American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Oxidative stress experienced during early development influences the offspring phenotype”

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Ana Angela Romero-Haro and Carlos Alonso-Alvarez (Dec 2020)

Transgenerational effects of sustaining low antioxidant (glutathione) levels during early life

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Zebra finch (<i>Taeniopygia guttata</i>) nestling.<br />(Photo © Lorenzo Pérez-Rodríguez)
Zebra finch (Taeniopygia guttata) nestling.
(Photo © Lorenzo Pérez-Rodríguez)

Oxidative stress is an imbalance between the level of reactive oxygen species produced by metabolism and the state of the antioxidant machinery controlling them. The imbalance leads to oxidative damage with potentially long-lasting consequences. However, the impact of oxidative stress in the next generations is poorly understood. Most studies analyzing these transgenerational effects have used compounds only indirectly related to oxidative stress, such as pollutants or radiation. Here, researchers from the University of Exeter (UK) and Museo Nacional de Ciencias Naturales (Spain) experimentally decrease the levels of a vital cellular antioxidant, glutathione, during the early development of zebra finches (Taeniopygia guttata) and study its impact on the next generation. Glutathione is synthesized from dietary amino acids, and undernourishment, a common situation in wild birds during early life, affects their levels. Previously, researchers demonstrated that low glutathione levels during development induced oxidative stress and changes in body mass and coloration in adulthood. When the same birds bred, their newborn chicks were moved among nests to distinguish between pre- and post-natal parental effects (i.e., those induced by the biological or, instead, foster parents). Female chicks from biological mothers that experienced early-life oxidative stress don’t attain a high body mass under favorable nest conditions (i.e. reduced brood sizes), suggesting a constraining effect on the maternal capacity to transfer resources to eggs. Moreover, nestlings grow shorter legs when raised by both foster parents from the early oxidative stress treatment. Hence, the treatment also affects the parental capacity to provide resources to chicks. The results demonstrate that early-life oxidative stress is able to alter the offspring phenotype, which might have an impact on evolutionary life-history trade-offs. Providing enough dietary resources to descendants to avoid oxidative stress could compromise parental survival, but simultaneously improve parental fitness through the phenotype of the second generation.


Abstract

Oxidative stress (OS) experienced early in life can affect an individual’s phenotype. However, its consequences for the next generation remain largely unexplored. We manipulated the OS level endured by zebra finches (Taeniopygia guttata) during their development by transitorily inhibiting the synthesis of the key antioxidant glutathione (‘early-high-OS’). The offspring of these birds and control parents were cross-fostered at hatching to enlarge or reduce its brood size. Independently of parents’ early-life OS levels, the chicks raised in enlarged broods showed lower erythrocyte glutathione levels, revealing glutathione sensitivity to environmental conditions. Control (“early-low-OS”) biological mothers produced females, not males, that attained a higher body mass when raised in a benign environment (i.e. the reduced brood). In contrast, biological mothers exposed to early-life OS produced heavier males, not females, when allocated in reduced broods. Early-life OS also affected the parental rearing capacity because 12d-old nestlings raised by a foster pair with both early-high-OS members grew shorter legs (tarsus) than chicks from other groups. The results indicate that environmental conditions during development can affect early glutathione levels, which may, in turn, influence the next generation through both pre- and postnatal parental effects. The results also demonstrate that early-life OS can constrain the offspring phenotype.