Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni)

https://doi.org/10.1016/j.jinsphys.2011.11.002Get rights and content

Abstract

Insect lifespan is often closely linked to diet, and diet manipulations have been central to studies of ageing. Recent research has found that lifespan for some flies is maximised on a very low yeast diet, but once all yeast is removed, lifespan drops precipitously. Although effects of yeast availability on lifespan are commonly interpreted in terms of protein, yeast is a complex mix of nutrients and provides a rich source of vitamins, minerals and sterols. Elucidating which components of yeast are involved in this lifespan drop provides insights into more specific nutritional requirements and also provides a test for the commonplace interpretation of yeast in terms of protein. To this end, we fed Queensland fruit flies (Bactrocera tryoni) one of eight experimental diets that differed in the nutrient group(s) found in yeast that were added to sucrose: none, vitamins, minerals, amino acids, cholesterol, vitamin + mineral + cholesterol (VMC), vitamin + mineral + cholesterol + amino acids (VMCA), and yeast. We measured survival rates and egg production in single sex and mixed sex cages, as well as nutrient intake of individual flies. We found that the addition of minerals increased lifespan of both male and female flies housed in single sex cages by decreasing baseline mortality. The addition of just amino acids decreased lifespan in female flies; however, when combined with other nutrient groups found in yeast, amino acids increased lifespan by decreasing both baseline mortality and age-specific mortality. Flies on the yeast and VMCA diets were the only ones to show significant egg production. We conclude that the drop in lifespan observed when all yeast is removed is explained by missing micronutrients (vitamins, minerals and cholesterol) as well as the absence of protein in females, whereas minerals alone can explain the pattern for males. These results indicate a need for caution when interpreting effects of dietary yeast as effects of protein.

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.

References (59)

  • N.T. Papadopoulos et al.

    Cost of reproduction in male medflies: the primacy of sexual courting in extreme longevity reduction

    Journal of Insect Physiology

    (2010)
  • L. Partridge et al.

    Dietary restriction, longevity and ageing: the current state of our knowledge and ignorance

    Mechanisms of Ageing and Development

    (2005)
  • R. Pereira et al.

    Enhancing male sexual success in a lekking fly (Anastrepha suspensa Diptera: Tephritidae) through a juvenile hormone analog has no effect on adult mortality

    Journal of Insect Physiology

    (2010)
  • J.J. Ramsey et al.

    Dietary restriction and aging in rhesus monkeys: the University of Wisconsin study

    Experimental Gerontology

    (2000)
  • E.S. Vanderzant et al.

    The role of ascorbic acid in the nutrition of three cotton insects

    Journal of Insect Physiology

    (1962)
  • P.D. Allison

    Survival analysis using the SAS system: a practical guide

    (1995)
  • V. Ayala et al.

    Dietary protein restriction decreases oxidative protein damage, peroxidizability index, and mitochondrial complex I content in rat liver

    The Journals of Gerontology Series A: Biological Sciences and Medical Sciences

    (2007)
  • J.D. Barry et al.

    Effect of adult diet on longevity of sterile Mediterranean fruit flies (Diptera: Tephritidae)

    The Florida Entomologist

    (2007)
  • T.E. Bellas et al.

    Identification of the major components in the secretion from the rectal pheromone glands of the Queensland fruit flies Dacus tryoni and Dacus neohumeralis (Diptera: Tephritidae)

    Journal of Chemical Ecology

    (1979)
  • C.J. Bissoondath et al.

    Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae)

    Functional Ecology

    (1996)
  • C.J. Bissoondath et al.

    Male butterfly investment in successive ejaculates in relation to mating system

    Behavioral Ecology and Sociobiology

    (1996)
  • J.R. Carey et al.

    Longevity-fertility trade-offs in the Tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients

    Aging Cell

    (2008)
  • J.R. Carey et al.

    Food pulses increase longevity and induce cyclical egg production in Mediterranean fruit flies

    Functional Ecology

    (2002)
  • J.R. Carey et al.

    Dual modes of aging in Mediterranean fruit fly females

    Science

    (1998)
  • C.L. Chang et al.

    Adult reproductive capacity of Ceratitis capitata (Diptera: Tephritidae) on a chemically defined diet

    Annals of the Entomological Society of America

    (2001)
  • R.F. Chapman

    The Insects: Structure and Function

    (1998)
  • T. Chapman et al.

    Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males

    Proceedings of the Royal Society B-Biological Sciences

    (1996)
  • A.K. Chippindale et al.

    Phenotypic plasticity and selection in Drosophila life history evolution. 2. Diet, mates and the cost of reproduction

    Journal of Evolutionary Biology

    (1997)
  • F. Engelmann

    Reproduction in insects

  • Cited by (0)

    View full text