of an epigenetic paradigm
    journal, July 2011

    • Ferguson-Smith, Anne C.
    • Nature Reviews Genetics, Vol. 12, Issue 8
    • DOI: 10.1038/nrg3032

    Genomic imprinting effects on brain development and function
    journal, November 2007

    • Wilkinson, Lawrence S.; Davies, William; Isles, Anthony R.
    • Nature Reviews Neuroscience, Vol. 8, Issue 11
    • DOI: 10.1038/nrn2235

    The meaning of intragenomic conflict
    journal, November 2017


    A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2
    journal, March 1999

    • Peters, J.; Wroe, S. F.; Wells, C. A.
    • Proceedings of the National Academy of Sciences, Vol. 96, Issue 7
    • DOI: 10.1073/pnas.96.7.3830

    Natural Selection for Variances in Offspring Numbers: A New Evolutionary Principle
    journal, September 1977

    • Gillespie, John H.
    • The American Naturalist, Vol. 111, Issue 981
    • DOI: 10.1086/283230

    Evolution in a Variable Environment
    journal, August 1990

    • Frank, Steven A.; Slatkin, Montgomery
    • The American Naturalist, Vol. 136, Issue 2
    • DOI: 10.1086/285094

    Intragenomic Conflict over Dispersal
    journal, September 2015

    • Farrell, Elizabeth J.; Úbeda, Francisco; Gardner, Andy
    • The American Naturalist, Vol. 186, Issue 3
    • DOI: 10.1086/682275

    Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression
    journal, June 2009

    • Monk, David; Arnaud, Philippe; Frost, Jennifer
    • Human Molecular Genetics, Vol. 18, Issue 16
    • DOI: 10.1093/hmg/ddp248

    Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole–rat, Heterocephalus glaber
    journal, August 1998

    • Clarke, F. M.; Faulkes, C. G.
    • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 265, Issue 1404
    • DOI: 10.1098/rspb.1998.0447

    A possible role for imprinted genes in inbreeding avoidance and dispersal from the natal area in mice
    journal, April 2002

    • Isles, Anthony R.; Baum, Michael J.; Ma, Dan
    • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 269, Issue 1492
    • DOI: 10.1098/rspb.2001.1911

    Impulsive choices in mice lacking imprinted Nesp55: Impulsive choices in mice lacking imprinted Nesp55
    journal, September 2016

    • Dent, C. L.; Humby, T.; Lewis, K.
    • Genes, Brain and Behavior, Vol. 15, Issue 8
    • DOI: 10.1111/gbb.12316

    Dopaminergic and behavioural changes in a loss-of-imprinting model of Cdkn1c : Dopaminergic and behavioural changes in a loss-of-imprinting model of
    journal, September 2017

    • McNamara, G. I.; Davis, B. A.; Browne, M.
    • Genes, Brain and Behavior, Vol. 17, Issue 2
    • DOI: 10.1111/gbb.12422

    Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism
    journal, July 2006


    Antagonistic Coevolution of two Imprinted loci with Pleiotropic Effects
    journal, January 2010


    A Model for Genomic Imprinting in the Social Brain: Juveniles: Genomic Imprinting in the Social Brain
    journal, September 2010


    A Model for Genomic Imprinting in the Social Brain: Adults: Genomic Imprinting in the Social Brain
    journal, September 2010


    Impulsive Choice in Mice Lacking Paternal Expression of Grb10 Suggests Intragenomic Conflict in Behavior
    journal, March 2018