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Sex-specific Plasticity and the Nutritional Geometry of Insulin-Signaling Gene Expression in Drosophila Melanogaster
Alexander Shingleton
University of Illinois at Chicago
Corresponding Author
ORCiD: https://orcid.org/0000-0001-9862-9947
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background: Sexual-size dimorphism (SSD) is replete among animals, but while the selective pressures that drive the evolution of SSD have been well studied, the developmental mechanisms upon which these pressures act are poorly understood. Ours and others’ research has shown that SSD in Drosophila reflects elevated levels of nutritional plasticity in females versus males, such that SSD increases with dietary intake and body size, a phenomenon called sex-specific plasticity (SSP). Additional data indicate that while body size in both sexes responds to variation in protein level, only female body size is sensitive to variation in carbohydrate level. Here we explore whether these difference in sensitivity at the morphological level are reflected by differences in how the insulin/IGF-signaling (IIS) and TOR-signaling pathways respond to changes in carbohydrates and proteins in females versus males, using a nutritional geometry approach.
Results: The IIS-regulated transcripts of 4E-BP and InR most strongly correlated with body size in females and males respectively, but neither responded to carbohydrate level and so could not explain the sex-specific response to body size to dietary carbohydrate. Transcripts regulated by TOR-signaling did, however, respond to dietary carbohydrate in a sex-specific manner. In females, expression of dILP5 positively correlated with body size, while expression of dILP2,3 and 8, was elevated on diets with a low concentration of both carbohydrate and protein. In contrast, we detected lower levels of dILP2 and 5 protein in the brains of females fed on low concentration diets. We could not detect any effect of diet on dILP expression in males.
Conclusion: Although females and males show sex-specific transcriptional responses to changes in protein and carbohydrate, the patterns of expression do not support a simple model of the regulation of body-size SSP by either insulin- or TOR-signaling. The data also indicate a complex relationship between carbohydrate and protein level, dILP expression and dILP peptide levels in the brain. In general, diet quality and sex both affect the transcriptional response to changes in diet quantity, and so should be considered in future studies that explore the effect of nutrition on body size.
Keywords
Sexual-size dimorphism, sex-specific plasticity, nutrition, body size, insulin/IGF-signaling, TOR-signaling
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This is a list of supplementary files associated with this preprint. Click to download.
- SupplementaryFigure1.pdf
Supplementary Figure 1: Thin plate spline of the effect of protein and carbohydrate concentration on female and male body size and sexual size dimorphism (SSD). (A, B) Surfaces shows the relationship between body size, carbohydrate level and protein level in female and male flies (C) Surface shows a thin plate spline of the difference in female and male body size (SSD) across the same nutritional landscape, using fitted values from A and B. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:14.6, 1:7.2, 1:3.5, 1:1.7, 1.3:1, 1.4 :1).
- SupplementaryFigure1.pdf
Supplementary Figure 1: Thin plate spline of the effect of protein and carbohydrate concentration on female and male body size and sexual size dimorphism (SSD). (A, B) Surfaces shows the relationship between body size, carbohydrate level and protein level in female and male flies (C) Surface shows a thin plate spline of the difference in female and male body size (SSD) across the same nutritional landscape, using fitted values from A and B. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:14.6, 1:7.2, 1:3.5, 1:1.7, 1.3:1, 1.4 :1).
- SupMaterialBodySizeAnalysis.pdf
- SupMaterialBodySizeAnalysis.pdf
- SupMaterialGeneExpressionAnalysis.pdf
- SupMaterialGeneExpressionAnalysis.pdf
- SupplementaryFigure2.pdf
Supplementary Figure 2: Thin plate spline of the effect of protein and carbohydrate concentration on the expression of IIS and TOR transcriptionally-regulated genes in females and males. Surfaces shows the relationship between gene expression, carbohydrate level and protein level in female and male flies. Expression of (A, A′) InR, and (B, B′) 4E-BP, both negatively regulated by the activity of the IIS via the Forkhead transcription factor FOXO. (C, C′) Expression of Ash2L, ostensibly negatively regulated by the activity of TOR signaling. (D, D′) Expression of CG3071, ostensibly positively regulated by the activity of TOR signaling. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:16, 1:8, 1:4, 1:2, 1:1, 2:1).
- SupplementaryFigure2.pdf
Supplementary Figure 2: Thin plate spline of the effect of protein and carbohydrate concentration on the expression of IIS and TOR transcriptionally-regulated genes in females and males. Surfaces shows the relationship between gene expression, carbohydrate level and protein level in female and male flies. Expression of (A, A′) InR, and (B, B′) 4E-BP, both negatively regulated by the activity of the IIS via the Forkhead transcription factor FOXO. (C, C′) Expression of Ash2L, ostensibly negatively regulated by the activity of TOR signaling. (D, D′) Expression of CG3071, ostensibly positively regulated by the activity of TOR signaling. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:16, 1:8, 1:4, 1:2, 1:1, 2:1).
- SupplementaryFigure3.pdf
Supplementary Figure 3: Thin plate spline of the effect of protein and carbohydrate concentration on the expression of dILPs in females and males. Surfaces shows the relationship between gene expression, carbohydrate level and protein level in female and male flies. (A) dILP2. (B) dILP3. (C) dILP 5. (D) dILP8. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:16, 1:8, 1:4, 1:2, 1:1, 2:1). Corresponding thin-plate spline plots are shown in Supplementary Figure 1.
- SupplementaryFigure3.pdf
Supplementary Figure 3: Thin plate spline of the effect of protein and carbohydrate concentration on the expression of dILPs in females and males. Surfaces shows the relationship between gene expression, carbohydrate level and protein level in female and male flies. (A) dILP2. (B) dILP3. (C) dILP 5. (D) dILP8. Points indicate diets tested and dotted lines connect diets with equal protein-to-carbohydrate ratios (1:16, 1:8, 1:4, 1:2, 1:1, 2:1). Corresponding thin-plate spline plots are shown in Supplementary Figure 1.
- SupplementaryTable1.docx
- SupplementaryTable1.docx
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This preprint is under consideration at EvoDevo. A preprint is a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research
Sex-specific Plasticity and the Nutritional Geometry of Insulin-Signaling Gene Expression in Drosophila Melanogaster
Alexander Shingleton
University of Illinois at Chicago
Corresponding Author
ORCiD: https://orcid.org/0000-0001-9862-9947
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Under Review
Version 1
Posted 23 Nov, 2020
No community comments so far
Reviewer #2 agreed
On 07 Dec, 2020
Review #1 received
Received 01 Dec, 2020
Reviewer #1 agreed
On 20 Nov, 2020
Editor assigned
On 18 Nov, 2020
Reviewers invited
Invitations sent on 18 Nov, 2020
Submission checks complete
On 18 Nov, 2020
Editor invited
On 18 Nov, 2020
First submitted
On 17 Nov, 2020
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
Subject Areas
Evolutionary Biology
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background: Sexual-size dimorphism (SSD) is replete among animals, but while the selective pressures that drive the evolution of SSD have been well studied, the developmental mechanisms upon which these pressures act are poorly understood. Ours and others’ research has shown that SSD in Drosophila reflects elevated levels of nutritional plasticity in females versus males, such that SSD increases with dietary intake and body size, a phenomenon called sex-specific plasticity (SSP). Additional data indicate that while body size in both sexes responds to variation in protein level, only female body size is sensitive to variation in carbohydrate level. Here we explore whether these difference in sensitivity at the morphological level are reflected by differences in how the insulin/IGF-signaling (IIS) and TOR-signaling pathways respond to changes in carbohydrates and proteins in females versus males, using a nutritional geometry approach.
Results: The IIS-regulated transcripts of 4E-BP and InR most strongly correlated with body size in females and males respectively, but neither responded to carbohydrate level and so could not explain the sex-specific response to body size to dietary carbohydrate. Transcripts regulated by TOR-signaling did, however, respond to dietary carbohydrate in a sex-specific manner. In females, expression of dILP5 positively correlated with body size, while expression of dILP2,3 and 8, was elevated on diets with a low concentration of both carbohydrate and protein. In contrast, we detected lower levels of dILP2 and 5 protein in the brains of females fed on low concentration diets. We could not detect any effect of diet on dILP expression in males.
Conclusion: Although females and males show sex-specific transcriptional responses to changes in protein and carbohydrate, the patterns of expression do not support a simple model of the regulation of body-size SSP by either insulin- or TOR-signaling. The data also indicate a complex relationship between carbohydrate and protein level, dILP expression and dILP peptide levels in the brain. In general, diet quality and sex both affect the transcriptional response to changes in diet quantity, and so should be considered in future studies that explore the effect of nutrition on body size.
Figure 1
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