Oxidative Damage Increases With Reproductive Energy Expenditure and Is Reduced by Food-Supplementation

Abstract

A central principle in life-history theory is that reproductive effort negatively affects survival. Costs of reproduction are thought to be physiologically-based, but the underlying mechanisms remain poorly understood. Using female North American red squirrels (Tamiasciurus hudsonicus), we test the hypothesis that energetic investment in reproduction overwhelms investment in antioxidant protection, leading to oxidative damage. In support of this hypothesis we found that the highest levels of plasma protein oxidative damage in squirrels occurred during the energetically-demanding period of lactation. Moreover, plasma protein oxidative damage was also elevated in squirrels that expended the most energy and had the lowest antioxidant protection. Finally, we found that squirrels that were food-supplemented during lactation and winter had increased antioxidant protection and reduced plasma protein oxidative damage providing the first experimental evidence in the wild that access to abundant resources can reduce this physiological cost.

Artificial Light at Night Reduces Daily Energy Expenditure in Breeding Great Tits (Parus major)

“…On the other hand, when resources are plentiful animals might afford to work harder and, for instance, provide more food to their offspring (Tinbergen and Verhulst, 2000;Welcker et al, 2009) or invest more energy and time in territorial defense (Vehrencamp et al, 1989), thereby increasing their DEE. In addition, a potential cost of high DEE at the cellular level is the production of reactive oxygen species, which may lead to oxidative stress (Speakman et al, 2002;Selman et al, 2008;Fletcher et al, 2013; but see also Speakman and Selman, 2011). However, higher food availability can also increase the capacity of organisms to acquire and use anti-oxidants and thus limit oxidative stress (Giordano et al, 2015).…”

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 of Soay sheep ( Ovies aries ) which produced two surviving offspring in the previous spring, had a lower concentration of TBARS than females with one or no surviving offspring (Nussey et al., 2009). In contrast, in another cross‐sectional study, oxidative damage to proteins in lactating female North American red squirrels ( Tamiasciurus hudsonicus ) exceeded by 1.9 times that in nonbreeding females (Fletcher et al., 2013). Female northern elephant seals ( Mirounga angustirostris ), which undergo prolonged fasts during breeding, showed increases in oxidative damage to proteins (Sharick et al., 2015).…”

“…Overall, these five studies provided very mixed results on the role of oxidative stress in reproduction. However, they show that a cross‐sectional study does not necessarily exclude the demonstration of the costs (Fletcher et al., 2013) and a longitudinal study does not always demonstrate such costs (Vitikainen et al., 2016). …”

“…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). …”

“…An important question is whether this situation adequately mimics the situation in the field with respect to the factors that generate oxidative stress. However, studies conducted on wild animals in their natural environment, especially on mammals, that provide important information about their real costs of living, are still scarce (Bergeron et al., 2011; Christensen et al., 2015; Fletcher et al., 2013; Nussey et al., 2009; Sharick, Vazquez‐Medina, Ortiz, & Crocker, 2015). …”