Regulation of immunocompetence by different androgen metabolites in a blenny with alternative reproductive tactics

Ros, Albert F. H.; Ferreira, Catarina; Santos, Ricardo Serrão; Oliveira, Rui Filipe

doi:10.1002/jez.a.349

Cited by 14 publications

(14 citation statements)

References 57 publications

(53 reference statements)

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“…However, androgen levels (T and KT) did not show the expected negative correlation with lymphocyte percentages. Overall, these results are in agreement with data obtained from a related blenny species, the Azorean rock‐pool blenny, P. parvicornis (Ros et al. 2006a,b), suggesting that a trade‐off between androgen‐dependent traits (morphotype) and immunocompetence may be present at the level of ARTs in blennies which is not likely explained by acute immunosuppressive effects of circulating androgens.…”

Section: Discussionsupporting

confidence: 89%

“…Granulocytes were scarce and left out of analyses (in bourgeois males: less than 0.1% of total blood cell count). We report lymphocyte counts as percentages of the total cell count (lymphocytes + granulocytes + thrombocytes + erythrocytes, see Ros et al. 2006a,b).…”

Section: Methodsmentioning

confidence: 99%

“…Alternative tactics in S. pavo are sequential and thus differ in both age and body size. In a closely related species, body size was found to be negatively correlated with leucocyte counts (Ros et al. 2006a,b).…”

Section: Methodsmentioning

confidence: 99%

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

Ros

Oliveira

2009

Ethology

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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.

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Section: Discussionsupporting

confidence: 89%

Section: Methodsmentioning

confidence: 99%

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

Ros

Oliveira

2009

Ethology

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“…Despite these inconsistencies, estrogens and estrogen-like endocrine disruptors appear to affect the balance of proliferation/apoptosis of lymphocytes. In contrast, androgens clearly exert an anti-proliferative effect on lymphocytes (Cook 1994;Slater and Schreck 1997;Saha et al 2004;Ros et al 2006) and affect IgM secretion (Hou et al 1999c;Saha et al 2004). Moreover, androgens are negatively correlated with plasma IgM during the reproductive cycle in rainbow trout (Suzuki et al 1997).…”

Section: Effects On Estrogens/androgens and Their Related Edcs On Immmentioning

confidence: 88%

The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review

2011

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During the last decade, a number of studies have shown that, in addition to their classically described reproductive function, estrogens and androgens also regulate the immune system in teleosts. Today, several molecules are known to interfere with the sex-steroid signaling. These chemicals are often referred to as endocrine disrupting contaminants (EDCs). We review the growing evidence that these compounds interfere with the fish immune system. These studies encompass a broad range of approaches from field studies to those at the molecular level. This integrative overview improves our understanding of the various endocrine-disrupting processes triggered by these chemicals. Furthermore, the research also explains why fish that have been exposed to EDCs are more sensitive to pathogens during gametogenesis. In this review, we first discuss the primary actions of sex-steroid-like endocrine disruptors in fish and the specificity of the fish immune system in comparison to mammals. Then, we review the known interactions between the immune system and EDCs and interpret the primary effects of sex steroids (estrogens and androgens) and their related endocrine disruptors on immune modulation. The recent literature suggests that immune parameters may be used as biomarkers of contamination by EDCs. However, caution should be used in the assessment of such immunotoxicity. In particular, more attention should be paid to the specificity of these biomarkers, the external/internal factors influencing the response, and the transduction pathways induced by these molecules in fish. The use of the well-known mammalian models provides a useful guide for future research in fish.

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“…However, there was no correlation between 11kT and immunity within each morphotype (Ros et al 2006a). Implant experiments indicated that the morphological effects are mediated by 11kT, whereas immunological effects seemed mediated by T, which led the authors to suggest that these effects might be decoupled in this species (Ros et al 2006b).…”

mentioning

confidence: 95%

An Experimental Test of the Immunocompetence Handicap Hypothesis in a Teleost Fish: 11‐Ketotestosterone Suppresses Innate Immunity in Three‐Spined Sticklebacks

Kurtz¹,

Kalbe²,

Langefors³

et al. 2007

The American Naturalist

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The immunocompetence handicap hypothesis (ICHH) provides a functional explanation for how sexual ornaments can provide honest signals of male quality. A key aspect of this hypothesis is that testosterone (T) has a bimodal effect: a higher T level enhances the expression of ornaments (increasing mating success and, ultimately, fitness); however, at the same time, it suppresses immune function. Tests of the latter assumption, which have focused mainly on aspects of adaptive immunity in birds, led to equivocal results. We performed a hormone-implant experiment in male three-spined sticklebacks (Gasterosteus aculeatus) to test the key assumptions of the ICHH in a fish, where the dominant circulating androgen is 11-ketotestosterone (11kT) rather than T. Males were implanted with 11-ketoandrostenedione, which is a natural precursor of 11kT. Each individual's circulating 11kT level, ornamentation, and immunocompetence were measured 2 weeks later. In addition, we quantified oxidative tissue damage because the ICHH has been hypothesized to work via oxidative stress. We found that the males' 11kT levels correlated positively with ornamentation but negatively with immunocompetence, in particular, measures of innate immunity. Moreover, there was a trend for fish with high 11kT levels to suffer more from oxidative stress. Thus, our data provide support for the ICHH.

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Regulation of immunocompetence by different androgen metabolites in a blenny with alternative reproductive tactics

Cited by 14 publications

References 57 publications

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

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

The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review

An Experimental Test of the Immunocompetence Handicap Hypothesis in a Teleost Fish: 11‐Ketotestosterone Suppresses Innate Immunity in Three‐Spined Sticklebacks

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