Trade-offs between the Reproductive and Immune Systems: Facultative Responses to Resources or Obligate Responses to Reproduction?

Abstract

A major challenge in biology is understanding how organisms partition limited resources among physiological processes. For example, offspring production and self-maintenance are important for fitness and survival, yet these critical processes often compete for resources. While physiological trade-offs between reproduction and immune function have been documented, their regulation remains unclear. Most current evidence suggests that physiological changes during specific reproductive states directly suppress various components of the immune system; however, some studies have not found this clear relationship. We performed two experiments in female tree lizards (Urosaurus ornatus) that demonstrate the presence of trade-offs between the reproductive and immune systems under controlled laboratory conditions. These results also support the hypothesis that these trade-offs are a facultative response to resource availability and are not obligatory responses to physiological changes during reproduction. We found that (1) experimentally increasing reproductive investment under limited resources resulted in suppressed immune function and (2) experimentally limiting resources resulted in immunosuppression but only during resource costly reproductive activities. There seems to be a critical balance of resources that is maintained between multiple processes, and changes in the balance between energy intake and output can have major consequences for immune function.

How do host sex and reproductive state affect host preference and feeding duration of ticks?

“…This again suggests that questing ixodid ticks may be unable to detect intraspecific differences in host physiological condition prior to attachment, or that reproductive condition alone does not negatively affect tick feeding success, and so there is no difference in host preference. We had expected more ticks to choose vitellogenic female lizards because vitellogenesis is an energetically costly process (French et al 2007a;Tinkle 1969;, and under limited resources can lead to a reproductiveimmune trade-off (Cichon et al 2001;Nordling et al 1998;Norris et al 1994) and increased parasite loads (Christe et al 2000;Nordling et al 1998;Sorci et al 1996). However, in female tree lizards (U. ornatus), immune activity was suppressed during vitellogenesis only under food-limited conditions (French and Moore 2008;French et al 2007a, b, c).…”

“…This trade-off could lead to increased parasite burdens on males with high T concentrations. In females of oviparous species, peak reproductive effort occurs during vitellogenesis (French et al 2007a;Tinkle 1969; during which vitellogenin production diverts energy to yolk production. This process is energetically costly and can negatively impact immune function (Cichon et al 2001;Nordling et al 1998;Norris et al 1994).…”

Free-Ranging Little Brown Myotis (Myotis lucifugus) Heal from Wing Damage Associated with White-Nose Syndrome

“…Thus, bats may experience energetic trade-offs by allocating more energy to regenerating lost tissue rather than to other important processes such as reproducing, mounting an immune response to challenges other than wound healing, or migration (Bernardo and Agosta 2005). A trade-off between reproduction and immune function has been shown in a number of vertebrate taxa, including small mammals (French et al 2007(French et al , 2009). If limited energy resources are allocated to repair wing tissue, then bats will face increased risks to survival and reproduction during the early weeks of the active season, a trade-off that would be exacerbated by low ambient temperatures (increasing thermoregulatory costs) and reduced insect availability during the spring in New England (Hoying and Kunz 1998).…”

Leptin, a neuroendocrine mediator of immune responses, inflammation, and sickness behaviors

“…For instance, female tree lizards that are yolking eggs (the most energetically expensive component of reproduction in this species) and provided with restricted access to food under laboratory conditions take twice as long to heal a wound as compared with non-reproductive females provided a similarly restricted diet. When food is provided ad libitum, however, there is no difference in the wound healing time between the reproductive and non-reproductive groups (French et al, 2007). Clearly, balancing these trade-offs among competing physiological systems via appropriate allocation of energetic resources can be critical for maximizing an animal's current health, survival, and reproductive success.…”