Reproduction Is Associated with a Tissue-Dependent Reduction of Oxidative Stress in Eusocial Female Damaraland Mole-Rats (Fukomys damarensis)

Abstract

Oxidative stress has been implicated as both a physiological cost of reproduction and a driving force on an animal's lifespan. Since increased reproductive effort is generally linked with a reduction in survival, it has been proposed that oxidative stress may influence this relationship. Support for this hypothesis is inconsistent, but this may, in part, be due to the type of tissues that have been analyzed. In Damaraland mole-rats the sole reproducing female in the colony is also the longest lived. Therefore, if oxidative stress does impact the trade-off between reproduction and survival in general, this species may possess some form of enhanced defense. We assessed this relationship by comparing markers of oxidative damage (malondialdehyde, MDA; protein carbonyls, PC) and antioxidants (total antioxidant capacity, TAC; superoxide dismutase, SOD) in various tissues including plasma, erythrocytes, heart, liver, kidney and skeletal muscle between wild-caught reproductive and non-reproductive female Damaraland mole-rats. Reproductive females exhibited significantly lower levels of PC across all tissues, and lower levels of MDA in heart, kidney and liver relative to non-reproductive females. Levels of TAC and SOD did not differ significantly according to reproductive state. The reduction in oxidative damage in breeding females may be attributable to the unusual social structure of this species, as similar relationships have been observed between reproductive and non-reproductive eusocial insects.

Oxidative shielding and the cost of reproduction

“…For example, most studies in the meta‐analyses that reported malondialdehyde as a marker of oxidative damage used a spectrophotometric assay that has been criticised for lack of specificity (reviewed by Monaghan et al, ; Selman et al, ), while a few recent studies have used a more precise HPLC method (e.g. Cram et al, ; Schmidt et al, ). Across all tissues and all markers, effect sizes were fairly consistent ( I 2 = 28%) for the relationship between reproductive effort and oxidative damage, while having a high level of heterogeneity ( I 2 = 81%) for the association between reproductive state and oxidative damage.…”

Reproduction is not costly in terms of oxidative stress

“…In wild-derived house mice, the damage to proteins in heart and skeletal muscles did not differ between nonreproducing females and those feeding enlarged or reduced litters, whereas in the liver, the damage either did not differ between these groups or was even decreased in the group with enlarged litters (Aloise Garratt et al, 2013). The results of the few studies on wild-derived small rodents showed that the damage to liver and other organs was unaffected or diminished by rearing nonmanipulated litters (Garratt et al, 2011;Ołdakowski et al, 2012;Schmidt et al, 2014). Interestingly, however, increased damage to proteins was found in the blood serum of reproducing females, even though the same studies showed no increased damage in the organs (Yang et al, 2013;Plumel et al, 2014;Xu et al, 2014).…”

Oxidative stress and life histories: unresolved issues and current needs

“…; Schmidt et al. ). The biological relevance of this diversity in response is unclear and has often been explained by individual, species, tissue or assay differences, and the difference between studies in the laboratory and field (see Themes 2 and 3 below).…”

“…Much of this research has focussed on mammals, mostly rodents, and almost exclusively on females. While some mammalian studies have supported the idea that investment in offspring production (during pregnancy and lactation) causes oxidative damage (Sainz et al 2000;Bergeron et al 2011;Stier et al 2012;Fletcher et al 2013), others have found no effect or that oxidative damage is actually reduced in lactating compared to nonreproducing females (Garratt et al 2011(Garratt et al , 2013Oldakowski et al 2012;Schmidt et al 2014). The biological relevance of this diversity in response is unclear and has often been explained by individual, species, tissue or assay differences, and the difference between studies in the laboratory and field (see Themes 2 and 3 below).…”