Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni)
Graphical abstract
Highlights
► Lifespan in adult flies precipitously drops when all yeast is removed. ► We test the role of protein and micronutrients in causing this lifespan drop. ► Protein and micronutrients explain the drop in virgin female Queensland fruit flies. ► Just minerals explain the drop in male Queensland fruit flies. ► Our results suggest caution in equating yeast with protein.
Introduction
Nutritional environment is a potent mediator of an organism’s lifespan. In particular, dietary restriction (DR: reduction in nutrient intake without malnutrition) has been consistently found to extend lifespan across a vast range of animal taxa, including yeast (Lin et al., 2002), fruit flies (Chippindale et al., 1997, Good and Tatar, 2001), mice (Weindruch and Walford, 1982), and rhesus monkeys (Roth et al., 1999, Ramsey et al., 2000; for general DR reviews, see Masoro, 2002, Masoro, 2005). Effects of DR on lifespan have most often been attributed to caloric restriction (CR) (Masoro, 2005, Partridge and Brand, 2005). However, in insects, growing evidence suggests that nutrients, rather than calories, are responsible for effects of DR on lifespan (Drosophila melanogaster – Mair et al., 2005, Lee et al., 2008; field crickets Teleogryllus commodus – Maklakov et al., 2008; Queensland fruit fly Bactrocera tryoni (‘Q-fly’) – Fanson et al., 2009).
Protein has emerged as a strong candidate as a nutritional mediator of lifespan in flies. Studies of D. melanogaster (Lee et al., 2008), Mexican fruit flies (Anastrepha ludens, Carey et al., 2008) and Q-flies (Fanson et al., 2009) have reported monotonic increase in lifespan when systemically decreasing the protein:carbohydrate (P:C) ratio (i.e., reducing protein content) of adult diet. In these studies, changing P:C ratios was accomplished by altering sucrose:yeast ratios. However, removing all protein (yeast) from the adult diet caused lifespan to precipitously drop instead of increase. When switched from a very low P:C diet to a diet containing no protein, mean lifespan decreased by 20% in D. melanogaster, 38% in Mexican fruit flies, and 50% in Q-flies. Using less detailed experimental designs than above, other studies with flies have found a similar pattern of a reduction in lifespan when flies are fed sugar without yeast (e.g., B. cucurbitae Haq and Hendrichs in press; Anastrepha suspensa ‘Caribbean fruit fly’ Pereira et al., 2010; Ceratitis capitata ‘medfly’ Barry et al., 2007, San Andrés et al., 2009). Since yeast contains a variety of nutrients, it is not clear which nutrient(s) are responsible for this drop in lifespan. Understanding the cause of this drop in lifespan should provide insights into the role of nutrients, especially protein, as mediators of ageing.
Yeast is a complex mixture of carbohydrates, protein, vitamins, minerals and sterols. Though high levels of dietary protein may be causing the decrease in lifespan, it may be that adults nonetheless need to acquire at least a small amount for basic biological function. Hence the precipitous drop in lifespan observed in flies fed sucrose without yeast may be due mainly to absence of protein. However, micronutrients (e.g. vitamins, minerals, and sterols) are required for many biological functions during the larval stage in insects, such as energy metabolism, growth and development (vitamin A, Claret and Volkoff, 1992; vitamin Bs, Dadd, 1961; vitamin C, Vanderzant et al., 1962; sterols, Clayton, 1964; phosphorus, Perkins et al., 2004). The role of adult-acquired micronutrients for insects is less known, especially in relation to survival, and failure to obtain these nutrients during the adult stage may result in increased mortality rates. To understand the relative roles of protein and micronutrients as mediators of lifespan there is a need for experimental approaches that manipulate these dietary components separately.
Here we examine the role of protein and micronutrients in mediating the sharp reduction in lifespan experienced by Q-flies maintained without yeast. We used a chemically defined diet (Fanson and Taylor, in press) that allowed us to add individual nutrient classes found in yeast (amino acids, vitamins, minerals, and sterols) to a sucrose diet and create select nutrient combinations. We measured lifespan, reproduction, and consumption rates on each diet. Consumption rates were measured as caloric intake affects lifespan positively (Lee et al., 2008, Maklakov et al., 2008, Fanson et al., 2009, Fanson and Taylor, in press). Mortality patterns of flies maintained in single sex and mixed sex cages can often differ, possibly due to physiological consequences of mating (Carey et al., 2002a, Piper and Partridge, 2007, Papadopoulos et al., 2010). We therefore recorded mortality patterns for males and females in both single sex and mixed sex cages.
Section snippets
Study species
Q-flies were obtained as pupae from the Fruit Fly Production Facility at Elizabeth Macarthur Agricultural Institute (EMAI, New South Wales, Australia). The EMAI fly stock was maintained on a larval diet of lucerne chaff, cane sugar, and torula yeast, and adult diet of cane sugar and yeast hydrolysate. For all experiments, temperature and relative humidity were maintained at ca. 25 °C and ca. 70%, respectively, and on a light schedule of 14L:10D including 1 h dawn and dusk periods.
Experimental diets
Increasing yeast
Survival
Lifespan of Q-flies varied with diet, sex and housing (Table 2). The two-step survival analysis approach allowed us to analyse how baseline mortality (scale factor) and age-specific mortality rate (Weibull shape) contributed to these differences in mean lifespan. Both sexes had higher baseline survival in mixed cages (Table 2, Table 3). For males, the addition of minerals to the diet caused a marginally significant decrease in baseline mortality (Table 3; Fig 1b and c), thus increasing
Discussion
In this study, we explored the role of specific nutrient classes as potential mediators of the precipitous drop in lifespan observed when yeast is excluded from the diet of Q-flies. We examined the role of micronutrients (vitamins, minerals, cholesterol) and protein (amino acids) on lifespan, reproduction, and diet consumption of Q-flies housed in single- and mixed-sex cages. Minerals increased survival rates in Q-flies, except for females housed in mixed-sex cages. Adding only amino acids to a
Conclusion
Tephritid flies commonly exhibit reduced lifespan when restricted to a diet of sugar alone rather than a diet including both sugar and yeast. For most species, this has been found in a simple presence/absence sense but for Q-flies we also have detailed data showing trends across a full range of possible proportions (Fanson et al. 2009). These data show the transition from a diet of low yeast to an all-sugar diet results in the greatest decrease in lifespan, a roughly 50% decrease. This presents
Acknowledgments
We thank the staff of Industry & Investment New South Wales, who generously provided us Queensland fruit flies from their mass-rearing facility. Financial support was provided through a Macquarie University Research Excellence Scholarship. K. Fanson and S. Yap provided insightful comments on earlier drafts.
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