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Cited by 69Neurobiology and Insect Physiology ResearchGenetics, Aging, and Longevity in Model OrganismsLipid metabolism and biosynthesis

Contribution of larval nutrition to adult reproduction in Drosophila melanogaster

Open access
Aguila, Jerell R., Hoshizaki, Deborah K., Gibbs, Allen G.·2012·Journal of Experimental Biology
DOI 10.1242/jeb.078311
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Abstract

Summary: Within the complex life cycle of holometabolous insects, nutritional resources acquired during larval feeding are utilized by the pupa and the adult. The broad features of the transfer of larval resources to the pupae and the allocation of larval resources in the adult have been described by studies measuring and tracking macronutrients at different developmental stages. However, the mechanisms of resource transfer from the larva and the factors regulating the allocation of these resources in the adult between growth, reproduction and somatic maintenance are unknown. Drosophila melanogaster Meigen presents a tractable system to test cellular/tissue mechanisms of resource acquisition and allocation, because of the detailed understanding of D. melanogaster development and the experimental tools to manipulate its tissues across developmental stages. In previous work, we demonstrated that the fat body of D. melanogaster larval is important for surviving starvation stress in the young adult and suggested that programmed cell death of the larval fat cells in the adult is important for allocation of resources for female reproduction. Here, we describe the temporal uptake of larval-derived carbon by the ovaries, and demonstrate the importance of larval fat-cell death in the maturation of the ovary and in fecundity. Larvae and adults were fed stable carbon isotopes to follow the acquisition of larval-derived carbon by the adult ovaries. We determined that over half of the nutrients acquired by the ovaries in 2-day old adult females are dependent upon the death of the fat cells. Furthermore, when programmed cell death is inhibited in the larval fat cells, ovarian development was depressed and fecundity reduced.

AI snapshot

Written from the paper’s full text.

TL;DR

This study uses stable carbon isotopes to show that larval-derived nutrients are transferred to adult ovaries in *Drosophila melanogaster*, and that programmed cell death (PCD) of larval fat cells is required for efficient allocation of those nutrients to reproduction. Inhibiting larval fat-cell death reduced early ovarian mass and fecundity without changing whole-animal energy stores.

Key findings

  • In 2-day-old control females, most ovarian sugar carbon came from larval feeding: when beet/cane and cane/beet treatments were combined, two-thirds of ovarian sugar carbon was larval-derived, compared with 42% in females where larval fat-cell death was inhibited (FCDI).
  • Inhibition of larval fat-cell PCD reduced ovarian dry mass: FCDI ovaries attained only half the dry mass of parental controls on day 2, though they reached control mass by day 4.
  • FCDI females produced ~200 eggs over the first 10 adult days versus ~300 eggs for parental controls; daily egg laying was reduced early but approached control rates by days 6–10.
  • Whole-animal triacylglyceride, glycogen, and protein stores were not altered by genotype at eclosion, and adult-derived ovarian sugar carbon did not differ among genotypes, arguing against compensatory feeding.

Methods

  • *D. melanogaster* were reared on cane-sugar (C4) or beet-sugar (C3) diets as larvae and switched or maintained as adults, yielding four larval/adult regimes: cane/cane, cane/beet, beet/beet, and beet/cane.
  • Larval fat-cell death was inhibited by expressing *diap1* in larval fat cells using *Lsp2*-GAL4; parental lines served as controls. Ovaries were dissected from 1- to 7-day-old virgin females for stable isotope analysis, dry mass, and carbon content.
  • Fecundity was measured daily for 10 days; macronutrients were assayed in individual flies. Data were analyzed with ANOVA in Statistica 7.0, with Bonferroni correction for the 12 stable-isotope ANOVAs (P<0.004).

Limitations

  • The paper states that isotope ratios alone cannot distinguish reduced larval nutrient uptake from compensatory increased adult uptake; the authors addressed this by calculating absolute larval- and adult-derived carbon amounts.
  • The paper notes that sugar is not the only dietary carbon source: yeast and corn meal provide nutrition at all stages, so the calculated larval/adult contributions are approximations and may change with age.
  • The paper states that transport of macronutrients from dying fat cells to ovaries is unresolved, including whether unique packaging mechanisms exist or circulating lipophorins suffice, and how nutrients are utilized once in the gonads.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1242/jeb.078311

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

4 of 29 cited sources checked · 1 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Holometabolous insects eclose to adulthood containing energy acquired during larval stages that often represents a significant fraction of the adult energy budget.

    “Holometabolous insects eclose to adulthood containing energy acquired during larval stages that often represents a significant fraction of the adult energy budget (Zera and Harshman, 2001;Fischer et al., 2004;Boggs and Freeman, 2005;Boggs, 2009).”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites Zera and Harshman, 2001 source
    • cites Fischer et al., 2004 source

      The Introduction (page not available in our copy) says that holometabolous insects draw on stored, usually larval-derived resources as well as adult feeding. The Discussion describes larval stores being depleted by metabolism or maintenance in the studied butterfly. The paper does not establish that those stores often make up a significant fraction of the adult energy budget across holometabolous insects. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites Boggs and Freeman, 2005 source
  • Premisecitation

    Energy reserves acquired during the larval stages of holometabolous insects are stored in the larval fat body to fuel the later re-architecture of the animal to the adult form during metamorphosis.

    “Energy reserves acquired during the larval stages of holometabolous insects are stored in the larval fat body to fuel the later re-architecture of the animal to the adult form during metamorphosis.”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites Fischer et al., 2004 source

      The Introduction (page not available) says holometabolous insects can draw on stored, usually larval-derived resources. The Discussion (page not available) also refers to larval reserves. Neither passage says those reserves are stored in the larval fat body or used to fuel metamorphosis. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites Boggs and Freeman, 2005 source
    • cites Min et al., 2006 source
  • Premisecitation

    Larval nutrients not consumed during metamorphosis are allocated to somatic maintenance and reproduction in the adult.

    “Those larval nutrients that are not consumed during metamorphosis are allocated to somatic maintenance and reproduction in the adult (Fischer et al., 2004;Boggs and Freeman, 2005;Min et al., 2006;Boggs, 2009).”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites Fischer et al., 2004 source

      The Introduction describes stored, usually larval-derived resources contributing to adult reproduction. The Discussion suggests that larval stores in starved adult females were depleted by metabolism or general maintenance, but presents this as a probable explanation, not a demonstrated allocation. The paper does not specifically establish how much larval nutrition remains after metamorphosis. (LLM, conf=0.83)

      Experimental — accuracy not yet measured
    • cites Boggs and Freeman, 2005 source
    • cites Min et al., 2006 source
  • Findingown data

    Ovaries from 1-day-old FCDI females on a cane/beet diet contained a more adult-like carbon isotope signature, indicative of a significant contribution from adult feeding, relative to control flies.

    “Thus, ovaries from 1-day-old FCDI females on a cane/beet diet contained a more adult-like carbon isotope signature, indicative of a significant contribution from adult feeding, relative to control flies.”
    Quote in the paperSubstantial claim
  • Findingown data

    Protein levels were unaffected by genotype or age.

    “Protein levels were also unaffected by genotype or age, although a statistically significant genotype-age interaction effect was noted (F 8,101 =2.58, P<0.02).”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 12
  • May combine two claims. 24

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Fat-cell autophagy in the adult has been linked to oogenic cycles in mosquitoes.

    “Fat-cell autophagy in the adult has also been linked to oogenic cycles in mosquitoes (Bryant and Raikhel, 2011).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Bryant and Raikhel, 2011 source

  • May combine two claims.

    Findingown data

    Carbon isotope signatures of ovaries from 1-day-old flies closely resembled those of their larval diet, and then changed to match the signature of the adult diet as the flies aged.

    “resembled those of their larval diet, and then changed to match the signature of the adult diet as the flies aged.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    ANOVAs for beet/corn and corn/beet flies revealed significant effects of genotype, age and their interaction on the amount of ovarian carbon derived from larval feeding (P<0.0001 for all comparisons), with ovaries from FCDI females having less larval carbon than parental controls.

    “ANOVAs for beet/corn and corn/beet flies revealed significant effects of genotype, age and their interaction on the amount of ovarian carbon derived from larval feeding (P<0.0001 for all comparisons), with ovaries from FDCI females having less larval carbon than parental controls.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    On days 2 and 3, genotype, larval diet and their interaction each significantly affected ovarian carbon isotope signature, with FCDI flies on the beet/cane diet having a more adult-derived carbon signature (less negative δ13C) than parental controls.

    “On days 2 and 3, genotype, larval diet and their interaction each significantly affected ovarian carbon isotope signature, with FCDI flies on the beet/cane diet having a more adult-derived carbon signature (less negative δ 13 C values) than parental controls.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Similar results were obtained on day 2, with significant main effects of genotype and larval diet and a significant genotype by larval diet interaction.

    “Similar results were obtained on day 2 (P<0.001 for main effects of genotype and larval diet), and a significant genotype by larval diet interaction was detected.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In ovaries from 4-day-old flies, δ13C did not differ between parental controls and FCDI flies, although ovaries still retained a significant contribution from larval sugar intake.

    “In ovaries from 4-day-old flies, δ 13 C did not differ between the parental controls and FCDI flies, although ovaries still retained a significant contribution from larval sugar intake.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Genotypic differences in ovarian δ13C were gone by day 4, although larval diet still had a significant effect (P<0.00002).

    “Genotypic differences were gone by day 4, although larval diet still had a significant effect (P<0.00002).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    On day 3, the same general pattern held, except that the effect of genotype was marginally significant and FCDI flies differed significantly only from the Lsp2-GAL4 controls.

    “The same general pattern held on day 3, except that the effect of genotype was marginally significant (F 2,12 =8.8, P<0.0045), and FCDI flies differed significantly only from the Lsp2-GAL4 controls.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    We found no indication that FCDI females compensated by eating more or directing more adult energy intake to the ovaries.

    “Thus, we found no indication that FCDI females compensated by eating more or directing more adult energy intake to the ovaries.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Approximately 50% of ovarian sugar carbon in 2-day-old parental control females was obtained from larval feeding in flies fed the beet/cane diet, compared with 25% in FCDI females.

    “Approximately 50% of ovarian sugar carbon in 2-day-old parental control females was obtained from larval feeding in flies fed the beet/cane diet, compared with 25% in FCDI females.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Ovarian mass and early fecundity were significantly reduced in FCDI flies.

    “Ovarian mass and early fecundity were significantly reduced.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Most of the sugar carbon contained in the ovaries of young flies is derived from larval feeding, but this pattern reverses when PCD is inhibited in the larval fat body.

    “Most of the sugar carbon contained in the ovaries of young flies is derived from larval feeding, but this pattern reverses when PCD is inhibited in the larval fat body.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In the silkworm moth Bombyx mori, PCD begins in the early pupal stage, when egg maturation occurs.

    “In the silkworm moth Bombyx mori, PCD begins in the early pupal stage (Kaneko et al., 2011), when egg maturation occurs.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kaneko et al., 2011 source

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The two parental stocks (UAS-diap and Lsp2-GAL4), in which normal PCD occurs, were used as controls in all experiments.

    “In all experiments, the two parental stocks (UAS-diap and Lsp2-GAL4), in which normal PCD occurs, were used as controls.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    These cells survive metamorphosis and are present in the newly eclosed adult.

    “These cells survive metamorphosis (Aguila et al., 2007) and are present in the newly eclosed adult.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Aguila et al., 2007 source

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Stable isotope analyses were performed on ovaries from 1- to 7-day-old virgin female adults to prevent transfer of male carbon sources to the ovaries.

    “We performed stable isotope analyses of ovaries from 1to 7-day-old virgin female adults to prevent transfer of male carbon sources to the ovaries.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Larvae must acquire enough nutrients not only to fuel the developmental re-organization of the pupa but also to survive the late larval and early adult periods.

    “Thus, larvae must acquire enough nutrients not only to fuel the developmental re-organization of the pupa but also to survive the late larval and early adult periods.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Sugar beet undergoes C3 photosynthesis and therefore contains a lower ratio of 13C relative to 12C than sugar cane, which utilizes C4 photosynthesis.

    “The sugar beet undergoes C3 photosynthesis and therefore contains a lower ratio of 13 C relative to 12 C than sugar cane, which utilizes C4 photosynthesis (Farquhar et al., 1989).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Farquhar et al., 1989 source

  • May combine two claims.

    Interpretationown data

    PCD is associated with both rapid maturation of the ovaries and efficient egg production.

    “Thus, PCD is associated with both rapid maturation of the ovaries and efficient egg production.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The fat body undergoes tissue remodeling into individual cells during the pre-pupal stages of metamorphosis.

    “A striking exception to the loss of larval tissues is the fat body, which undergoes tissue remodeling into individual cells during the pre-pupal stages of metamorphosis (Nelliot et al., 2006).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Nelliot et al., 2006 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Sugar is not the only carbon source in the diet, and differences in assimilation of yeast and cornmeal protein could affect calculations of larval and adult carbon contributions.

    “It is important to note that sugar is not the only carbon source in the diet, and differences in assimilation of yeast and cornmeal protein could affect these calculations.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    By 96 h, larval energy stores have been released, and inhibition of fat-cell death should no longer affect ovarian function.

    “By this time, larval energy stores have been released, and inhibition of fat-cell death should no longer affect ovarian function.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The larval fat cells serve as 'meals-ready-to-eat' in the face of starvation, where newly eclosed females that still retain their larval fat cells are over twice as starvation resistant as older adults in which the larval fat cells have undergone PCD.

    “The larval fat cells also serve as 'meals-ready-to-eat' in the face of starvation (Aguila et al., 2007), where newly eclosed females that still retain their larval fat cells are over twice as starvation resistant as older adults in which the larval fat cells have undergone PCD.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Aguila et al., 2007 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    PCD of fat cells begins during the wandering period of the final larval instar in Manduca sexta and has not been linked to oogenesis.

    “It should be noted, however, that PCD of fat cells begins during the wandering period of the final larval instar in Manduca sexta (Müller et al., 2004) and has not been linked to oogenesis.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Müller et al., 2004 source

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Early egg production is largely supported by larval nutrition, with half of the carbon content of the eggs derived from dietary sugar.

    “Previous work has shown that early egg production is largely supported by larval nutrition, with half of the carbon content of the eggs derived from dietary sugar (Min et al., 2006;O'Brien et al., 2008).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Min et al., 2006 source
    • cites O'Brien et al., 2008 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The timing of PCD of larval fat cells differs among holometabolous insects.

    “The timing of PCD of larval fat cells differs among holometabolous insects.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    A high-turnover 'fast' pool of carbon associated with reproductive effort and a 'slow' pool of somatic carbon exist.

    “Min et al. (Min et al., 2006) proposed the existence of a high-turnover 'fast' pool of carbon associated with reproductive effort, and a 'slow' pool of somatic carbon.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Min et al., 2006 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    D. melanogaster females can reabsorb eggs during nutritional stress.

    “This is unexpected, as D. melanogaster females can reabsorb eggs during nutritional stress (Wilson, 1985).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wilson, 1985 source

  • May combine two claims.

    Interpretationreasoning

    Mechanisms for macronutrient mobilization are active within the fat cells but may not be sufficiently rapid to support early ovarian development.

    “We propose that mechanisms for macronutrient mobilization are active within the fat cells but may not be sufficiently rapid to support early ovarian development.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premiseown data

    The larval fat cells are carried forward into the adult D. melanogaster and are the physical transporters of larval nutrients into the adult.

    “Previously we reported that the larval fat cells are carried forward into the adult D. melanogaster, thus leading to the conclusion that the larval fat cells are the physical transporters of larval nutrients into the adult.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In B. mori, PCD of larval fat cells begins in the early pupal stage, when egg maturation occurs.

    “In B. mori, it begins in the early pupal stage (Kaneko et al., 2011), when egg maturation occurs.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kaneko et al., 2011 source

  • May combine two claims.

    Study design and conductreasoning

    These values are only approximations of the relative contributions of larval and adult nutrition, as yeast and corn meal provide significant nutrition during all life stages, and their relative contributions to ovarian carbon may change as flies age.

    “These values are only approximations of the relative contributions of larval and adult nutrition, as yeast and corn meal provide significant nutrition during all life stages, and their relative contributions to ovarian carbon may change as flies age.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    PCD or autophagy may be generally characteristic of rapid oogenesis in insects.

    “Although the timing and extent of PCD differ among these species, PCD or autophagy may be generally characteristic of rapid oogenesis in insects.”
    Quote in the paperNot a substantial claim
33 of 33

  • The authors state this as an assumption.

    Once larval reserves are released and taken up by adult tissues, they are not available to maintain the adult during starvation.

    “yet once these reserves are released (and presumably taken up by adult tissues) they are not available to maintain the adult during starvation.”

  • The authors state this as an assumption.

    Larval nutrients represent a major energy source for the maturation of the ovaries in the adult.

    “Concomitant with this idea is the assumption that larval nutrients represent a major energy source for the maturation of the ovaries in the adult.”
2 of 2

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Cane sugar isotope ratio differs from Table 1

    Major

    The Results give the cane sugar used in the experiments a δ13C value of −11.2±0.3‰, while Table 1 lists cane sugar at −14.1±0.44‰.

  • Beet sugar isotope ratio differs from Table 1

    Minor

    The Results give the beet sugar used to prepare the media a δ13C value of −23.6±0.5‰, while Table 1 lists beet sugar at −24.7±0.27‰.

  • ANOVA diet names conflict with the stated feeding regimes

    Minor

    The analysis names beet/corn and corn/beet flies, but the stated reciprocal diet treatments are beet/cane and cane/beet; corn is not listed as a sugar-source treatment.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. Bodenstein, 1950, The postembryonic development of Drosophila, 275
  2. Riddiford, 1993, Hormones and Drosophila development, 899

Cited by

Still being checked.

Related

Authors
Aguila, J. R., Hoshizaki, D. K., & Gibbs, A. G.
Affiliations
  • University of Nevada, Las Vegas (US)
  • National Institutes of Health (US)
  • University of Nevada, Reno (US)
ORCID
Gibbs, Allen G.
Venue
Journal of Experimental Biology
Publisher
The Company of Biologists
Published
2012-01-01
Volume
216
Issue
Pt 3
Pages
399-406
ISSN
  • 0022-0949 (ISSN-L)
  • 1477-9145
DOI
10.1242/jeb.078311
OpenAlex
W2100979447
Semantic Scholar
14dff5b2255027ab62d9e5959684b32fc22689b7
Cited by
69
References
24
Citations by year
2026: 4 · 2025: 1 · 2024: 4 · 2023: 4 · 2022: 6 · 2021: 9 · 2020: 11 · 2019: 9 · 2018: 6 · 2017: 4 · 2016: 3 · 2015: 3 · 2014: 4 · 2013: 1
FWCI
0.96
Type
journal article
Language
en
Open access
Locations
  • Journal of Experimental Biology (publishedVersion)
  • PubMed (publishedVersion)
  • HighWire Press Open Archive (submittedVersion)
Funders
National Science Foundation (0719551)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords
larval nutrition, resource allocation, Drosophila melanogaster, fat body, programmed cell death, ovarian development, fecundity, adult reproduction, stable carbon isotopes, nutrient transfer, starvation stress, holometabolous insects
MeSH terms
Animals, Animal Nutritional Physiological Phenomena, Carbon, Drosophila melanogaster, Energy Metabolism, Female, Fertility, Larva, Ovary, Reproduction, Adipocytes

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