Abstract

The expression of life-history traits, such as lifespan or reproductive effort, is tightly correlated with the amount and blend of macronutrients that individuals consume. In a range of herbivorous insects, consuming high protein to carbohydrate ratios (P:C) decreases lifespan but increases female fecundity. In other words, females face a resource-based trade-off between lifespan and fecundity. Redox metabolism may help mediate this trade-off, if oxidative damage is elevated by reproductive investment and if this damage, in turn, reduces lifespan. Here, we test how diets varying in P:C ratio affect oxidative damage and antioxidant protection in female and male of the marula fly, Ceratitis cosyra (Diptera: Tephritidae). We use replicated lines that have been subjected to experimental evolution and differ in their lifespan and reproductive scheduling. We predicted that high fecundity would be associated with high oxidative damage and reduced antioxidant defences, while longer lived flies would show reduced damage and elevated antioxidant defences. However, higher levels of oxidative damage were observed in long-lived control lines than selection lines, but only when fed the diet promoting lifespan. Flies fed diets promoting female fecundity (1:4 and 1:2 P:C) suffered greater oxidative damage to lipids than flies fed the best diet (0:1 P:C) for lifespan. Total antioxidant capacity was not affected by the selection regime or nutrition. Our results reiterate the importance of nutrition in affecting life-history traits, but suggest that in C. cosyra, reactive oxygen species play a minimal role in mediating dietary trade-offs between lifespan and reproduction.

Highlights

  • Life-history theory considers how organisms schedule investment in key fitness traits, such as when and how large to grow, when to invest in offspring and when to invest in somatic maintenance (Stearns, 2000)

  • Wild flies experienced the lowest oxidative damage to proteins (CT/Wild: ratio = 1.24, p = 0.017; Wild/DS: ratio = 0.73, p < 0.001), while there was no difference between CT and DS flies (CT/DS: ratio = 0.91, p = 0.119; Figure 1A)

  • We tested the hypothesis that the diet-mediated trade-off between lifespan and reproduction observed in female C. cosyra is associated with the balance between reactive oxygen species (ROS) production and antioxidant defences

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Summary

Introduction

Life-history theory considers how organisms schedule investment in key fitness traits, such as when and how large to grow, when to invest in offspring and when to invest in somatic maintenance (Stearns, 2000). For example, a low protein, high carbohydrate ratio (P:C) typically improves lifespan (Lee et al, 2008; Dussutour and Simpson, 2009; Fanson et al, 2009; Archer et al, 2014; Paoli et al, 2014; Jensen et al, 2015; Malod et al, 2017; Rapkin et al, 2017; Jang and Lee, 2018; Krabbe et al, 2019; Moatt et al, 2019; Duffield et al, 2020). This nutrient ratio often reduces female fecundity, which tends to be greater in females fed diets richer in protein (Maklakov et al, 2008; Jensen et al, 2015; Le Couteur et al, 2016; Rapkin et al, 2017). Apparent sex differences in responses to dietary manipulation may reflect the lack of data testing how nutrition shapes male reproductive success rather than a genuine biological signal (Moatt et al, 2016)

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