The Level of an Intracellular Antioxidant during Development Determines the Adult Phenotype in a Bird Species: A Potential Organizer Role for Glutathione

Abstract

Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.1rd58.abstract: Life-history traits are often involved in trade-offs whose outcome would depend on the availability of resources but also on the state of specific molecular signals. Early conditions can influence trade-offs and program the phenotype throughout the lifetime, with oxidative stress likely involved in many taxa. Here we address the potential regulatory role of a single intracellular antioxidant in lifehistory trade-offs. Blood glutathione levels were reduced in a large sample of birds (zebra finch Taeniopygia guttata) during development using the synthesis inhibitor buthionine sulfoximine (BSO). Results revealed several modifications in the adult phenotype. BSO-treated nestlings showed lower glutathione and plasma antioxidant levels. In adulthood, BSO birds endured greater oxidative damage in erythrocytes but stronger expression of a sexual signal. Moreover, adult BSO females also showed weaker resistance to oxidative stress but were heavier and showed better body condition. Results suggest that low glutathione values during growth favor the investment in traits that should improve fitness returns, probably in the form of early reproduction. Higher oxidative stress in adulthood may be endured if this cost is paid later in life. Either the presence of specific signaling mechanisms or the indirect effect of increased oxidative stress can explain our findings.

The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species

“…A blood sample (approximately 100 ml from the brachial vein) was collected for each bird 8 days after the start of the treatment. The effect of the treatment on total glutathione (tGSH) levels was significant in all subsamples of birds analysed in the study (always: [25]). Males and females were housed separately in different indoor aviaries at independence (approximately 40 days old).…”

“…Half of the birds underwent a transient artificial reduction in their capacity to synthesize the most important intracellular antioxidant (i.e. glutathione) during growth [25,26]. In adulthood, the birds were allowed to mate and breed freely in an outdoor aviary.…”

“…Thus, BSO chicks received a total of 12 mg BSO. BSO is a specific inhibitor of the first enzyme in the glutathione biosynthesis pathway (see the electronic supplementary material; also [25]). The treatments were randomly allocated in each brood (electronic supplementary material).…”

Temperature experienced during incubation affects antioxidant capacity but not oxidative damage in hatchling red-eared slider turtles (Trachemys scripta elegans)

“…Consistent with this prediction, both pre-and postnatal stress experience has been related to variability in adult redox status (Constantini et al, 2012;Marasco et al, 2013;Noguera et al, 2015;Romero-Haro and Alonso-Alvarez, 2015;Zimmer and Spencer, 2015). For instance, following an intense heat stress in adulthood, zebra finches (Taeniopygi guttata) that had been exposed to a mild heat stress as juveniles acquired less oxidative damage than individuals with no prior exposure to heat stress (Constantini et al, 2012).…”

“…Similarly, plasticity of oxidative stress resistance and antioxidant defenses has also been observed following prenatal glucocorticoid exposure (Marasco et al, 2013;Zimmer and Spencer, 2015) and limited posthatch nutrient availability (Noguera et al, 2015;Romero-Haro and Alonso-Alvarez, 2015). The apparent priming of redox systems by early life experiences has been suggested to arise through epigenetic modifications of gene expression or post-translational alterations of enzymes (Romero-Haro and Alonso-Alvarez, 2015;Noguera et al, 2015) and may result in context-dependent fitness consequences (Marasco et al, 2013;Constantini et al, 2014;Noguera et al, 2015;Zimmer and Spencer, 2015).…”