Transmissibility model to evaluate transgenerational transmission of environmental effects in quails

Both genetic and non-genetic information, which contribute to the development of phenotypes, can be transmitted across generations. Non-genetic information can be modified by the environment, allowing environmental effects to be transmitted to the next generation. The objective of the present study was to use an experimental design in quail combined with the transmissibility models, to demonstrate the vertical transmission of environmental effects. The study involved creating two lines: a control line and a treatment line, where female quails were fed a genistein-supplemented diet. Genistein is an endocrine disruptor that affects methylation patterns. Then, reproduction of these lines was conducted in a mirrored mating design over three generations, with a total of 1 566 animals studied. Quails underwent behavioural tests measuring locomotor activity and were weighed at one, four, and 7 weeks of age. At slaughter, body and abdominal adipose weights were recorded. The transmissibility model was a mixed model with fixed effects of rearing condition, sex, generation, age at time of measurement and direct effect of the genistein (on the animal, embryo and germ cells) and the random effect of the transmissible potential of the animal which transmissibility matrix contains sire and dam path coefficients of transmission that have to be estimated conversely to the genetic model where they are fixed to 0.5. The transmissibility model with environment included additional covariance for offspring of genistein-fed dams which is then transmitted to next generations via sires and dams. Models were chosen according to the likelihood ratio test. The proportion of transmitted variance varied from 0.34 (at 1 week) to 0.72 (at 7 weeks) for BW, 0.20 for the behavioural trait and 0.22 for adiposity. The estimated sire and dam path coefficients ranged from 0.42 to 0.52, but were not significantly different from 0.50. With the transmissibility model with environment, the additional covariance was significantly different from zero for BW traits, indicating transgenerational transmission of genistein's effects. This value corresponded to a high correlation at 1 week (0.44) but low for other BW traits. The transmissibility model with environment demonstrated the transgenerational transmission of genistein-induced environmental effects on BW traits in quail, putatively mediated by epigenetic inheritance. The findings suggest that beneficial environmental factors can positively impact multiple generations, and combining this with genetic selection could accelerate adaptation to new environmental challenges.

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Publication Details

Journal
animal
Published
2025-08-28
DOI
https://doi.org/10.1016/j.animal.2025.101636
Primary Topic
Animal Nutrition and Physiology
Type
article
Field-Weighted Citation Impact
0.00

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article

Transmissibility model to evaluate transgenerational transmission of environmental effects in quails

Anne Ricard, Keyvan Karami, Sonia E Eynard, Ingrid David et al.
animal
Animal Nutrition and Physiology
article

Transmissibility model to evaluate transgenerational transmission of environmental effects in quails

Anne Ricard, Keyvan Karami, Sonia E Eynard, Ingrid David, Frédérique Pitel, David Gourichon, Sophie Leroux, Stacy Rousse
article en

Abstract

Both genetic and non-genetic information, which contribute to the development of phenotypes, can be transmitted across generations. Non-genetic information can be modified by the environment, allowing environmental effects to be transmitted to the next generation. The objective of the present study was to use an experimental design in quail combined with the transmissibility models, to demonstrate the vertical transmission of environmental effects. The study involved creating two lines: a control line and a treatment line, where female quails were fed a genistein-supplemented diet. Genistein is an endocrine disruptor that affects methylation patterns. Then, reproduction of these lines was conducted in a mirrored mating design over three generations, with a total of 1 566 animals studied. Quails underwent behavioural tests measuring locomotor activity and were weighed at one, four, and 7 weeks of age. At slaughter, body and abdominal adipose weights were recorded. The transmissibility model was a mixed model with fixed effects of rearing condition, sex, generation, age at time of measurement and direct effect of the genistein (on the animal, embryo and germ cells) and the random effect of the transmissible potential of the animal which transmissibility matrix contains sire and dam path coefficients of transmission that have to be estimated conversely to the genetic model where they are fixed to 0.5. The transmissibility model with environment included additional covariance for offspring of genistein-fed dams which is then transmitted to next generations via sires and dams. Models were chosen according to the likelihood ratio test. The proportion of transmitted variance varied from 0.34 (at 1 week) to 0.72 (at 7 weeks) for BW, 0.20 for the behavioural trait and 0.22 for adiposity. The estimated sire and dam path coefficients ranged from 0.42 to 0.52, but were not significantly different from 0.50. With the transmissibility model with environment, the additional covariance was significantly different from zero for BW traits, indicating transgenerational transmission of genistein's effects. This value corresponded to a high correlation at 1 week (0.44) but low for other BW traits. The transmissibility model with environment demonstrated the transgenerational transmission of genistein-induced environmental effects on BW traits in quail, putatively mediated by epigenetic inheritance. The findings suggest that beneficial environmental factors can positively impact multiple generations, and combining this with genetic selection could accelerate adaptation to new environmental challenges.

animalVol. 19(10)
École Nationale Vétérinaire de Toulouse (FR), Université Fédérale de Toulouse Midi-Pyrénées (FR), AgroParisTech (FR), Université Paris-Saclay (FR), Microbiologie de l’alimentation au service de la santé (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Services déconcentrés d'appui à la recherche Val de Loire (FR), Génétique Physiologie et Systèmes d'Elevage (FR)
Horizon 2020 Framework Programme
Openalex Percentile: Top 74%
Animal Nutrition and Physiology
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