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Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs

Maternal effects on offspring growth can impact survival and evolution of natural and domesticated populations. Genetic correlation estimates often support a negative relationship between direct and maternal effects. However, the genetic underpinnings whereby this antagonism operates are unclear. In...

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Autores principales: Solé, Emma, Ros-Freixedes, Roger, Tor, Marc, Reixach, Josep, Pena, Ramona N., Estany, Joan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7842917/
https://www.ncbi.nlm.nih.gov/pubmed/33508034
http://dx.doi.org/10.1371/journal.pone.0246198
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author Solé, Emma
Ros-Freixedes, Roger
Tor, Marc
Reixach, Josep
Pena, Ramona N.
Estany, Joan
author_facet Solé, Emma
Ros-Freixedes, Roger
Tor, Marc
Reixach, Josep
Pena, Ramona N.
Estany, Joan
author_sort Solé, Emma
collection PubMed
description Maternal effects on offspring growth can impact survival and evolution of natural and domesticated populations. Genetic correlation estimates often support a negative relationship between direct and maternal effects. However, the genetic underpinnings whereby this antagonism operates are unclear. In pigs, sow feeding status and body composition condition piglet development and growth. We hypothesized that variants in genes impacting these traits may be causative of maternal influences that could be antagonistic to the direct effects for piglet growth. A recessive missense mutation (C>T) in the porcine leptin receptor (LEPR) gene (rs709596309) has been identified as the possible causal polymorphism for increased feed intake and fatness. Using data from a Duroc line, we show that the TT sows exerted a negative impact on the body weight of their offspring at the end of the growing period of similar extent to the positive direct effect of the TT genotype over each individual. Thus, TT pigs from TT dams were about as heavy as CC and CT (C–) pigs from C–dams, but TT pigs from C–dams were around 5% heavier than C–pigs from TT dams. In contrast, body composition was only influenced by LEPR direct effects. This antagonism is due to a higher propensity of TT pigs for self-maintenance rather than for offspring investment. We show that TT pigs consumed more feed, favored fatty acid uptake over release, and produced lighter piglets at weaning than their C–counterparts. We conclude that LEPR underlies a transgenerational mechanism for energy distribution that allocates resources to the sow or the offspring according to whether selective pressure is exerted before or after weaning.
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spelling pubmed-78429172021-02-02 Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs Solé, Emma Ros-Freixedes, Roger Tor, Marc Reixach, Josep Pena, Ramona N. Estany, Joan PLoS One Research Article Maternal effects on offspring growth can impact survival and evolution of natural and domesticated populations. Genetic correlation estimates often support a negative relationship between direct and maternal effects. However, the genetic underpinnings whereby this antagonism operates are unclear. In pigs, sow feeding status and body composition condition piglet development and growth. We hypothesized that variants in genes impacting these traits may be causative of maternal influences that could be antagonistic to the direct effects for piglet growth. A recessive missense mutation (C>T) in the porcine leptin receptor (LEPR) gene (rs709596309) has been identified as the possible causal polymorphism for increased feed intake and fatness. Using data from a Duroc line, we show that the TT sows exerted a negative impact on the body weight of their offspring at the end of the growing period of similar extent to the positive direct effect of the TT genotype over each individual. Thus, TT pigs from TT dams were about as heavy as CC and CT (C–) pigs from C–dams, but TT pigs from C–dams were around 5% heavier than C–pigs from TT dams. In contrast, body composition was only influenced by LEPR direct effects. This antagonism is due to a higher propensity of TT pigs for self-maintenance rather than for offspring investment. We show that TT pigs consumed more feed, favored fatty acid uptake over release, and produced lighter piglets at weaning than their C–counterparts. We conclude that LEPR underlies a transgenerational mechanism for energy distribution that allocates resources to the sow or the offspring according to whether selective pressure is exerted before or after weaning. Public Library of Science 2021-01-28 /pmc/articles/PMC7842917/ /pubmed/33508034 http://dx.doi.org/10.1371/journal.pone.0246198 Text en © 2021 Solé et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Solé, Emma
Ros-Freixedes, Roger
Tor, Marc
Reixach, Josep
Pena, Ramona N.
Estany, Joan
Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title_full Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title_fullStr Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title_full_unstemmed Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title_short Antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
title_sort antagonistic maternal and direct effects of the leptin receptor gene on body weight in pigs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7842917/
https://www.ncbi.nlm.nih.gov/pubmed/33508034
http://dx.doi.org/10.1371/journal.pone.0246198
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