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A dietary sterol trade off determines lifespan responses to dietary restriction in Drosophila melanogaster

10.1101/2020.08.21.260489 ◽

2020 ◽

Author(s):

Brooke Zanco ◽

Christen K. Mirth ◽

Carla M. Sgrò ◽

Matthew D.W. Piper

Keyword(s):

Drosophila Melanogaster ◽

Dietary Restriction ◽

Dietary Protein ◽

Life Histories ◽

Important Principle ◽

Trade Offs ◽

Dietary Sterol ◽

Mechanistic Basis ◽

Dietary Sterols

AbstractDiet plays a significant role in maintaining lifelong health. In particular, lowering the dietary protein : carbohydrate ratio can improve lifespan. This has been interpreted as a direct effect of these macronutrients on physiology. Using Drosophila melanogaster, we show that the role of protein and carbohydrate on lifespan is indirect, acting by altering the partitioning of limiting amounts of dietary sterols between reproduction and lifespan. Shorter lifespans in flies fed on high protein : carbohydrate diets can be rescued by supplementing their food with cholesterol. Not only does this fundamentally alter the way we interpret the mechanisms of lifespan extension by dietary restriction, these data highlight the important principle that life histories can be affected by nutrient-dependent trade-offs that are indirect and independent of the nutrients (often macronutrients) that are the focus of study. This brings us closer to understanding the mechanistic basis of dietary restriction.

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Testing evolutionary explanations for the lifespan benefit of dietary restriction in Drosophila melanogaster

10.1101/2020.06.18.159731 ◽

2020 ◽

Cited By ~ 1

Author(s):

Eevi Savola ◽

Clara Montgomery ◽

Fergal M. Waldron ◽

Katy Monteith ◽

Pedro Vale ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Dietary Restriction ◽

Side Effect ◽

Bacterial Pathogen ◽

Lifespan Extension ◽

Trade Off ◽

Scarce Resources ◽

Evolutionary Hypothesis ◽

Laboratory Conditions ◽

Extended Lifespan

ABSTRACTDietary restriction (DR), limiting calories or specific nutrients, extends lifespan across diverse taxa. This lifespan extension has been explained as diet-mediated changes in the trade-off between lifespan and reproduction, with survival favoured with scarce resources. Another evolutionary hypothesis suggests the selective benefit of the response is the maintenance of reproduction. This hypothesis predicts that lifespan extension is a side effect of benign laboratory conditions, where DR individuals are frailer and unable to deal with additional stressors, and thus lifespan extension should disappear under more stressful conditions. We tested this by rearing outbred female Drosophila melanogaster on 10 different protein:carbohydrate diets. Flies were either infected with a bacterial pathogen (Pseudomonas entomophila), injured or unstressed. We monitored lifespan, fecundity and ageing measures. DR extended lifespan and reduced reproduction irrespective of injury and infection. These results do not support lifespan extension under DR being a side effect of benign laboratory conditions.

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A dietary sterol trade-off determines lifespan responses to dietary restriction in Drosophila melanogaster females

eLife ◽

10.7554/elife.62335 ◽

2021 ◽

Vol 10 ◽

Author(s):

Brooke Zanco ◽

Christen K Mirth ◽

Carla M Sgrò ◽

Matthew DW Piper

Keyword(s):

Drosophila Melanogaster ◽

Dietary Restriction ◽

Dietary Protein ◽

Life Histories ◽

Important Principle ◽

Trade Offs ◽

Dietary Sterol ◽

Mechanistic Basis ◽

Dietary Sterols

Diet plays a significant role in maintaining lifelong health. In particular, lowering the dietary protein: carbohydrate ratio can improve lifespan. This has been interpreted as a direct effect of these macronutrients on physiology. Using Drosophila melanogaster, we show that the role of protein and carbohydrate on lifespan is indirect, acting by altering the partitioning of limiting amounts of dietary sterols between reproduction and lifespan. Shorter lifespans in flies fed on high protein: carbohydrate diets can be rescued by supplementing their food with cholesterol. Not only does this fundamentally alter the way we interpret the mechanisms of lifespan extension by dietary restriction, these data highlight the important principle that life histories can be affected by nutrient-dependent trade-offs that are indirect and independent of the nutrients (often macronutrients) that are the focus of study. This brings us closer to understanding the mechanistic basis of dietary restriction.

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Testing evolutionary explanations for the lifespan benefit of dietary restriction in fruit flies ( Drosophila melanogaster )

Evolution ◽

10.1111/evo.14146 ◽

2020 ◽

Author(s):

Eevi Savola ◽

Clara Montgomery ◽

Fergal M. Waldron ◽

Katy M. Monteith ◽

Pedro Vale ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Dietary Restriction ◽

Fruit Flies ◽

Evolutionary Explanations

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Repeated stress exposure results in a survival–reproduction trade-off in Drosophila melanogaster

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2009.1807 ◽

2009 ◽

Vol 277 (1683) ◽

pp. 963-969 ◽

Cited By ~ 135

Author(s):

Katie E. Marshall ◽

Brent J. Sinclair

Keyword(s):

Drosophila Melanogaster ◽

Model Organism ◽

Intrinsic Rate ◽

Intrinsic Rate Of Increase ◽

Stress Exposure ◽

Trade Off ◽

Repeated Stress ◽

Rate Of Increase ◽

In The Wild ◽

Future Reproduction

While insect cold tolerance has been well studied, the vast majority of work has focused on the effects of a single cold exposure. However, many abiotic environmental stresses, including temperature, fluctuate within an organism's lifespan. Given that organisms may trade-off survival at the cost of future reproduction, we investigated the effects of multiple cold exposures on survival and fertility in the model organism Drosophila melanogaster . We found that multiple cold exposures significantly decreased mortality compared with the same length of exposure in a single sustained bout, but significantly decreased fecundity (as measured by r , the intrinsic rate of increase) as well, owing to a shift in sex ratio. This change was reflected in a long-term decrease in glycogen stores in multiply exposed flies, while a brief effect on triglyceride stores was observed, suggesting flies are reallocating energy stores. Given that many environments are not static, this trade-off indicates that investigating the effects of repeated stress exposure is important for understanding and predicting physiological responses in the wild.

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Absence of reproduction-immunity trade-off in male Drosophila melanogaster evolving under differential sexual selection

BMC Evolutionary Biology ◽

10.1186/s12862-019-1574-1 ◽

2020 ◽

Vol 20 (1) ◽

Cited By ~ 2

Author(s):

Zeeshan Ali Syed ◽

Vanika Gupta ◽

Manas Geeta Arun ◽

Aatashi Dhiman ◽

Bodhisatta Nandy ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Sexual Selection ◽

Trade Off

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Dietary Restriction Extends Lifespan in Wild-Derived Populations of Drosophila melanogaster

PLoS ONE ◽

10.1371/journal.pone.0074681 ◽

2013 ◽

Vol 8 (9) ◽

pp. e74681 ◽

Cited By ~ 23

Author(s):

Athanasios Metaxakis ◽

Linda Partridge

Keyword(s):

Drosophila Melanogaster ◽

Dietary Restriction

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Genetic variation of dietary restriction and the effects of nutrient-free water and amino acid supplements on lifespan and fecundity of Drosophila

Genetics Research ◽

10.1017/s001667231100019x ◽

2011 ◽

Vol 93 (4) ◽

pp. 265-273 ◽

Cited By ~ 20

Author(s):

KENNETH B. DICK ◽

CHELSEA R. ROSS ◽

LEV Y. YAMPOLSKY

Keyword(s):

Amino Acids ◽

Genetic Variation ◽

Dietary Restriction ◽

Free Water ◽

Water Source ◽

Essential Amino Acids ◽

Inbred Lines ◽

Life History Variation ◽

Trade Off ◽

Specific Mortality

SummaryWe measure genetic variation in lifespan and fecundity at two food levels in 34 core lines of the Drosophila Genetic Reference Panel collection. Lines were significantly different from each other in lifespan and fecundity at both restricted and full food. There was a strong food-by-line interaction for the slope of age-specific mortality, fecundity and proportion of fertilized eggs, indicating the presence of genetic variation for the strength of the dietary restriction effect, likely to represent standing genetic variation in a natural population from which the lines used have originated. No trade-off between fecundity and lifespan manifested in life-history variation among inbred lines. Our data partially corroborate the recent proposition that availability of nutrient-free water eliminates the apparent dietary restriction at least in some conditions. Although flies on full food with water added had lifespan slightly higher than those without a water source, it was still significantly lower than that in flies on restricted food, with no indication of interaction. We fully corroborate the recently discovered effect of addition of essential amino acids to the medium: addition of 1·5 mM methionine to restricted food significantly increased fecundity without a measurable decrease in lifespan; addition of each of 10 essential amino acids increased fecundity and decreased females lifespan to the levels observed on full food, again with no evidence of line-by-food interactions. We propose a mechanistic hypothesis explaining the observed data, based on the assumption that food consumption by flies is adjusted according to flies’ saturation in water and methionine.

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