Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in Red Bishops Euplectes orix

Abstract

The immunocompetence handicap hypothesis (ICHH) posits that the hormone testosterone mediates a trade-off between investment in reproduction and immunological condition. In this study, we tested the ICHH in the Red Bishop Euplectes orix, a polygynous weaverbird. Males of this strongly sexually dimorphic species show an elaborate courtship display to attract females and compete aggressively with other males for nesting sites in breeding colonies. We experimentally elevated testosterone levels in breeding male Red Bishops kept in an aviary with a subcutaneous implantation of testosterone-releasing pellets. We then compared behaviour, development of territory size and immunological condition (as assessed through a white blood cell count) of the experimental group with a control group treated with placebos. In addition, we measured the primary and secondary response to phytohaemagglutinin (PHA) to investigate the effect of testosterone on both innate and acquired immunity. Males with elevated levels of testosterone enlarged their territories and conducted more courtship behaviour, while showing a decrease in health, expressed by an increased heterophil ⁄ lymphocyte ratio compared with the control group. Males of the control group showed an increase of the secondary response to PHA, as expected under the assumption that repeated exposure to an antigen enhanced the immune response due to acquired immunity. However, males with experimentally increased testosterone levels did not show such an enhanced immune response in the secondary PHA test (although sample size and power of the statistical tests were low), indicating that testosterone treatment might directly or indirectly suppress some component of the acquired immune response.

Testosterone Affects Song Modulation during Simulated Territorial Intrusions in Male Black Redstarts (Phoenicurus ochruros)

“…Other correlational and experimental studies with testosterone treatment failed to find effects on structural song parameters [29], [32], [33]. Studies that implant birds with testosterone may be problematic, because especially immediately after implantation testosterone may circulate in pharmacological doses [34], [35]. It is thus questionable whether manipulations exclusively within the physiological range of testosterone would reveal similar results.…”

Heterogeneity in pathogen transmission: mechanisms and methodology

“…In addition to suppressing immune function, variation in testosterone levels may alter male contact rates, activity patterns, space use and home range size, which may enhance or reduce opportunities for pathogen transmission (Grear, Perkins & Hudson ; Edler et al . ; Fuxjager et al . ).…”

Hormones and the neuromuscular control of courtship in the golden-collared manakin (Manacus vitellinus)

“…The golden-collared manakin may therefore stand in contrast to other lekking males in temperate regions, as testosterone levels remain elevated in males of these species throughout the entire displaying season, even though the season is much shorter (∼2 or 3 weeks) (Lisano and Kaennamer, 1977; Alatalo et al, 1996). Although somewhat controversial, prolonged high testosterone concentrations may be costly to males, such as in reduced immune function and increased oxidative stress (Folstad and Karter, 1992; Roberts et al, 2004; Mougeot et al, 2009; Edler et al, 2011) so manakins may need to limit such costs by reducing peripheral testosterone secretion. One possibility is that aggressive or competitive interactions between and among males within a lek, or even sexual interactions with females, produce transient pulses in circulating testosterone that 58 do not always detect but which serve to maintain testosterone-dependent properties in males at this time of year.…”