Is reproduction costly? No increase of oxidative damage in breeding bank voles

Abstract

SUMMARYAccording to life-history theory, investment in reproduction is associated with costs, which should appear as decreased survival to the next reproduction or lower future reproductive success. It has been suggested that oxidative stress may be the proximate mechanism of these trade-offs. Despite numerous studies of the defense against reactive oxygen species (ROS) during reproduction, very little is known about the damage caused by ROS to the tissues of wild breeding animals. We measured oxidative damage to lipids and proteins in breeding bank vole (Myodes glareolus) females after rearing one and two litters, and in non-breeding females. We used bank voles from lines selected for high maximum aerobic metabolic rates (which also had high resting metabolic rates and food intake) and non-selected control lines. The oxidative damage was determined in heart, kidneys and skeletal muscles by measuring the concentration of thiobarbituric acid-reactive substances, as markers of lipid peroxidation, and carbonyl groups in proteins, as markers of protein oxidation. Surprisingly, we found that the oxidative damage to lipids in kidneys and muscles was actually lower in breeding than in non-breeding voles, and it did not differ between animals from the selected and control lines. Thus, contrary to our predictions, females that bred suffered lower levels of oxidative stress than those that did not reproduce. Elevated production of antioxidant enzymes and the protective role of sex hormones may explain the results. The results of the present study do not support the hypothesis that oxidative damage to tissues is the proximate mechanism of reproduction costs.

Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

“…Also, the analysis limited to the large litters (4-7 pups), i.e. as large as or larger than the mean litter size in bank voles (about 4 pups; Ołdakowski et al, 2012), showed that final mean pup mass decreased with litter size (Table 1). Thus, females nursing large litters were at least close to a ceiling limiting their reproductive performance.…”

Plasma markers of oxidative stress are uncorrelated in a wild mammal

“…2008; who found no significant effects of lifelong cold exposure on mortality, oxidative damage, or AOX protection in captive short‐tailed field voles ( Microtus agrestis ); Ołdakowski et al. 2012; who found no effect of reproduction on oxidative damage to heart, kidney, or skeletal muscle in captive bank voles ( Myodes glareolus ); and Brzęk et al. 2014; who found no effect of reproduction on oxidative damage to lipids in two lines of laboratory mice ( Mus musculus ), selected either for high basal metabolic rate (H‐BMR) or low basal metabolic rate (L‐BMR)).…”

Oxidative damage and antioxidant defense are assay and tissue‐dependent both in captive and wild‐caught bank voles (Myodes glareolus) before and after reproduction

“…Females which weaned two litters had unaltered oxidative damage or lower damage (TBARS in kidneys and muscles) in relation to nonbreeding females (Ołdakowski et al., 2012). In another study, where females were forced to wean four consecutive manipulated (either enlarged or decreased) litters, these two groups of breeding females did not differ and had lower damage levels (TBARS in the liver, carbonyls in the liver and the heart) or unaltered levels of oxidative damage compared with nonreproducing females (Ołdakowski et al., 2015).…”

“…The idea that oxidative damage (to lipids, proteins, and DNA) is a consequence of reproductive effort has been extensively studied in recent years, but has received mixed support (Blount, Vitikainen, Stott, & Cant, 2016; Metcalfe & Monaghan, 2013; Monaghan, Metcalfe, & Torres, 2009; Selman, Blount, Nussey, & Speakman, 2012; Speakman & Garratt, 2013; Speakman et al., 2015). The general picture from studies on various species is very diverse: from an increase in the oxidative stress during reproduction (Alonso‐Alvarez et al., 2004; Bergeron et al., 2011; Fletcher et al., 2013) through the lack of significant differences between breeders and nonbreeders (Nussey, Pemberton, Pilkington, & Blount, 2009; Vitikainen et al., 2016), to the decrease in oxidative stress in breeding individuals (Costantini, Casasole, & Eens, 2014; Garratt, Pichaud, King, & Brooks, 2013; Garratt et al., 2011; Ołdakowski, Wasiluk, Sadowska, Koteja, & Taylor, 2015; Ołdakowski et al., 2012). …”

“…They can be easily adapted to breeding in laboratory conditions (Sadowska, Baliga‐Klimczyk, Chrząścik, & Koteja, 2008). In the first experiment (Ołdakowski et al., 2012), bank vole females were allowed to produce one or two litters, and used females without access to males as a control group. In the second experiment (Ołdakowski et al., 2015), we manipulated the reproductive effort of bank vole females by either increasing or decreasing litter size in four consecutive litters and nonbreeding females were controls.…”