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Research
Fatter or Stronger: Resource Allocation Strategy and the Underlying Metabolic Mechanisms in Amphibian Tadpole
Bin Wang
CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chengdu 610041, China
Corresponding Author
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background
Resource allocation trade-off between storage and somatic growth is an essential physiological phenomenon in animals. Revealing its patterns and underlying mechanisms are fundamental for behavior, evolutionary, and population ecological studies. Currently, our understanding of the real-time resource allocating patterns in animals is still limited, and the underlying metabolic mechanisms have been rarely investigated. The life strategy of amphibian larvae relies on precise coordination between storage and somatic growth, which makes them good model for studying this issue.
Results
Here, the resource allocation strategy was investigated for Rana omeimontis tadpoles, who exhibit prominent hepatic fat-accumulation. Results showed that their ontogenetic fat accumulation emerged when tadpoles grew to a body weight range of 30–50 mg, where their fat storage had a high priority in resource allocation. Beyond this range, the resource proportion for somatic growth increased, but continuous storage investment was likely maintained to kept higher body fat index in larger individuals. This seeming paradoxical allocation pattern could be explained by assuming a positive relationship between storage abundance and the investment to somatic growth. This speculation was supported by the observation that storage had the priority in resource allocation to reach a higher body fat index before increment in body weight when food level increased. Moreover, it was also supported by the metabolic pattern that presented lipid-based energy metabolism after ontogenetic fat accumulation, and activating the mobilization of fat storage in the liver can promote the somatic growth. In short, fat synthesis and fat accumulation in the liver may well modulated the resource allocation to somatic growth, and their liver likes a reservoir with valves to regulate energy flow for the downstream developmental processes.
Conclusion
In Rana omeimontis tadpoles, their hepatic fat level positively modulated the resource allocation to somatic growth through lipid-based energy metabolism. We reveal the real-time resource allocation pattern in an amphibian tadpole and explain it at molecular level. These results likely provide a new mechanistic insight into the resource allocation in animals.
Keywords
Fat storage, Allocation trade-off, Fatty liver, Metabolic switch, PPARs, Size variation
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This is a list of supplementary files associated with this preprint. Click to download.
- Supplementarymaterial2.xlsx
Supplementary material 2: Blood metabolite table.
- Supplementarymaterial1.pdf
Supplementary material 1: Figure S1 Liver of R. omeimontis tadpoles. (A-B) Morphorlogical and histological traits of liver accumulated with fat (provided with adequate food). Livers with high fat level are similar to adipose tissue in white to yellow colour [1]. (C-D) Morphorlogical and histological traits of liver with little fat (starved for ten days). Livers with low fat level are always in darker colour (brown to black), because their pigment is more obvious due to higher tissue transparency. Overall, fat accumulation transforms the semitransparent gel-like liver to a non-transparent oil-like tissue. These traits make it feasible to identify the onset of ontogenetic hepatic fat accumulation in these tadpoles. Figure S2 Morphological traits of the liver collected at different timepoints. Note the prominent morphological differences in the liver between tadpoles collected at 23 d.a.h and others [19]. Figure S3 Curve-fitting of the relationship between liver weight and body weight. Two fitting model (linear regression and piecewise linear regression) were conducted (1stOpt software). The vertical axis is the R square value of the regression model, and the horizontal axis is the inflection point (body weight) for the piecewise linear regression. The results show that piecewise linear regression performs better than linear regression, and the optimum inflection points locate between 30-40 mg body weight. Figure S4 Distribution fitting of the tadpole body weight with Gaussian mixture model (mixtools, a R package). The distribution pattern changed from Gaussian distribution to skewed or bimodal distribution gradually after most tadpoles reached to 30-40 mg body weight. The skewed or bimodal distribution can be explained by a Gaussian distribution whose average value move forward with time and another Gaussian distribution whose average value stay within 30-40 mg. Figure S5 Transcriptional comparison between liver before and after ontogenetic fat accumulation. (A) Typical morphology of the livers collected for RNA-seq. Left, liver before fat accumulation; right, liver after fat accumulation. Arrows denotes the liver lobes. (B) Information of the samples. Each sample was consisted of livers of 4-7 tadpoles. (C) Gene expression correlations between samples. (D) An overview on the DEGs between group L and S (FDR < 0.05; DESeq and Benjamini and Hochberg’s correction). (E) Significantly enriched KEGG pathways based on upregulated DEGs in group L (q < 0.01; Kobas 3.0). (F-H) Variation trends of differently expressed (p < 0.05, T test) ribosomal components (F), aminoacyl tRNA synthesis (G), DNA replication elements, and enzymes of aerobic energy production (I). Figure S6 Abundances of potential metabolic substrates in tadpoles after ontogenetic fat accumulation (n=3 for the blood; n=7 for the liver and tail). The liver and tail data were adpoted from our previously published metabolomes [19]. Figure S7 Involvement of PPARs in regulating lipid metabolism and somatic growth (supplementary). (A) Transcriptional upregulation of nuclear receptors regulating lipid metabolism. (B-C) The effect of PPAR agonists on hepatic fat mobilization in starved tadpoles (supplementary). Different letters indicate significant differences between groups (p < 0.05), as shown by the Student Newman Keuls post hoc test after one-way ANOVA. Figure S8 Deduced resource allocation pattern after initial ontogenetic fat accumulation. It was supposed that a higher level of energy abundance was the precondition for a higher growth rate (or higher investment proportion of resource to somatic growth).
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Research
Fatter or Stronger: Resource Allocation Strategy and the Underlying Metabolic Mechanisms in Amphibian Tadpole
Bin Wang
CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chengdu 610041, China
Corresponding Author
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
History
CURRENT STATUS: Posted
Version 1
Posted 17 Sep, 2020
No community comments so far
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
Subject Areas
Animal Science
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background
Resource allocation trade-off between storage and somatic growth is an essential physiological phenomenon in animals. Revealing its patterns and underlying mechanisms are fundamental for behavior, evolutionary, and population ecological studies. Currently, our understanding of the real-time resource allocating patterns in animals is still limited, and the underlying metabolic mechanisms have been rarely investigated. The life strategy of amphibian larvae relies on precise coordination between storage and somatic growth, which makes them good model for studying this issue.
Results
Here, the resource allocation strategy was investigated for Rana omeimontis tadpoles, who exhibit prominent hepatic fat-accumulation. Results showed that their ontogenetic fat accumulation emerged when tadpoles grew to a body weight range of 30–50 mg, where their fat storage had a high priority in resource allocation. Beyond this range, the resource proportion for somatic growth increased, but continuous storage investment was likely maintained to kept higher body fat index in larger individuals. This seeming paradoxical allocation pattern could be explained by assuming a positive relationship between storage abundance and the investment to somatic growth. This speculation was supported by the observation that storage had the priority in resource allocation to reach a higher body fat index before increment in body weight when food level increased. Moreover, it was also supported by the metabolic pattern that presented lipid-based energy metabolism after ontogenetic fat accumulation, and activating the mobilization of fat storage in the liver can promote the somatic growth. In short, fat synthesis and fat accumulation in the liver may well modulated the resource allocation to somatic growth, and their liver likes a reservoir with valves to regulate energy flow for the downstream developmental processes.
Conclusion
In Rana omeimontis tadpoles, their hepatic fat level positively modulated the resource allocation to somatic growth through lipid-based energy metabolism. We reveal the real-time resource allocation pattern in an amphibian tadpole and explain it at molecular level. These results likely provide a new mechanistic insight into the resource allocation in animals.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5