The Impact of Exposure to a Novel Female on Symptoms of Infection and on the Reproductive Axis

Abstract

Background/Aim: Sickness behaviors are the behavioral alterations animals exhibit during the course of an infection, often accompanied by reduced reproductive activity. Adopting sickness behaviors may aid in overcoming the infection, by diverting energy from routine activities towards enhancement of the immune system. Nonetheless, sickness behaviors are plastic, being influenced by specific environmental and social circumstances. Here, we tested whether the presentation of a novel female to males suffering from a simulated infection could impact the behavioral effects of sickness, the reproductive axis, or both. Methods: Male zebra finches were housed in isolation and injected intramuscularly with lipopolysaccharide or saline. Behaviors were recorded before (3 h before injection) and after (3.5 h after injection) addition of a novel female to the cage for 30 min. Four hours after injection, we collected the brain and testis for the analysis of important reproductive axis modulators, gonadotropin-releasing hormone, and gonadotropin-inhibitory hormone, and to quantify gene expression of a proinflammatory cytokine involved in the regulation of sickness behaviors [interleukin (IL)-1β]. Testosterone was quantified in the plasma. Results: The presence of a novel female diminished sickness behaviors and induced alterations in the reproductive axis within 30 min, with no associated changes in brain gene expression of IL-1β. Social environment itself altered brain gene expression of IL-1β. Conclusions: Male zebra finches prioritize the opportunity to mate versus investment in recovery from an infection, as determined by reduced expression of sickness behaviors when a potential mate was present. The behavioral effects of IL-1β appear to be context dependent in this species.

Birds receiving extra carotenoids keep singing during the sickness phase induced by inflammation

“…We found that an inflammatory stimulus, such as LPS, can cause a significant decrease in song rate, in accordance with previous results obtained in other species Munoz et al 2010;Lopes et al 2013). Since the activation of the immunoresponse is expensive (see BIntroduction^), a negative relationship between the expression of a demanding trait, such as birdsong, and an inflammatory response was expected (Hasselquist and Nilsson 2012).…”

“…It is possible that the mitigated sickness syndrome mirrored the suppression of the immune response expressed at the physiological level and that starlings fed with extra carotenoids could have switched from a costly inflammatory response to a highly specific, but less costly, antibody production (Lee 2006), accelerating the recovery processes. Nevertheless, another scenario is also possible as the behavioural symptoms of sickness induced by LPS can be suppressed without altering the inflammatory response (Lopes et al 2013). Indeed, Lopes and colleagues detected the presence of specific inflammatory interleukins both when birds displayed sickness behaviour and when they did not.…”

“…Although behavioural traits were not considered in their study, a consequent mitigation of an energy-saving behaviour, such as sickness, can be predicted. Nevertheless, independently from carotenoids, it is not so evident that a suppression of inflammation is always translated in suppression of sickness behaviour and vice versa (Lopes et al 2013). …”

When is it socially acceptable to feel sick?

“…There is also indication that immune challenged male zebra finches (Taeniopygia guttata) are affected by the presence of a potent sexual stimulus. When presented with a novel female, animals suffering from a simulated acute infection were able to not only behave similarly to controlinjected birds, but also to activate their reproductive axis and to court females to the same extent as the controls [35]. However, experiments in male mice show an almost opposite effect, with an increase in depressive-like behaviours when presented with a receptive female, as compared to control males kept in isolation, as well as elimination of mating behaviour, as compared to control-injected mice [36].…”

The Signaling Theory of Symptoms

“…Further, avoidant behavior of conspecifics may contribute to these social costs (Avitsur, Cohen, & Yirmiya, 1997). In certain situations, opportunity costs are so high that the immune response is suppressed in order to enable normal behavior (Aubert, Goodall, Dantzer, & Gheusi, 1997;Lopes, 2014;Lopes et al, 2013;Lopes, Adelman, Wingfield, & Bentley, 2012;Owen-Ashley & Wingfield, 2006). For example, male zebra finches whose immune systems were artificially provoked, display symptoms of illness when they are housed in a single cage, but when housed in a group cage, they do not display these symptoms (Lopes et al, 2012).…”