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Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition.

ABSTRACT: Competition between conspecifics during the breeding season can result in behavioural and physiological programming of offspring via maternal effects. For birds, in which maternal effects are best studied, it has been claimed that exposure to increased competition causes greater deposition of testosterone into egg yolks, which creates faster growing, more aggressive offspring; such traits are thought to be beneficial for high-competition environments. Nevertheless, not all species show a positive relationship between competitive interactions and yolk testosterone, and an explanation for this interspecific variation is lacking. We here test if the magnitude and direction of maternal testosterone allocated to eggs in response to competition can be explained by life-history traits while accounting for phylogenetic relationships. We performed a meta-analysis relating effect size of yolk testosterone response to competition with species coloniality, nest type, parental effort and mating type. We found that effect size was moderated by coloniality and nest type; colonial species and those with open nests allocate less testosterone to eggs when in more competitive environments. Applying a life-history perspective helps contextualize studies showing little or negative responses of yolk testosterone to competition and improves our understanding of how variation in this maternal effect may have evolved.

SUBMITTER: Bentz AB

PROVIDER: S-EPMC5180134 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition.

Bentz Alexandra B AB Becker Daniel J DJ Navara Kristen J KJ

Royal Society open science 20161130 11

Competition between conspecifics during the breeding season can result in behavioural and physiological programming of offspring via maternal effects. For birds, in which maternal effects are best studied, it has been claimed that exposure to increased competition causes greater deposition of testosterone into egg yolks, which creates faster growing, more aggressive offspring; such traits are thought to be beneficial for high-competition environments. Nevertheless, not all species show a positiv ...[more]

PMID: 28018636

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Project description: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 (Coturnix japonica) 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 in ovo 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.

Dataset Information

Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition.

Publications

Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition.

Similar Datasets

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