Sex-specific transcriptomic responses to changes in the nutritional environment

Abstract

23Males and females typically pursue divergent reproductive strategies and accordingly require 24 different dietary compositions to maximise their fitness. Here we move from identifying sex-25 specific optimal diets to understanding the molecular mechanisms that underlie male and 26 female responses to dietary variation. We examine male and female gene expression on male-27 optimal (carbohydrate-rich) and female-optimal (protein-rich) diets. We find that the sexes 28 share a large core of metabolic genes that are concordantly regulated in response to dietary 29 composition. However, we also observe smaller sets of genes with divergent and opposing 30 regulation, most notably in reproductive genes which are over-expressed on each sex's 31 optimal diet. Our results suggest that nutrient sensing output emanating from a shared 32 metabolic machinery are reversed in males and females, leading to opposing diet-dependent 33 regulation of reproduction in males and females. Further analysis and experiments suggest 34 that this reverse regulation occurs within the IIS/TOR network. 35 36 [3]. 46Studies in insect species [3][4][5][6][7] have shown that the two sexes require different diets to 47 maximise fitness. Female fitness is typically maximised on a high concentration of protein, 48 which fulfils the demands of producing and provisioning eggs. Males, in contrast, achieve 49 optimal fitness with a diet consisting of more carbohydrate, which can fuel activities such as 50 locating and attracting mates. Work on nutritional choices has shown that individuals tailor 51 their diet in line with their physiological needs. In insects, females overall prefer diets with 52 higher protein content, whereas males chose a more carbohydrate-rich diet [8, 9]. These 53 choices are further adapted to reflect the individual's current condition and reproductive 54 investment [9, 10]. For example, Camus et al. [11] found that the female preference for 55 protein in fruit flies was significantly higher in mated females (who require resources to 56 produce eggs) than virgins, while the preferences of males (who start producing sperm before 57 reaching sexual maturity) did not significantly differ between mated and virgin flies. 58But individuals not only choose diets to suit their needs where possible, they also adapt 59 their physiology and reproductive investment in response to the quality and quantity of 60 nutrition available. This has been studied extensively using experiments that either alter the 61 macronutrients composition (carbohydrates vs. protein) of the diet while keeping the overall 62 caloric intent constant, or by manipulating the overall nutrient content of the food-dietary 63 restriction (DR). These studies have shown that a wide range of life history traits respond to 64 changes in both the composition of the food [7, 12, 13] and the quantity of nutrients supplied 65 [14][15][16]. For example, DR typically causes an extension of lifespan at the cost of reduced 66reproduction [17], and a similar response can be triggered ...

Early-life hypoxia alters adult physiology and reduces stress resistance and lifespan in Drosophila

“…For example, a recent study showed that genetic suppression of insulin signaling in adult flies could alter sexually dimorphic differences in gene expression, including many metabolic genes (Graze et al, 2018). In addition, alterations in TOR signaling have also been shown to have sex-dependent effects in gene expression and on nutrient control of reproduction in Drosophila (Camus et al, 2019).…”

Insights into how development and life-history dynamics shape the evolution of venom

“…Progeny protection is another interesting function related to intersexual venom variation, such as eggs being loaded with venom from the mother, or males having a higher protein yield and potency for guarding eggs against predators and conspecifics. Furthermore, theoretical and empirical evidence suggests that males and females should be under selection for different dietary preferences and resource utilization that maximize their sex-specific fitness [147,148]. This can be explained by evidence that different dietary requirements are needed to maximize their fertility may not be the same.…”

Impact of high-fat diet on lifespan, metabolism, fecundity and behavioral senescence inDrosophila

“…Fecundity in Drosophila females depends on nutrient availability and diet composition (Armstrong, 2020;Camus et al, 2019;Hartman et al, 2013;Musselman and Kühnlein, 2018;Partridge et al, 1987). Therefore, we asked whether the fecundity of the mated flies is affected by HFD.…”