Enzymatic antioxidants but not baseline glucocorticoids mediate the reproduction–survival trade-off in a wild bird

Abstract

The trade-off between reproductive investment and survival is central to life-history theory, but the relative importance and the complex interactions among the physiological mechanisms mediating it are still debated. Here we experimentally tested whether baseline glucocorticoid hormones, the redox system or their interaction mediate reproductive investment–survival trade-offs in wild great tits ( Parus major ). We increased the workload of parental males by clipping three feathers on each wing, and 5 days later determined effects on baseline corticosterone concentrations (Cort), redox state (reactive oxygen metabolites, protein carbonyls, glutathione peroxidase [GPx], total non-enzymatic antioxidants), body mass, body condition, reproductive success and survival. Feather-clipping did not affect fledgling numbers, chick body condition, nest provisioning rates or survival compared with controls. However, feather-clipped males lost mass and increased both Cort and GPx concentrations. Within feather-clipped individuals, GPx increases were positively associated with reproductive investment (i.e. male nest provisioning). Furthermore, within all individuals, males that increased GPx suffered reduced survival rates. Baseline Cort increases were related to mass loss but not to redox state, nest provisioning or male survival. Our findings provide experimental evidence that changes in the redox system are associated with the trade-off between reproductive investment and survival, while baseline Cort may support this trade-off indirectly through a link with body condition. These results also emphasize that plastic changes in individuals, rather than static levels of physiological signals, may mediate life-history trade-offs.

Physiological adjustments to high foraging effort negatively affect fecundity but not final reproductive output in captive zebra finches

“…Although some studies investigating the effects of increased workload on reproduction generally found a delay in the timing of reproduction (Deerenberg and Overkamp, 1999;Simons et al, 2014;Wiersma, 2005), many other studies failed to find evidence of impaired reproduction due to increased workload (Schmidt-Wellenburg et al, 2008;Tomotani et al, 2018). Additionally, some studies also found that increased workload during reproduction did not affect final reproductive output, but negatively impact body condition of the parents (Casagrande and Hau, 2018;Fletcher et al, 2013). A few studies in rodents even found positive effects of high activity level on reproduction (Vega et al, 2015;Zhang et al, 2018b), which is possibly due to mitochondrial hormesis (Zhang and Hood, 2016;Zhang et al, 2018c).…”

Understanding diversity in oxidative status and oxidative stress: the opportunities and challenges ahead

“…We need to measure multiple markers multiple times (avoiding anaemia) before and during an experiment if we aim to determine the dynamics of the individual's oxidative status and to detect biochemical oxidative stress. While baseline values of oxidative status markers provide information about constitutive levels, inducible levels reflect the individual physiological responsiveness to a given stressor (Dotan et al, 2004;Costantini, 2014;Casagrande and Hau, 2018). Furthermore, antioxidant enzyme activities and GSH need to be assessed more frequently in free-living animals because, as compared with some non-enzymatic antioxidants, their functions in the regulation of oxidative status are better known and may have fitness consequences (Norte et al, 2008;Koivula et al, 2011;Casagrande and Hau, 2018).…”

“…However, results appear more conflicting when we come to the role of oxidative stress in determining lifespan or reproductive outcomes (e.g. Alonso-Alvarez et al, 2004Isaksson et al, 2011b;Noguera et al, 2012;Stier et al, 2012;Costantini, 2014;Beaulieu et al, 2015;Costantini and Dell'Omo, 2015;Blount et al, 2016;Costantini et al, 2016Costantini et al, , 2017Herborn et al, 2016;Colominas-Ciuró et al, 2017;Marasco et al, 2017;Merkling et al, 2017;Boonekamp et al, 2018;Casagrande and Hau, 2018;Losdat et al, 2018;Viblanc et al, 2018;Vágási et al, 2019). It is not trivial to assess the ecological and evolutionary relevance of oxidative stress, particularly in free-ranging animals.…”

Acute aggressive behavior perturbates the oxidative status of a wild bird independently of testosterone and progesterone

“…Further, the concentration of enzymatic antioxidants (i.e., GPX) was not different between control and STI birds. The latter could be explained because GPX plays an important role in cellular detoxification of dROMs [59,60], which did not change after the STI, or by the fact that an up- or down-regulation of enzymatic defenses takes more than 20 minutes. On the other hand, aggressive behaviors can increase oxidative stress indirectly through an increase in testosterone levels [8,19,20].…”