Photoperiod differentially affects energetics of immunity in pregnant and lactating Siberian hamsters (<i>Phodopus sungorus</i>)

Drazen, Deborah L.; Trasy, Anjali; Nelson, Randy J.

doi:10.1139/z03-120

Cited by 21 publications

(24 citation statements)

References 43 publications

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“…A growing body of evidence suggests that raising an immune response is also energetically costly, and may play a key role in physiological trade-offs (Lochmiller and Deerenberg, 2000;Martin et al, 2008) in both mammals (Christe et al, 2000;Drazen et al, 2003) and birds (Nordling et al, 1998;Knowles et al, 2009;Christe et al, 2012). Immunosuppression caused by reproduction could be the result of an energetic trade-off between reproductive demands and immune function, which is in line with the standard predictions of life history theory (Stearns, 1992).…”

Section: Introductionsupporting

confidence: 64%

Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent

Yang

Wang

et al. 2013

Journal of Experimental Biology

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SUMMARYLife history parameters appear to be traded off against each other, but the physiological mechanisms involved remain unclear. One hypothesis is that potentially energetically costly processes such as immune function and protection from oxidative stress may be compromised during reproductive attempts because of selective resource allocation. Lower temperatures also impose energy costs, and hence allocation decisions might be more pronounced when animals are forced to reproduce in the cold. Here, we experimentally tested whether reproduction at different ambient temperatures was associated with elevated oxidative stress and suppressed immune function in Mongolian gerbils (Meriones unguiculatus). Using a variety of different markers for both immune function and oxidative stress, we found that some measures of immune function (serum bactericidal capacity and size of the thymus) were significantly suppressed, while some measures of oxidative protection [serum superoxide dismutase (SOD) activity and glutathione peroxidase (GPx) activity] were also reduced, and a marker of oxidative damage (protein carbonyls in serum) was increased in lactating compared with non-reproductive gerbils. These changes were in line with the selective resource allocation predictions. However, the phytohaemagglutinin response and serum total immunoglobulin (IgG) were not suppressed, and other markers of oxidative damage [malondialdehyde (MDA) (TBARS) and protein carbonyls in the liver] were actually lower in lactating compared with non-reproductive gerbils, consistent with increased levels of SOD activity and total antioxidant capacity in the liver. These latter changes were opposite of the expectations based on resource allocation. Furthermore, other measures of protection (GPx levels in the liver and protein thiols in both serum and liver) and damage [MDA (TBARS) in serum] were unrelated to reproductive status. Ambient temperature differences did not impact on these patterns. Collectively, our results indicated that the inferred effects of reproduction on immunosuppression and oxidative damage, and hence support or otherwise for particular physiological mechanisms that underpin life history trade-offs, are critically dependent on the exact markers and tissues used. This may be because during reproduction individuals selectively allocate protection to some key tissues, but sacrifice protection of others. Supplementary material available online at

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Section: Introductionsupporting

confidence: 64%

Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent

Yang

Wang

et al. 2013

Journal of Experimental Biology

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“…Most studies across mammalian species demonstrate decreased immunity, including production of certain antibodies, during pregnancy (Weinberg 1984;Medina et al 1993). In fact, previous studies in Siberian hamsters show decreased anti-KLH IgM response during pregnancy (Drazen et al 2003). We neither observed any pregnancy-related decrease, nor any change in response to increased litter size in leptin-treated females (either IgG or IgM; figure 4).…”

Section: Discussioncontrasting

confidence: 68%

“…Immune function is suppressed during breeding stages across a wide range of species, concurrent with increased energy expenditure required for courtship, territorial defence or pregnancy (Cichon et al 2001;Drazen et al 2003; for review see Zuk & Stoehr 2002). For example, immune function is suppressed during pregnancy and lactation in the Siberian hamster (Phodopus sungorus) (Drazen et al 2003).…”

Section: Introductionmentioning

confidence: 99%

“…For example, immune function is suppressed during pregnancy and lactation in the Siberian hamster (Phodopus sungorus) (Drazen et al 2003). Moreover, changes in sex steroid hormones, such as testosterone and oestradiol, that occur during reproduction can exert pronounced effects on various components of the immune system (Saino et al 1995;Casto et al 2000;Greives et al 2006).…”

Section: Introductionmentioning

confidence: 99%

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Leptin increases maternal investment

et al. 2009

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The primary goal of virtually all organisms is to produce genetic offspring, thereby passing on their genes to future generations. Offspring production, however, is limited by available resources within an environment. Moreover, distributing sufficient energy among competing physiological systems is challenging and can result in trade-offs between self-maintenance and offspring investment when resources are limited. In the current study, we tested the hypothesis that the adipose hormone leptin is involved in mediating energetic trade-offs between competing physiological systems. Specifically, we tested the effects of elevated maternal leptin on investment into offspring production versus self maintenance (immune function), in the Siberian hamster (Phodopus sungorus). The current study provides the first evidence that leptin serves as a signal to mothers of available energy resulting in epigenetic effects. Therefore, elevated leptin allows females to retain more embryos to parturition, and rear more offspring to weaning via reduced maternal infanticide. Innate immune response was suppressed seemingly as a result of these enlarged litters, suggesting that the observed fitness increase is not without costs to the mother. Collectively, these findings suggest that leptin plays a critical role in allowing mothers to determine how much energy to invest in the production and care of young versus self-maintenance.

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“…Additional factors may be the consequences of reproduction for oxidative stress (Costantini, 2008;Speakman, 2008;Dowling and Simmons, 2009;Monaghan et al, 2009;Selman et al, 2012) (but see Speakman and Selman, 2011) and immune function (Christe et al, 2000;Christe et al, 2011;Drazen et al, 2003). Among mammals, studies of the impact of reproduction on oxidative stress have generated mixed results, with some field studies, using serum or plasma, indicating increased damage as a consequence of reproduction (Bergeron et al, 2011;Fletcher et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Limits to sustained energy intake. XV. Effects of wheel running on the energy budget during lactation

Zhao

Król

Moille

et al. 2013

Journal of Experimental Biology

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SUMMARYThe capacity of animals to dissipate heat may constrain sustained energy intake during lactation. We examined these constraints at peak lactation in MF1 mice that had ad libitum access to food, or that had to run a pre-set target on running wheels to obtain ad libitum access to food. The voluntary distance run decreased sharply during pregnancy and peak lactation. When lactating females were provided with 80% of their estimated food requirements, and had to run pre-set distances of 2, 4 or 6km before given access to additional ad libitum food, most of them did not complete the running target during late lactation and the mice with the highest targets failed to reach their targets earlier in lactation. There were consequently significant group differences in asymptotic food intake (2km, 16.97±0.40gday ) and weaned litter masses (2km, 71.11±2.39g; 4km, 54.63±4.28g and 6km, 47.18±2.46g). When the females did run sufficiently to gain ad libitum food access, their intake did not differ between the different distance groups or from controls that were not required to run. Thus, despite being physically capable of running the distances, mice could not exercise sufficiently in lactation to gain regular ad libitum access to food, probably because of the risks of hyperthermia when combining heat production from exercise with thermogenesis from lactation. Supplementary material available online at

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Photoperiod differentially affects energetics of immunity in pregnant and lactating Siberian hamsters (Phodopus sungorus)

Cited by 21 publications

References 43 publications

Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent

Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent

Leptin increases maternal investment

Limits to sustained energy intake. XV. Effects of wheel running on the energy budget during lactation

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