Abstract
BackgroundIn chicken, oils in the maternal diet confer a specific scent to the yolk. Embryos are known to perceive and memorize chemosensory signals of the surrounding environment; however, the potential impact of the maternal diet has not previously been investigated. In the present study, we hypothesized that chicken embryos memorize the chemical signals of the maternal diet and that this perceptual learning may orient subsequent feeding behavior of the hatchlings.Methodology/Principal FindingsLaying hens were fed standard food enriched with 2% menhaden oil (MH group) or 2% soybean oil (controls). The scent of menhaden was significantly more detected in MH egg yolks than in control yolks by a human panel. We analyzed the development and behavior of offspring towards different types of food, bearing or not bearing the menhaden scent. When chicks were exposed to a 3-min choice test between the familiar food bearing the menhaden scent and the familiar food without menhaden, no effect of treatment was observed. In a 3-min choice test with unfamiliar food (mashed cereals) MH chicks showed a clear positive orientation toward the unfamiliar food bearing the menhaden scent. By contrast, control chicks showed a preference for the non-odorized unfamiliar food. MH chicks expressed higher emotional reactivity level than control chicks as expressed by food neophobia and longer immobility in a restraint test.Conclusion/SignificanceChicks exposed in ovo to menhaden oil via the maternal diet preferentially oriented their feeding behavior towards food containing menhaden oil, but only when the food was unfamiliar. We propose that oil in the maternal diet engenders maternal effects and contributes to the development of behavioral phenotype in the offspring. In ovo chemosensory learning may have evolved to prepare precocial offspring for their environment. This suggests a common principle of embryonic chemosensory learning across vertebrate taxa.
Highlights
During the last two decades, extensive research has shown that fetuses can respond to and memorize the chemosensory signals to which they are exposed
We propose that oil in the maternal diet engenders maternal effects and contributes to the development of behavioral phenotype in the offspring
The main results can be summarized as follows: (i) offspring of hens fed with a diet containing menhaden oil showed a short-term preference for unfamiliar food bearing the scent of menhaden; and (ii) when confronted with a novel food or restraint in a tonic immobility test, offspring of hens fed with a diet containing menhaden oil expressed stronger fear reactions than did control chicks
Summary
During the last two decades, extensive research has shown that fetuses can respond to and memorize the chemosensory signals to which they are exposed. In utero odorants – which include metabolites from the mother’s diet – can pass through the placental barrier and enter the amniotic liquid or blood of the fetus [1,2,3] Exposure to such chemosensory signals can orient the behavior of young animals. The preferential response of infant mammals to odors or flavors encountered in utero and prior to weaning is well documented for lambs [5], dogs [6], rats [7] mice [8] and humans [9,10,11] This positive orientation towards familiar odors influences the feeding behavior of young individuals. We hypothesized that chicken embryos memorize the chemical signals of the maternal diet and that this perceptual learning may orient subsequent feeding behavior of the hatchlings
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