Turning food into eggs: insights from nutritional biology and developmental physiology of Drosophila

doi:10.1016/j.cois.2018.08.006

Current Opinion in Insect Science

Volume 31, February 2019, Pages 49-57

https://doi.org/10.1016/j.cois.2018.08.006 Get rights and content

Highlights

•
Nutrition regulates the rates of egg production.
•
Nutrients impact egg production rates with differing dynamics.
•
Egg production rate is a function of rates of egg development.
•
Nutrients serve as building blocks and energy sources for developing eggs.
•
Nutrients also induce the synthesis of hormones that drive egg development.
•
New approaches will untangle the varied effects of nutrients on egg development.

Nutrition plays a central role in fecundity, regulating the onset of reproductive maturity, egg production, and the survival and health of offspring from insects to humans. Although decades of research have worked to uncover how nutrition mediates these effects, it has proven difficult to disentangle the relative role of nutrients as the raw material for egg and offspring development versus their role in stimulating endocrine cascades necessary to drive development. This has been further complicated by the fact that both nutrients and the signalling cascades they regulate interact in complex ways to control fecundity. Separating the two effects becomes important when trying to understand how fecundity is regulated, and in devising strategies to offset the negative effects of nutrition on reproductive health. In this review, we use the extensive literature on egg development in the fruit fly Drosophila melanogaster to explore how the nutrients from food provide the building blocks and stimulate signalling cascades necessary for making an egg.

Introduction

The nutrients obtained from food affect a wide range of life history and health related traits, from regulating the pace of development, to modulating aging, fecundity, and the propensity for disease [1]. The primary goal of nutritional biology is to understand how diet impacts these traits [2,3]. It is apparent that not all nutrients are equal in their effects, and that both their quantities and qualities matter. For example, numerous studies in insects have highlighted that while lifespan is maximized on high carbohydrate, low protein diets, lifetime fecundity requires higher concentrations of protein and lower concentrations of carbohydrates to obtain maximum values [4, 5, 6, 7, 8]. Precisely how nutrients are able to exert these effects is a topic of active research.

Perhaps one of the best understood traits relating to how food affects life history is the development of eggs (otherwise known as oogenesis), which relies heavily on the maternal nutritional environment in a diverse range of animals ranging from flies to humans [9]. Restricting animals of dietary protein, carbohydrates, or lipids induces a characteristic, well described range of phenotypes. Despite substantial study, the extent to which these phenotypes result from a lack of raw materials required for egg development or from the nutrients’ effects on the production of developmental hormones necessary to drive reproduction remains poorly understood. Here, we make use of the extensive literature on egg development in the fruit fly Drosophila melanogaster in an attempt to disentangle the effects of nutrients themselves from the effects on the signalling pathways they regulate, providing our perspectives on how to best approach this problem in future studies. It is our hope that by separating these effects, we can generate deeper knowledge with regards to how and when nutrients matter for life history traits, and provide the foundation for interventions aiming to offset the effects of poor nutrition.

Section snippets

Effects of nutrition on egg production?

Drosophila are generally thought to live on rotting fruit and vegetable matter, where they participate in the decay process along with a succession of invertebrates and microbes [10]. In the laboratory, flies can be reared under a range of nutritional conditions that loosely resemble those in nature, but at a minimum require sugar and yeast for maximal growth and reproduction [11,12]. Yeast provides the majority of essential ingredients, which, depending on the strain and growth conditions, is

How do you make an egg?

In insects, ovaries are made up of strings of ovarioles, which are essentially assembly lines working in parallel for egg production. In well fed Drosophila females, each ovary contains an average of 22 ovarioles [18, 19, 20, 21], although this number varies between genotypes [19,22, 23, 24, 25, 26]. Ovarioles are composed of germ cells as well as somatic cells necessary to provide structure and to support egg production. The number of ovarioles in the ovary limits the maximum egg production

The effects of nutrition on egg development

Several studies have found that nutrition, specifically yeast starvation, affects many stages of egg chamber development to impact the number of eggs an adult female can lay. Starving female flies of yeast decreases the rate of division in the germline and somatic cells, thereby reducing rates of egg chamber growth [45]. Further, it increases the rate of cell death specifically at the transition between stages 2a and 2b and at stage 8 before vitellogenesis begins [45, 46, 47, 48, 49]. Yeast

How does diet modify physiology to change egg production?

In addition to contributing the building blocks for egg development, nutrition affects the production of at least three hormones important for oogenesis: the insulin-like peptides, ecdysone, and JH. By regulating each other’s activity, these hormones generate a complex network of interactions across organs and cell types to fine tune rates of egg production with the nutritional environment.

The concentration of nutrients circulating in the hemolymph is sensed by the fat body [64, 65, 66, 67]. In

How can we disentangle the effects of nutrients and hormones in building eggs?

Making an egg requires a complex balance of nutritional input and hormone signalling. Nutrients are required both to provide the raw material for energy storage and support growth and development of the egg chamber and to tune the levels of circulating hormones that drive egg development (Figure 1). Further, withdrawal of nutrients and interfering with these hormone cascades often produce similar types of phenotypes. For example, amino acid starvation or eliminating insulin, JH, or ecdysone

Conclusions

Decades of research on egg production in Drosophila have provided valuable insight into the genetic cascades and nutritional inputs that regulate this process. Despite these insights, we still do not understand to what extent each nutrient is required to function as a building block for egg development versus acting as a regulator of the hormones that control the developmental progression of the egg. This is complicated by the fact that many of the phenotypes induced by starvation seem to be

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as

• of special interest
•• of outstanding interest

Acknowledgements

We thank the editors Dolors Piulachs and Elisabeth Marchal for inviting us to write this review. This work was supported by an Australian Research Council Future Fellowship (FT170100259) to CKM, and an Australian Research Council Future Fellowship (FT150100237) to MDWP.

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View all citing articles on Scopus

View full text

Turning food into eggs: insights from nutritional biology and developmental physiology of Drosophila

Highlights

Introduction

Section snippets

Effects of nutrition on egg production?

How do you make an egg?

The effects of nutrition on egg development

How does diet modify physiology to change egg production?

How can we disentangle the effects of nutrients and hormones in building eggs?

Conclusions

Conflict of interest statement

References and recommended reading

Acknowledgements

Curr Opin Genet Dev

Cell Metab

Curr Opin Insect Sci

J Insect Physiol

Dev Biol

Curr Biol

J Insect Physiol

Dev Biol

Gen Comp Endocrinol

Dev Biol

J Insect Physiol

Dev Biol

Dev Biol

Cell

Curr Biol

G3 (Bethesda)

Dev Biol

Cell

Cell Metab

Science

Cell Tissue Res

Front Endocrinol

Genetics

The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity

Assuaging nutritional complexity: a geometrical approach

Proc Nutr Soc

Lifespan and reproduction in Drosophila: new insights from nutritional geometry

Proc Natl Acad Sci U S A

Macronutrient balance and lifespan

Aging

Protein:carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast:sugar ratios

Age (Dordr).

Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni)

Aging Cell

Control of adult stem cells in vivo by a dynamic physiological environment: diet-dependent systemic factors in Drosophila and beyond

WIRES Dev Biol

The secret lives of Drosophila flies

eLife

Optimization of dietary restriction protocols in Drosophila

J Gerontol Ser A Biol Sci Med Sci

Culture media for Drosophila. II. A new synthetic medium and its influence on fertility at different densities of population

Am Nat

Statistical reconciliation of the elemental and molecular biomass composition of Saccharomyces cerevisiae

Biotechnol Bioeng

A holidic medium for Drosophila melanogaster

Nat Methods

Nutritional requirements of axenically cultured Drosophila melanogaster adults

J Exp Biol

The quantitative nutritional requirements of Drosophila melanogaster

J Exp Biol

Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in Drosophilids (Insecta: Diptera)

Evolution

Le nombre d'ovarioles chez Drosophila melanogaster: relation avec la fécondité et valeur adaptive

Arch Zool Exp Gen

The roles of cell size and cell number in determining ovariole number in Drosophila

Dev Biol

Stage-specific plasticity in ovary size is regulated by insulin/insulin-like growth factor and ecdysone signalling in Drosophila

Genetics

Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster

Genetics

Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster — ovarian size and developmental temperature

Evolution

Environmental stress and reproduction in Drosophila melanogaster: starvation resistance, ovariole numbers and early age egg production

BMC Evolut Biol

Oocyte maturation and ovariole number in lines of Drosophila melanogaster selected for postponed senescence

Funct Ecol

Quantitative genetics of ovariole number in Drosophila melanogaster. I. Segregating variation for chromosome 3 and fitness