Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly, Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist

Abstract

In insects, lifespan and reproduction are strongly associated with nutrition. The ratio and amount of nutrients individuals consume affect their life expectancy and reproductive investment. The geometric framework (GF) enables us to explore how animals regulate their intake of multiple nutrients simultaneously and determine how these nutrients interact to affect life‐history traits of interest. Studies using the GF on host‐generalist tephritid flies have highlighted trade‐offs between longevity and reproductive effort in females, mediated by the protein‐to‐carbohydrate (P:C) ratio that individuals consume. Here, we tested how P and C intake affect lifespan (LS) in both sexes, and female lifetime (LEP), and daily (DEP) egg production, in Ceratitis cosyra, a host‐specialist tephritid fly. We then determined the P:C ratio that C. cosyra defends when offered a choice of foods. Female LS was optimized at a 0:1 P:C ratio, whereas to maximize their fecundity, females needed to consume a higher P:C ratio (LEP = 1:6 P:C; DEP = 1:2.5 P:C). In males, LS was also optimized at a low P:C ratio of 1:10. However, when given the opportunity to regulate their intake, both sexes actively defended a 1:3 P:C ratio, which is closer to the target for DEP than either LS or LEP. Our results show that female C. cosyra experienced a moderate trade‐off between LS and fecundity. Moreover, the diets that maximized expression of LEP and DEP were of lower P:C ratio than those required for optimal expression of these traits in host‐generalist tephritids or other generalist insects.

Macronutrients and micronutrients drive trade‐offs between male pre‐ and postmating sexual traits

“…The trade‐off between life span and reproduction has been studied extensively in life‐history research (van Noordwijk & de Jong, ). However, there is increasing evidence that the trade‐off between longevity and reproduction arises because these traits are optimized at different P:C ratios (reviewed in Le Couteur et al, ), and that females generally display the greatest reproductive effort at higher P:C ratios (Harrison et al, ; Lee et al, ; Malod et al, ; Solon‐Biet et al, ). In contrast, the effects of macronutrients on the life span cost of reproduction for males are less well defined.…”

“…However, the use of a multidimensional approach, the Geometric Framework for nutrition, allows the study of interactions between nutrition and trait expression with respect to multiple components in the diet (Simpson & Raubenheimer, ). The Geometric Framework has been used successfully to disentangle the effects of calories and macronutrient balance on life span (Lee et al, ; Solon‐Biet et al, ), and to demonstrate that different ratios of macronutrients, such as protein, carbohydrate and fats, are necessary to maximize different life‐history traits (Bunning et al, ; Malod, Archer, Hunt, Nicolson, & Weldon, ; Solon‐Biet et al, ). For example, in Drosophila melanogaster , females maximize their egg laying rate when consuming food with a protein (P)‐to‐carbohydrate (C) ratio of 1:2, but have the longest life span when given a diet of 1P:16C (Jensen, McClure, Priest, & Hunt, ; Lee et al, ).…”

“…However, a simple resource limitation model for life‐history trade‐offs is being challenged by evidence that covariation between life span and reproduction can be uncoupled from caloric intake (Grandison, Piper, & Partridge, ; Tu & Tatar, ). Recent work suggests that the balance of macronutrients, rather than caloric intake, is a crucial factor underlying the trade‐off between life span and reproduction (Jensen et al, ; Lee et al, ; Maklakov et al, ; Malod et al, ; Solon‐Biet et al, ). Trade‐offs between pre‐ and postmating sexual traits have been reported in animals with polyandrous mating systems (Simmons, Lüpold, & Fitzpatrick, ) and is a central assumption in sperm competition theory (Parker, Lessells, & Simmons, ).…”

Adult diet of a tephritid fruit fly does not compensate for impact of a poor larval diet on stress resistance

“…Alternatively, an insect may exhibit compensatory feeding and dietary selection (e.g. Abisgold and Simpson, 1987;Fanson et al, 2009;Maklakov et al, 2008;Malod et al, 2017) to achieve a nutrient intake that approaches an optimum defined by its evolved life history strategy. However, it has also been found that restriction of food intake (calories) can lead to 'hormetic' effects, whereby individuals experiencing a mild stress exhibit improved stress resistance and life extension (Le Bourg, 2009).…”

“…We predicted that stress resistance would be improved by larval development in a nutrient-rich diet, leading to greater body reserves, but consumption of a nutrient-rich diet as an adult would compensate for poor stress resistance associated with a suboptimal larval diet. C. cosyra was chosen as the focus of this study due to availability of data on its adult nutritional intake targets and life history (Malod et al, 2017), its close phylogenetic relationship to other fruit fly species that have been the subject of water balance studies (Weldon et al, 2016(Weldon et al, , 2018 and because it exhibits relatively high desiccation resistance (Weldon et al, 2016). In addition, C. cosyra is an important quarantine pest across sub-Saharan Africa where it affects production of mangoes (Vayssieres et al, 2009;White and Elson-Harris, 1992).…”