Immune activity suppresses reproduction in food‐limited female tree lizards Urosaurus ornatus

Abstract

Summary1. When resources are scarce, organisms are faced with critical challenges trying to optimize competing functions. Reproduction and immune function are both resource intensive and important to most species. Most studies have reported a down-regulation of immune function during reproduction. Conversely, it is unclear whether mounting an immune response can affect the reproductive process and few studies have examined competition for resources between these two processes. 2. Here we report evidence for direct competition for resources between the reproductive and immune systems in a vertebrate model system, the tree lizard ( Urosaurus ornatus ). We manipulated food intake in reproductive female tree lizards, where half of the females were undergoing cutaneous wound healing and the other half were not. We then measured reproductive investment in all animals and wound healing rate in all wounded animals. 3. We found that animals with unlimited access to food sustained both reproduction and immune function whereas animals maintained on a restricted diet were not. Specifically, when food was unlimited, females were able to invest in reproduction and heal their wounds. However, when food was limited, females forced to heal a cutaneous wound had significantly smaller follicles than their non-wounded counterparts. Under extreme food limitation (i.e. no food) both reproductive investment and wound healing were suppressed. 4. These results clearly demonstrate resource competition between the reproductive and immune systems, whereby physiological trade-offs between the two systems only arise when resources are limiting. Furthermore, this type of facultative regulation is adjustable and allows animals to respond to changing environmental conditions.

Relationships between metabolic status, corticosterone secretion and maintenance of innate and adaptive humoral immunities in fasted re-fed mallards

“…Likewise, it was shown that trade-offs between reproduction and immune capacity were only found when food resources were experimentally reduced in female zebra finches (Love et al, 2008) and female tree lizards (Urosaurus ornatus) (French et al, 2007a). Our results tend to support the so-called energy-based (or resource-driven) trade-off between immunity and life-history stages.…”

Timing of reproduction of a cold desert viperid snake from North America, the Great Basin rattlesnake (Crotalus lutosus)

“…hormone production) is largely controlled by environmental conditions, such as food availability (Ballinger, 1977;French et al, 2007), temperature and/or photoperiod (Marion, 1970;Pancharatna and Patil, 1997;Hilder and Pankhurst, 2003;Yoneda and Wright, 2005). Female C. lutosus significantly reduces feeding during follicular development and pregnancy (Glaudas, unpublished data), suggesting that this species mainly rely on stored body fat to fuel reproduction (i.e., capital breeder; Jö nsson, 1997; Bonnet et al, 1998).…”

Factors Influencing Ectoparasitism on Western Fence Lizards (Sceloporus Occidentalis): Host Sex, Testosterone, Reproductive Condition, and Behavior

“…Under food-limited conditions the reproductive system draws energy from the immune system to support the costly process of vitellogenesis, which in turn may benefit ectoparasites on the host because of decreased host immune response. However, as shown by French et al (2007French et al ( , 2007aFrench et al ( , 2007b) the immune response of vitellogenic female lizards is only impacted under conditions where there is not enough energy to support both immune and reproductive systems. The studies above found a decrease in immune function in vitellogenic lizards only when they were energy-limited; when food was available ad libitum, no difference were observed.…”

“…Consequently, initiating a robust immune response may prevent ticks from feeding to repletion or at least slow down the rate at which ticks feed. Vitellogenesis is an energetically expensive process (Braña et al, 1992;Bonnet et al, 1994) and if a female individual does not have appropriate resources to support both reproductive and immune systems during this time, then a trade-off may occur, leading to suppression of the immune response (French et al, 2007(French et al, , 2007a(French et al, , 2007bFrench, 2008). This may enhance the ability and speed of attached ticks to feed to repletion.…”

“…When female birds have larger clutch sizes their immune function is significantly lowered (Norris et al, 1994;Nordling et al, 1998;Cichon et al, 2001). In female tree lizards (Urosaurus ornatus), immune activity is suppressed during vitellogenesis, but only under conditions when lizards are food-limited (French et al, 2007(French et al, , 2007a(French et al, , 2007bFrench, 2008). Immunosuppression caused by increased reproductive effort may result in increased parasite intensities, as observed in greater mouse-eared bats (Myotis myotis, Christe et al, 2000), collared fly catchers (Ficedula albicollis, Nordling et al, 1998), and common lizards (Lacerta vivipara, Sorci et al, 1996).…”