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

In the early 2000s, a new component of the cost of reproduction was proposed: oxidative stress. Since then the oxidative cost of reproduction hypothesis has, however, received mixed support. Different arguments have been provided to explain this. Among them, the lack of a life-history perspective on most experimental tests was suggested. We manipulated the levels of a key intracellular antioxidant (glutathione) in captive zebra finches (Taeniopygia guttata) during a short period of early life and subsequently tested the oxidative cost of reproduction. Birds were allowed to mate freely in an outdoor aviary for several months. We repeatedly enlarged or reduced their broods to increase or reduce, respectively, breeding effort. Birds whose glutathione levels were reduced during growth showed higher erythrocyte resistance to free radical-induced haemolysis when forced to rear enlarged broods. This supports the hypothesis predicting the occurrence of developing programmes matching early and adult environmental conditions to improve fitness. Moreover, adult males rearing enlarged broods endured higher plasma levels of lipid oxidative damage than control males, whereas adult females showed the opposite trend. As most previous studies reporting non-significant or opposite results used females only, we also discuss some sex-related particularities that may contribute to explain unexpected results.

Early Oxidative Stress May Prevent a Red Ornament From Signaling Longevity.

Harsh early environmental conditions can exert delayed, long-lasting effects on phenotypes, including reproductive traits such as sexual signals. Indeed, adverse early conditions can accelerate development, increasing oxidative stress that may, in turn, impact adult sexual signals. Among signals, colorations produced by red ketocarotenoids seem to depend on mitochondrial functioning. Hence, they could reveal individual cell respiration efficiency. It has been hypothesized that these traits are unfalsifiable "index" signals of condition due to their deep connection to individual metabolism. Since mitochondrial dysfunction is frequently linked to aging, red ketocarotenoid-based ornaments could also be good signals of a critical fitness component: longevity. We tested this red color per longevity correlation in captive zebra finches. In addition, we experimentally decreased the synthesis of glutathione (a critical intracellular antioxidant) during the first days of the birds' life to resemble harsh early environmental conditions (e.g., undernutrition). Longevity was recorded until the death of the last bird (almost 9 years). Males, but not females, exhibiting a redder bill in early adulthood lived longer than males with paler bills, which agrees with some precedent studies. However, such bill redness-longevity connection was absent among males with inhibited glutathione synthesis. These findings may suggest that environmental factors can alter the reliability of red ketocarotenoid-based sexual signals, making them less unfalsifiable than believed.

Low Antioxidant Glutathione Levels Lead to Longer Telomeres: A Sex-Specific Link to Longevity?

Telomeres are repetitive DNA sequences at the end of chromosomes that protect them from degradation. They have been the focus of intense research because short telomeres would predict accelerated ageing and reduced longevity in vertebrates. Oxidative stress is considered a physiological driver of the telomere shortening and, consequently, short lifespan. Among molecules fighting against oxidative stress, glutathione is involved in many antioxidant pathways. Literature supports that oxidative stress may trigger a compensatory "hormetic" response increasing glutathione levels and telomere length. Here, we tested the link between total glutathione concentration and telomere length in captive birds (zebra finches; Taeniopygia guttata). Total glutathione levels were experimentally decreased during birds' growth using a specific inhibitor of glutathione synthesis (buthionine sulfoximine; BSO). We monitored the birds' reproductive performance in an outdoor aviary during the first month of life, and their longevity for almost 9 years. Among control individuals, erythrocyte glutathione levels during development positively predicted erythrocyte telomere length in adulthood. However, BSO-treated females, but not males, showed longer telomeres than control females in adulthood. This counterintuitive finding suggests that females mounted a compensatory response. Such compensation agrees with precedent findings in the same population where the BSO treatment increased growth and adult body mass in females but not males. BSO did not influence longevity or reproductive output in any sex. However, early glutathione levels and adult telomere length interactively predicted longevity only among control females. Those females with "naturally" low (non-manipulated) glutathione levels at the nestling age but capable of producing longer telomeres in adulthood seem to live longer. The results suggest that the capability to mount a hormetic response triggered by low early glutathione levels can improve fitness via telomere length. Overall, the results may indicate a sex-specific link between glutathione and telomere values. Telomerase activity and sexual steroids (estrogens) are good candidates to explain the sex-biased mechanism underlying the early-life impact of oxidative stress on adult telomere length.

Spanish abstract Los telómeros son secuencias repetitivas de ADN que se encuentran al final de los cromosomas protegiéndolos de la degradación. Los telómeros han sido foco de intensa investigación ya que tener telómeros cortos predice un envejecimiento acelerado y una longevidad reducida en vertebrados. El estrés oxidativo se considera causante del acortamiento de los telómeros y, consecuentemente, una corta esperanza de vida. Entre las moléculas que luchan contra el estrés oxidativo, el glutatión está relacionado con numerosas vías metabólicas de otros antioxidantes. La literatura defiende que el estrés oxidativo podría desencadenar una respuesta hormética compensatoria, aumentando los niveles de glutatión y la longitud de los telómeros. En este trabajo testamos la relación entre los niveles de glutatión y la longitud de los telómeros en aves en condiciones de cautividad (diamantes mandarines; Taeniopygia guttata). Los niveles de glutatión fueron reducidos experimentalmente durante el desarrollo de las aves usando un inhibidor específico de la síntesis de glutatión (Buthionina sufolximina; BSO). El desempeño reproductivo de estas aves fue monitoreado en un aviario exterior durante los primeros meses de vida y la longevidad durante casi nueve años. Entre los individuos controles, los niveles de glutatión durante el desarrollo predijeron positivamente la longitud de los telómeros a edad adulta. Sin embargo, las hembras tratadas con BSO, pero no los machos, mostraron telómeros más largos a edad adulta que las hembras controles. Este hallazgo aparentemente contradictorio sugiere que las hembras desarrollaron una respuesta compensatoria. Tal compensación concuerda con los hallazgos anteriores obtenidos en la misma población: las hembras tratadas con BSO vieron aumentado su peso corporal a edad adulta, resultado no encontrado entre los machos. El tratamiento con BSO no afectó la longevidad o el desempeño reproductivo de ningún sexo. Sin embargo, los niveles de glutatión durante el desarrollo y la longitud de los telómeros a edad adulta predijeron interactivamente la longevidad de las hembras controles. Aquellas hembras con niveles bajos "naturales" (no manipulados) de glutatión cuando eran pollos pero que pudieron producir telómeros más largos a edad adulta vivieron más. Este resultado sugiere que la capacidad de desarrollar una respuesta hormética desencadenada por niveles bajos de glutatión durante el desarrollo puede mejorar la eficacia biológica a través de la longitud de los telómeros. De manera general, los resultados indicarían una relación específica del sexo entre los valores de glutatión y de telómeros. La actividad de la enzima telomerasa y los esteroides sexuales (estrógenos) son buenos candidatos para explicar este mecanismo dependiente del sexo que impulsa el impacto del estrés oxidativo sufrido durante el desarrollo en la longitud de los telómeros de adultos.