Rapid larval development under time stress reduces adult life span through increasing oxidative damage

Abstract

While a trade‐off between larval development and adult life span is key to understand why not all animals develop at their maximum rate and why life histories align along a fast‐slow continuum, it has been rarely studied. More general, the physiological mechanisms underlying life‐history trade‐offs are poorly understood and there is ongoing debate about the mediatory role of oxidative stress. We explicitly investigated the role of oxidative stress in mediating the trade‐off between larval development and adult life span in the damselfly Lestes viridis. We exposed larvae to time stress (by manipulating photoperiods) and manipulated oxidative stress levels using the mitochondrial uncoupler 2,4‐dinitrophenol (DNP) that causes a reduced production of reactive oxygen species. In addition, we considered other costs of an accelerated development in terms of reductions in immune function (the activity of phenoloxidase [PO]) and energy storage (fat content). Larvae accelerated their development but not growth under time stress, allowing to identify costs of rapid development without confounding effects of rapid growth. Rapid development came at the cost of a much shorter life span, which was associated with an increase in oxidative damage to lipids, proteins and DNA. Other costs in the adult stage of a rapid larval development included a lower body mass and reduced immune function, while the fat and protein contents were not reduced. Time‐stressed animals exposed to DNP developed even faster and did not show the increase in oxidative damage. Notably, they did not suffer the costs of rapid development: they had no shorter life span, lower body mass or reduced PO activity. Our results provide strong experimental support for a trade‐off between rapid development and life span and for the mediatory role of oxidative stress in shaping this life‐history trade‐off. Our study highlights that manipulation of mitochondrial uncoupling may be a powerful method to study the mechanistic underpinnings of life‐history trade‐offs. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13068/suppinfo is available for this article.

Pace of life syndrome under warming and pollution: integrating life history, behavior, and physiology across latitudes

“…The inclusion of oxidative stress parameters is motivated by the recognition of oxidative stress as a mediator of life history trade‐offs (Monaghan et al. ; for damselfly larvae, Janssens and Stoks ) and the suggested integration of sensitivity to oxidative stress as part of the POLS, with high sensitivity associated with a fast pace (Réale et al. ).…”

“…We assayed a large number of physiological variables: metabolic rate and traits related to investment in selfmaintenance (antioxidant enzymes, oxidative damage, energy storage, immune function and melanin content). The inclusion of oxidative stress parameters is motivated by the recognition of oxidative stress as a mediator of life history trade-offs (Monaghan et al [2009]; for damselfly larvae, Janssens and Stoks [2018]) and the suggested integration of sensitivity to oxidative stress as part of the POLS, with high sensitivity associated with a fast pace (R eale et al 2010). Melanin is a pigment that fulfils a variety of functions, such as immune defense, cuticular hardening, camouflage, and wound healing (Roulin 2014).…”

Long‐term effects of superoxide and DNA repair on lizard telomeres

“…However, recent work in vivo on birds (Boonekamp, Bauch, Mulder, & Verhulst, ) suggests that six independent oxidative stress markers are uncorrelated with telomere attrition, calling into question the relative role and effect of reactive molecules for telomere dynamics. These are important observations and suggest incomplete understanding of the causal links between reactive molecules, oxidative stress, telomere attrition and life history evolution (see also Janssens & Stoks, ).…”

The Effect of Shelter on Oxidative Stress and Aggressive Behavior in Crested Newt Larvae (Triturus spp.)

“…The physiological cost can be expressed in terms of the consumption of energy needed to maintain the upregulated antioxidant defenses, to activate the repair systems, to synthesize endogenous antioxidants (such as GSH) as well as to increase the dietary intake of exogenous antioxidants [15,62]. The required energy can be diverted from other processes and can further affect the animal's fitness [63][64][65][66]. This can be more pronounced in natural conditions under which the animals are potentially limited by the available feeding time, food availability, capacity to process energy, predation and other abiotic and biotic factors.…”