Interacting effects of early dietary conditions and reproductive effort on the oxidative costs of reproduction

Abstract

The hypothesis that oxidative damage accumulation can mediate the trade-off between reproduction and lifespan has recently been questioned. However, in captive conditions, studies reporting no evidence in support of this hypothesis have usually provided easy access to food which may have mitigated the cost of reproduction. Here, I test the hypothesis that greater investment in reproduction should lead to oxidative damage accumulation and telomere loss in domestic zebra finches Taeniopygia guttata. Moreover, since the change or fluctuation in diet composition between early and late postnatal period can impair the ability to produce antioxidant defences in zebra finches, I also tested if early nutritional conditions (constant vs fluctuating early diet) influenced the magnitude of any subsequent costs of reproduction (e.g., oxidative damage and/or telomere shortening). In comparison to pairs with reduced broods, the birds that had to feed enlarged broods showed a higher level of oxidative DNA damage (8-OHdG), but brood size had no effect on telomeres. Fluctuating early diet composition reduced the capacity to maintain the activity of endogenous antioxidants (GPx), particularly when reproductive costs were increased (enlarged brood). The decline in GPx in birds feeding enlarged broods was accompanied by a change in bill colouration. This suggests that birds with lower endogenous antioxidant defences might have strategically increased the mobilization of antioxidants previously stored in other tissues (i.e., bill and liver) and thus, preventing an excessive accumulation of damage during reproduction.

Are trade‐offs really the key drivers of ageing and life span?

“…Christe, Glaizot, Strepparava, Devevey, & Fumagalli, 2012), reproduction was found to have no effect on free-ranging female Soay sheep oxidative damage levels (Nussey, Pemberton, Pilkington, & Blount, 2009) and little effect in eastern chipmunks (Bergeron et al, 2011). In birds, several experimental studies demonstrate that reproduction does decrease oxidative resistance (Alonso-Alvarez et al, 2004;Wiersma, Selman, Speakman, & Verhulst, 2004) in a condition-dependent way (Noguera, 2017), leading to short-term mortality rather than a longterm change in longevity prospects (Alonso-Alvarez et al, 2006). This emphasizes the difficulty arising when trying to relate apparent CoR with the disposable soma theory (Monaghan et al, 2009).…”

Maternal oxidative stress and reproduction: Testing the constraint, cost and shielding hypotheses in a wild mammal

“…Recently, oxidative stress has been suggested as a proximate mechanism that underlies variation in fitness related to breeding effort (Alonso-Alvarez, Bertrand, Faivre, & Sorci, 2007;Alonso-Alvarez et al, 2004;Bize, Devevey, Monaghan, Doligez, & Christe, 2008;Fletcher et al, 2012;Monaghan, Metcalfe, & Torres, 2009;Noguera, 2017;Stier, Reichert, Massemin, Bize, & Criscuolo, 2012). This proposition stems from the notion that when adults are reproducing, increased metabolism should lead to increased oxidative stress as a consequence of enhanced mitochondrial activity during ATP synthesis (Raha & Robinson, 2000).…”

Divergent patterns of telomere shortening in tropical compared to temperate stonechats

“…Reproduction, especially parental care, is energetically costly (Nilsson, 2002), can lead to oxidative DNA damage (Noguera, 2017) and potentially increased telomere loss (Heidinger et al, 2012;Reichert et al, 2014 Reproduction, especially parental care, is energetically costly (Nilsson, 2002), can lead to oxidative DNA damage (Noguera, 2017) and potentially increased telomere loss (Heidinger et al, 2012;Reichert et al, 2014 …”

“…In contrast to our predictions, tropical and temperate stonechats had telomeres of similar length during their first breeding season and as adults. Reproduction, especially parental care, is energetically costly (Nilsson, 2002), can lead to oxidative DNA damage (Noguera, 2017) and potentially increased telomere loss (Heidinger et al, 2012;Reichert et al, 2014). Our previous comparative studies on hormone levels and mating behavior in tropical and temperate stonechats have shown that territorial aggression is accompanied by a peak in testosterone and corticosterone concentrations during nest-building in both temperate and tropical male stonechats (Apfelbeck, Helm, et al, 2017;Apfelbeck, Mortega, et al, 2017…”

“…Furthermore, in tropical species, reproductive workload is reduced as they lay smaller clutches, thereby caring for fewer young and expending less energy than temperate birds (Nilsson, 2002;Tieleman et al, 2006). Thus, they may reduce high levels of oxidative stress (Noguera, 2017) and potential telomere loss associated with breeding (Reichert et al, 2014). In addition, tropical songbirds seem to have lower post-natal metabolic rates and slower, more sustained growth despite similar nestling times than temperate birds (Martin, 2015;Ton & Martin, 2016).…”