Sensitivity of organ growth to chronically low oxygen levels during incubation in Red Junglefowl and domesticated chicken breeds

Abstract

Genetic selection programs have imposed large phenotypic changes in domesticated chicken breeds that are also apparent during embryonic development. Broilers, for example, have a faster growth rate before hatching in comparison with White Leghorns, indicating that the allocation of resources toward different functions already begins before hatching. Therefore, we hypothesized that embryonic organ growth would follow different developmental trajectories and would be differentially affected by an oxygen shortage during incubation. Heart, brain, and liver growth were studied in broiler, White Leghorn, and Red Junglefowl embryos at embryonic (E) ages E11, E13, E15, E18, and E20, and the results were fitted to growth allometric equations to determine the degree of organ stunting or sparing caused by low oxygen during incubation. Hypoxia caused a 3-fold larger mortality in Red Junglefowl than in the domesticated breeds, with a similar impairment of embryonic growth of 18%, coupled with a reduction in yolk utilization of 56%. Relative brain size was not affected by hypoxia in any breed, but a substantial stunting effect was observed for the liver and heart at late embryonic ages, with marked differences between breeds. In Red Junglefowl, only the heart was stunted. In White Leghorns, only the liver was stunted, and in broilers, both organs were stunted. These results can be explained in terms of the selection pressure on long-term production traits (reproductive effort) in White Leghorns, requiring a more efficient lipid metabolism, compared with the selection pressure on shorter-term production traits (growth) in broilers, requiring overall metabolic turnover and convective nutrient delivery to all tissues. At the same time, a remarkable sparing of the heart was observed in broilers and Red Junglefowl between E11 and E15, which suggests that cardiac growth can be manipulated during embryonic development. This result could be relevant for manipulating the phenotype of the heart for management purposes at a developmental stage when the bird is most versatile and phenotypically malleable.

Plasticity of cardiovascular function in snapping turtle embryos (Chelydra serpentina): chronic hypoxia alters autonomic regulation and gene expression

“…Hypoxia has also been shown to have discordant effects on cardiac versus somatic growth in crocodilian and mammalian embryos, i.e., reduced body size and increased heart-to-body mass ratio (15,49). The precise effect of hypoxia on heart mass relative to body mass in chicken embryos varies by breed and embryonic age (37). Nevertheless, all breeds displayed the same general pattern with enlarged hearts earlier in development and smaller hearts later in development.…”

“…For example, hypoxic conditions during embryogenesis have pronounced effects on cardiovascular development in mammals (5, 12, 46), including catecholaminergic overstimulation that modified signaling pathways associated with adrenergic regulation (41,44,50). Over the past 30 years, research has clarified patterns of cardiovascular maturation during early development (18,30,37,51,52). Cardiovascular responses to hypoxic stress during embryogenesis have been investigated in chickens (Gallus gallus) and several mammals, including rats (Rattus sp.…”

Genome Resequencing Identifies Unique Adaptations of Tibetan Chickens to Hypoxia and High-Dose Ultraviolet Radiation in High-Altitude Environments

“…When elevated metabolic requirements exceed the supply of oxygen due to the reduced partial pressure with increasing altitude, the capacity of cardiovascular and respiratory systems is suppressed ( Tekin et al 2010 ). Hypoxic conditions have been previously reported to result in hypotension in Red Jungle fowl ( Lindgren and Altimiras 2011 ). The inadequate supply of oxygen also affects physiological performance and inhibits growth capacity ( Semenza 2012 ).…”

Developmental programming of cardiovascular disease by prenatal hypoxia

“…It is now established that exposure of the chick embryo to chronic hypoxia promotes asymmetric fetal growth restriction, cardiac and aortic hypertrophic growth, altered cardiac function and sympathetic hyper-innervation of peripheral resistance arteries by the end of the incubation period. [42][43][44][45][46][47][48][49][50][51][52][53] The asymmetric growth restriction and cardiac and aortic wall remodelling that develops in sea level chick embryos incubated at high altitude no longer occurs in sea level embryos incubated at high altitude with oxygen supplementation, 49,52 underlying the direct effects of isolated chronic hypoxia on fetal growth and cardiovascular development. Asymmetric growth restriction, aortic wall thickening, cardiac and vascular dysfunction have also been reported in the chronically hypoxic fetus of mammalian species, such as in sheep, rodents and guinea pigs.…”