Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback.

Mirre J P Simons,Ton G G Groothuis,Marion Sebire,Simon Verhulst

doi:10.3389/fcell.2021.752352

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.

Highlights

Organisms evolve to optimize allocation of resources between different physiological processes to maximize fitness
We purposefully studied the consequences of androgens on the reproductive phase in which males display and attract females, as we were interested in trade-offs with carotenoiddependent signaling
11-Ketotestosterone elevation decreased our proxy for future reproductive success, the length that reproductive activities are maintained

Summary

Introduction

Organisms evolve to optimize allocation of resources between different physiological processes to maximize fitness Such resource-based trade-offs are central to life-history theory (Stearns, 1989) and have been adopted throughout biology, including the biology of aging (Maklakov and Chapman, 2019). The most direct test of these “costs of reproduction” is to increase reproductive effort experimentally and measure the long-term fitness consequences for the parents In birds, this approach, by manipulating clutch or brood size, has been used many times. The costs of an increased brood size are mainly paid by the offspring This notion is supported by the finding that, in general, animals will not increase parental effort to such a degree that it fully compensates for the extra provisioning and care required by the offspring added, reducing offspring quality (Dijkstra et al, 1990; Simons et al, 2011). Whether the relationship between survival and investment in reproduction is causal and central in shaping the aging phenotype of animals remains less clear than current theory predicts

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