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. 2021 Dec 17:9:752352.
doi: 10.3389/fcell.2021.752352. eCollection 2021.

Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback

Mirre J P Simons  1 , Marion Sebire  2 , Simon Verhulst  3 , Ton G G Groothuis  3
Affiliations

Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback

Mirre J P Simons et al. Front Cell Dev Biol. .

Abstract

Costs of reproduction shape the life-history evolution of investment in current and future reproduction and thereby aging. Androgens have been proposed to regulate the physiology governing these investments. Furthermore, androgens are hypothesized to play a central role in carotenoid-dependent sexual signaling, regulating how much carotenoids are diverted to ornamentation and away from somatic maintenance, increasing oxidative stress, and accelerating aging. We investigated these relationships in male three-spined stickleback in which we elevated 11-ketotestosterone and supplied vitamin E, an antioxidant, in a 2 × 2 design. Androgen elevation shortened the time stickleback maintained reproductive activities. We suspect that this effect is caused by 11-ketotestosterone stimulating investment in current reproduction, but we detected no evidence for this in our measurements of reproductive effort: nest building, body composition, and breeding coloration. Carotenoid-dependent coloration was even slightly decreased by 11-ketotestosterone elevation and was left unaffected by vitamin E. Red coloration correlated with life expectancy and reproductive capacity in a quadratic manner, suggesting overinvestment of the individuals exhibiting the reddest bellies. In contrast, blue iris color showed a negative relationship with survival, suggesting physiological costs of producing this aspect of nuptial coloration. In conclusion, our results support the hypothesis that androgens regulate investment in current versus future reproduction, yet the precise mechanisms remain elusive. The quadratic relationships between sexual signal expression and aspects of quality have wider consequences for how we view sexual selection on ornamentation and its relationship with aging.

Keywords: aging; carotenoid; fecundity; sexual hormone; sexual selection; signaling; stickleback.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Results of the pilot experiment to determine resulting plasma concentrations of 11-ketotestosterone after treatment with different dosages of 11-keto-androstenedione.
FIGURE 2
FIGURE 2
11-ketotestosterone plasma concentrations in the main experiment regressed against residual testis mass (against body mass). Open dots and dashed regression line, 11-keto-androstenedione treated individuals; closed dots and solid line, controls.
FIGURE 3
FIGURE 3
Example of the automatic selection and thresholding used to obtain red and blue chroma of the nuptial coloration of the stickleback. Top shows the individual stickleback extracted from the picture, the middle part shows the selected pixels (in white) above the red chroma threshold, and the bottom part shows the extraction of the blue iris, also using chroma thresholding.
FIGURE 4
FIGURE 4
Period (in weeks) during which reproductive activities could be maintained was reduced in individuals in which 11-ketotestosterone was elevated (dashed line) compared to controls (closed line).
FIGURE 5
FIGURE 5
Survival (in days after the start of the experiment) plotted across the whole follow-up period, separated for 11-keto-androstenedione-treated individuals (dashed) and controls (solid). The breeding season from which data on coloration and nest building are presented lasted for 160 days of long photoperiod after the start of the experiment.
FIGURE 6
FIGURE 6
Breeding coloration plotted against the weeks after injections. Red chroma of the belly is plotted in the top panel and first increases during the breeding season to subsequently decline after an optimum. 11-Keto-androstenedione-treated animals have slightly less concentrated coloration of their bellies before and after the period of the optimum. The bottom panel shows blue iris coloration, which steadily declines during the breeding season irrespective of treatment.
FIGURE 7
FIGURE 7
Nesting intensity [amount of days extra material was added minus the time needed to complete a nest (days)] first increased during the breeding season and then declined. 11-Keto-androstenedione (open dots)-treated individuals showed in general reduced nesting intensity during the start of the breeding season.
FIGURE 8
FIGURE 8
Higher maximum red chroma achieved during the breeding season signaled higher reproductive capacity. However, the significance of the quadratic term suggests that in the reddest individuals, this relationship levels off or may even become negative.
See this image and copyright information in PMC

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