Thermal conditioning of quail embryos has transgenerational and reversible long-term effects.
Avian
Embryo
Programming
Temperature
Transgenerational inheritance
Journal
Journal of animal science and biotechnology
ISSN: 1674-9782
Titre abrégé: J Anim Sci Biotechnol
Pays: England
ID NLM: 101581293
Informations de publication
Date de publication:
03 Oct 2023
03 Oct 2023
Historique:
received:
27
03
2023
accepted:
01
08
2023
medline:
3
10
2023
pubmed:
3
10
2023
entrez:
2
10
2023
Statut:
epublish
Résumé
In the current context of global warming, thermal manipulation of avian embryos has received increasing attention as a strategy to promote heat tolerance in avian species by simply increasing the egg incubation temperature. However, because of their likely epigenetic origin, thermal manipulation effects may last more than one generation with consequences for the poultry industry. In this work, a multigenerational and transgenerational analysis of thermal manipulation during embryogenesis was performed to uncover the long-term effects of such procedure. Thermal manipulation repeated during 4 generations had an effect on hatchability, body weight, and weight of eggs laid in Japanese quails, with some effects increasing in importance over generations. Moreover, the effects on body weight and egg weight could be transmitted transgenerationally, suggesting non-genetic inheritance mechanisms. This hypothesis is reinforced by the observed reversion of the effect on growth after five unexposed generations. Interestingly, a beneficial effect of thermal manipulation on heat tolerance was observed a few days after hatching, but this effect was not transgenerational. Our multigenerational study showed that thermal conditioning of quail embryos has a beneficial effect on post-hatch heat tolerance hampered by transgenerational but reversible defects on growth. Assuming that no genetic variability underlies these changes, this study provides the first demonstration of epigenetic inheritance of traits induced by environmental temperature modification associated with long-term impacts in an avian species.
Sections du résumé
BACKGROUND
BACKGROUND
In the current context of global warming, thermal manipulation of avian embryos has received increasing attention as a strategy to promote heat tolerance in avian species by simply increasing the egg incubation temperature. However, because of their likely epigenetic origin, thermal manipulation effects may last more than one generation with consequences for the poultry industry. In this work, a multigenerational and transgenerational analysis of thermal manipulation during embryogenesis was performed to uncover the long-term effects of such procedure.
RESULTS
RESULTS
Thermal manipulation repeated during 4 generations had an effect on hatchability, body weight, and weight of eggs laid in Japanese quails, with some effects increasing in importance over generations. Moreover, the effects on body weight and egg weight could be transmitted transgenerationally, suggesting non-genetic inheritance mechanisms. This hypothesis is reinforced by the observed reversion of the effect on growth after five unexposed generations. Interestingly, a beneficial effect of thermal manipulation on heat tolerance was observed a few days after hatching, but this effect was not transgenerational.
CONCLUSIONS
CONCLUSIONS
Our multigenerational study showed that thermal conditioning of quail embryos has a beneficial effect on post-hatch heat tolerance hampered by transgenerational but reversible defects on growth. Assuming that no genetic variability underlies these changes, this study provides the first demonstration of epigenetic inheritance of traits induced by environmental temperature modification associated with long-term impacts in an avian species.
Identifiants
pubmed: 37784159
doi: 10.1186/s40104-023-00924-2
pii: 10.1186/s40104-023-00924-2
pmc: PMC10546792
doi:
Types de publication
Journal Article
Langues
eng
Pagination
124Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-15-CE02-0009-01
Informations de copyright
© 2023. Chinese Association of Animal Science and Veterinary Medicine.
Références
J Anim Sci. 2013 Aug;91(8):3674-85
pubmed: 23736053
Poult Sci. 2008 Aug;87(8):1516-25
pubmed: 18648043
Res Vet Sci. 2015 Apr;99:105-11
pubmed: 25596919
Science. 2012 Aug 3;337(6094):584-7
pubmed: 22798408
J Appl Physiol (1985). 2009 Jan;106(1):233-40
pubmed: 19023019
Front Physiol. 2019 Dec 12;10:1495
pubmed: 31920700
Br Poult Sci. 1987 Dec;28(4):749-52
pubmed: 3446342
Genet Sel Evol. 2017 Jan 26;49(1):14
pubmed: 28125975
Science. 2016 Oct 7;354(6308):59-63
pubmed: 27846492
Environ Epigenet. 2018 Apr 26;4(2):dvy008
pubmed: 29732172
BMC Genomics. 2016 May 04;17:329
pubmed: 27142519
Eur J Neurosci. 2008 Dec;28(11):2267-77
pubmed: 19046370
Cell. 2011 Jun 24;145(7):1049-61
pubmed: 21703449
PLoS One. 2020 Jan 23;15(1):e0227700
pubmed: 31971994
Nature. 2011 Jul 24;476(7358):105-8
pubmed: 21785438
Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14247-52
pubmed: 22891320
BMC Genomics. 2021 Jun 30;22(1):488
pubmed: 34193035
Poult Sci. 2017 Jan 1;96(1):234-240
pubmed: 27587725
Front Genet. 2019 Nov 26;10:1207
pubmed: 31850067
Biom J. 2008 Jun;50(3):346-63
pubmed: 18481363
J Exp Biol. 2018 Jul 17;221(Pt 14):
pubmed: 29844198
Animal. 2015 Jan;9(1):76-85
pubmed: 25118598