Long-term effect of yolk carotenoid levels on testis size in a precocial bird

Giraudeau, Mathieu; Ziegler, Ann-Kathrin; Tschirren, Barbara

doi:10.1098/rsbl.2016.0008

Cited by 11 publications

(4 citation statements)

References 30 publications

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“…Surprisingly, the consequences of variations in the levels of these maternally transmitted antioxidants on chick development and then on the adult phenotype have been seldom considered in the literature. The few studies that experimentally examined this question manipulated the concentration of one antioxidant in isolation through egg injections [3,5,[23][24][25][26]. Other studies used dietary carotenoid supplementation of females to indirectly manipulate levels of yolk antioxidants [27][28][29].…”

Section: Discussionmentioning

confidence: 99%

Co-adjustment of yolk antioxidants and androgens in birds

Giraudeau

Ducatez

2016

Biol. Lett.

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Mothers can shape the developmental trajectory of their offspring through the transmission of resources such as hormones, antioxidants or immunoglobulins. Over the last two decades, an abundant literature on maternal effects in birds has shown that several of these compounds (i.e. androgens, glucocorticoids and antioxidants) often influence the same offspring phenotypic traits (i.e. growth, immunity or oxidative stress levels), making interaction effects between egg components a likely scenario. However, the potential interactive effects of maternally transmitted compounds on offspring development and potential co-adjustment of these compounds within an egg are still poorly understood. Here, we report the results of an interspecific comparative analysis on birds' egg yolk composition (i.e. androgens and antioxidants) where we found that yolk carotenoid and vitamin E concentrations are positively associated, supporting the hypothesis that these two antioxidants act in synergy. The concentrations of vitamin E also increased with increasing concentrations of testosterone. This last result confirms the emerging idea that androgens and antioxidants are co-adjusted within eggs and that maternally transmitted antioxidants might limit the potential direct and indirect effects of prenatal exposure to high testosterone levels on oxidative stress.

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Section: Discussionmentioning

confidence: 99%

Co-adjustment of yolk antioxidants and androgens in birds

Giraudeau

Ducatez

2016

Biol. Lett.

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“…In turn, egg quality is the main mediator of maternal effects, which profoundly affect offspring fitness (Bernardo 1996;Mousseau and Fox 1998). Previous studies have extensively investigated the impact of maternal carotenoids on offspring fitness across a range of bird species, by mean of direct or indirect manipulation of carotenoids in the egg yolk (Surai et al 2001;Blount et al 2002;Saino et al 2003Saino et al , 2011McGraw et al 2005;Romano et al 2008;Giraudeau et al 2016). Egg carotenoids have important biological functions during embryonic development (Blount et al 2000;Koutsos et al 2003;Tyndale et al 2008).…”

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confidence: 99%

The DomesticBCO2Allele Buffers Low-Carotenoid Diets in Chickens: Possible Fitness Increase Through Species Hybridization

et al. 2019

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Domestic animals are adapted to conditions vastly different from those of their wild ancestors, and this is particularly true for their diets. The most numerous of all domestic species, the chicken, originated from the Red Junglefowl (RJF), a native of subtropical forests in Southeast Asia. Surprisingly however, in domestic chicken breeds, a common haplotype of the b-carotene oxygenase 2 (BCO2) gene, which is involved in carotenoid metabolism, is introgressed from a related species, the Gray Junglefowl, and has been under strong selective pressure during domestication. This suggests that a hybridization event may have conferred a fitness advantage on chickens carrying the derived allele. To investigate the possible biological function of the introgressed BCO2 allele in chicken, we introgressed the ancestral BCO2 allele into domestic White Leghorn chickens. We measured gene expression as well as carotenoid accumulation in skin and eggs of chickens carrying either the ancestral or the derived BCO2 allele. The derived haplotype was associated with down-regulation of BCO2 in skin, muscle, and adipose tissue, but not in liver or duodenum, indicating that carotenoid accumulation occurred in the tissues with reduced gene expression. Most importantly, we found that hens with the derived BCO2 genotype were capable of allocating stored carotenoids to their eggs, suggesting a functional benefit through buffering any shortage in the diet during egg production. Nevertheless, it is of interest that loss of function mutations in BCO2 gene are prevalent in other domesticates including cows, rabbits, and sheep, and, given the importance of carotenoids in development, reproduction, and immunity, it is possible that derived BCO2 alleles may provide a general mechanism in multiple domestic species to deal with higher demand for carotenoids in an environment with carotenoid shortage in the diet.

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“…Alternatively, or in addition, prenatal exposure to high carotenoid levels might shift the trade-off between selfmaintenance and reproduction towards a reduced reproductive investment during the first breeding event, as we have previously shown in males (i.e. reduced testis size [15]). Importantly, the transfer of lower concentrations of yolk antioxidants to eggs was only observed in females that experienced increased carotenoid but unmanipulated testosterone levels during embryo development.…”

Section: Discussionmentioning

confidence: 77%

In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs

et al. 2018

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Mothers can influence prenatal conditions by varying the amount of nutrients, hormones or antioxidants they provide to their developing young. Some of these substances even affect the transfer of these compounds in the next generation, but it is less clear how different maternally transmitted compounds interact with each other to shape reproductive resource allocation in their offspring. Here, we found that female Japanese quails () that were exposed to high carotenoid levels during embryonic development transferred lower concentrations of yolk antioxidants to their own eggs later in life. This effect disappeared when both testosterone and carotenoid concentrations were manipulated simultaneously, showing long-term and interactive effects of these maternally derived egg components on a female's own egg composition. Given that exposure to high levels of testosterone during embryo development stimulates the production of reactive oxygen species (ROS) and impairs antioxidant defenses, we propose that carotenoids act as antioxidants in an oxidatively stressful environment (i.e. when levels of testosterone are high) but might have prooxidant properties in an environment where they are not used to counteract an increased production of ROS. In line with this hypothesis, we previously showed that prenatal exposure to increased concentrations of yolk carotenoids leads to a rise of oxidative damage at adulthood, but only when yolk testosterone concentrations were not experimentally increased as well. As a consequence, antioxidants in the body may be used to limit oxidative damage in females exposed to high levels of carotenoids during development (but not in females exposed to increased levels of both carotenoids and testosterone), resulting in lower amounts of antioxidants being available for deposition into eggs. Since prenatal antioxidant exposure is known to influence fitness-related traits, the effect detected in this study might have transgenerational consequences.

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Long-term effect of yolk carotenoid levels on testis size in a precocial bird

Cited by 11 publications

References 30 publications

Co-adjustment of yolk antioxidants and androgens in birds

Co-adjustment of yolk antioxidants and androgens in birds

The DomesticBCO2Allele Buffers Low-Carotenoid Diets in Chickens: Possible Fitness Increase Through Species Hybridization

In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs

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