Androgens and Immune Function in Male Alternative Reproductive Morphotypes of the Peacock Blenny Salaria pavo

Abstract

Species with alternative reproductive tactics offer the opportunity to analyse how behavioural and morphological traits are tuned to produce successfully competing phenotypes within one sex. In the teleost fish Salaria pavo, alternative reproductive tactics are sequential. The older ornamented males compete for access to females by guarding a cavity to which they attract females to spawn. Ornamented males that are found without a nest are called ‘floaters’. Younger mature males which are too small to compete with nest‐holders attempt to ‘sneak’ as female mimics into successful nests and release their sperm to fertilize freshly spawned eggs. The alternative tactics in S. pavo are associated with different levels of the androgens testosterone and 11‐ketotestosterone, which have been found to suppress immune function in several teleost fish. A field study was carried out to analyse the relationship between these reproductive tactics, androgens and blood levels of lymphocytes as a monitoring method of immune function. We expected highest investment in the immune system in sneakers because these have the lowest androgen levels and functionally because investing in self‐maintenance increases their future prospect to switch tactic and to reproduce as a nest‐holder. Indeed, the relative count of lymphocytes correlated negatively with body size and thus was highest in sneakers and lowest in nest‐holders. In concordance, 11‐ketotestosterone and testosterone levels were found to be higher in floaters and nest‐holders than in sneakers. However, no correlation was found between individual levels of testosterone or 11‐ketotestosterone and lymphocytes. Thus, a trade‐off between reproductive traits associated with high androgen levels and immunocompetence might exist at the level of alternative tactics but this might not be explained by acute immunosuppressive effects of circulating androgens.

Androgen responses to reproductive competition of males pursuing either fixed or plastic alternative reproductive tactics

“…This was also reported for bourgeois and parasitic males in the saddleback wrasse and rock-pool blenny (Hourigan et al, 1991;Oliveira et al, 2001c). In contrast, in the peacock blenny, both 11-KT and T levels were higher in floaters and nest holders than in sneaker males (Ros and Oliveira, 2009). This highlights the possibility that T responses in species with ARTs may be rather inconsistent (Mayer et al, 1990;Brantley et al, 1993;Cheek et al, 2000), as they may depend on the peculiar behavioural differences involved in the alternative reproductive tactics expressed in a species.…”

“…ARTs may be fixed for life, in which case individual males permanently differentiate into pursuing one of the tactics, or they may be plastic, when individual males may reversibly or irreversibly switch tactics during their lifetime . These different patterns have been shown to be associated with diverging hormone responses in several species with ARTs (Oliveira et al, 2001b;Ros et al, 2004;Knapp and Neff, 2007;Gonçalves et al, 2008;Ros and Oliveira, 2009;Saraiva et al, 2013).…”

Immunoecology of species with alternative reproductive tactics and strategies

“…At the peak of the reproductive period, 11to 43% (mean 25%) of males are M-(Fagundes, pers.obs.). Females visit several males and prefer to lay their eggs in nests that already have large broods (Ros & Oliveira, 2009) Ros et al (2006a) tested the ICHH in rock-pool blennies correlationally by measuring circulating androgens, lymphocyte ratios and primary antibody responses. Both 11ketotestosterone and testosterone were higher in M+ males than in M-males and lymphocyte numbers and humoral immunity were lower in M+ males than in M-males.…”

“…As a result older (M+) males might decrease production of naïve leukocytes which would be necessary for acquiring immunity to new pathogens. Therefore, the fact that if M+ males had lower lymphocyte blood cell counts and lower antibody responsiveness than M-males does not necessarily mean that they are more susceptible to disease (Ros & Oliveira, 2009). Under this scenario, the immune system improves with age, but using some measures of immunity, the exact opposite is true.…”

Does access to the bluestreak cleaner wrasse Labroides dimidiatus affect indicators of stress and health in resident reef fishes in the Red Sea?

“…These comprise a variety of cells involved in the production of specific antibodies, like T and B cells; and (3) all other cell types for calculating the total cell count= lymphocytes + granulocytes + thrombocytes+ erythrocytes. We report total leukocyte as percentage of the total cell count (see Ros et al, 2006;Ros and Oliveira, 2009) and lymphocyte and granulocyte counts as differential percentage (percentage of lymphocytes + granulocytes + thrombocytes). We further calculated the H-L ratio as the ratio of granulocytes over lymphocytes.…”