Embryonic thermal manipulation has short and long-term effects on the development and the physiology of the Japanese quail

Anaïs Vitorino Carvalho,Nathalie Couroussé,Veerle M Darras,Sabine Crochet,Tatiana Zerjal,Pascal Chartrin,Thierry Bordeau,Vincent Coustham,Christelle Hennequet-Antier,Estelle Cailleau-Audouin,Anne Collin

doi:10.1371/journal.pone.0227700

Abstract

In vertebrates, the embryonic environment is known to affect the development and the health of individuals. In broiler chickens, the thermal-manipulation (TM) of eggs during the incubation period was shown to improve heat tolerance at slaughter age (35 days of age) in association with several modifications at the molecular, metabolic and physiological levels. However, little is known about the Japanese quail (Coturnix japonica), a closely related avian species widely used as a laboratory animal model and farmed for its meat and eggs. Here we developed and characterized a TM procedure (39.5°C and 65% relative humidity, 12 h/d, from days 0 to 13 of incubation) in quails by analyzing its short and long-term effects on zootechnical, physiological and metabolic parameters. Heat-tolerance was tested by a heat challenge (36°C for 7h) at 35 days of age. TM significantly reduced the hatching rate of the animals and increased mortality during the first four weeks of life. At hatching, TM animals were heavier than controls, but lighter at 25 days of age for both sexes. Thirty-five days after hatching, TM decreased the surface temperature of the shank in females, suggesting a modulation of the blood flow to maintain the internal temperature. TM also increased blood partial pressure and oxygen saturation percentage at 35 days of age in females, suggesting a long-term modulation of the respiration physiology. Quails physiologically responded to the heat challenge, with a modification of several hematologic and metabolic parameters, including an increase in plasma corticosterone concentration. Several physiological parameters such as beak surface temperature and blood sodium concentration revealed that TM birds responded differently to the heat challenge compared to controls. Altogether, this first comprehensive characterization of TM in Japanese quail showed durable effects that may affect the response of TM quails to heat.

Highlights

In vertebrates, the embryonic environment affects the development and health of individuals from birth to adulthood [1]
TM was applied by increasing the incubation temperature to 39.5 ̊C and 65% relative humidity (RH) for 12 h/d from I0 [39,40,41] to I13 (Fig 1), in the second incubator
We found that TM significantly increased quail mortality during this period (Fig 2)

Summary

Introduction

The embryonic environment affects the development and health of individuals from birth to adulthood [1]. The incubation conditions can be modified in order to study the impact of environmental challenges or stressors during embryogenesis, reducing the impact of the maternal influence. Incubation parameters such as temperature [2], light [3] or noise [4] are known to impact development and behavior. The TM protocols were shown to have a long-term impact on the performance (weight gain, muscle yield, etc.), the physiology (thyroid axis function, acid-base balance, respiratory process, etc.), the metabolism (glucose metabolism, regulation of mitochondrial function, etc.), the regulation of gene expression and the epigenome landscape [7,9,10,12,13,14,22,23]

Methods

Results

Discussion

Conclusion