Ovariectomy in grasshoppers increases somatic storage, but proportional allocation of ingested nutrients to somatic tissues is unchanged

Abstract

SummaryReduced reproduction increases storage and extends lifespan in several animal species. The disposable soma hypothesis suggests this life extension occurs by shifting allocation of ingested nutrients from reproduction to the soma. A great deal of circumstantial evidence supports this hypothesis, but no direct tracking of nutrients has been performed in animals that are long‐lived because of direct reduction in reproduction. Here, we use the stable isotopes to track carbon and nitrogen from ingestion to somatic organs in long‐lived, ovariectomized grasshoppers. Three estimates of somatic storage (viz., quantity of hemolymph storage proteins, amount of femur muscle carbohydrates, and size of the fat body) all doubled upon ovariectomy. In stark contrast, ovariectomy did not increase the proportion of these tissues that were made from recently ingested foods. In other words, the physiology underlying relative allocation to these somatic tissues was not affected by ovariectomy. Thus, at the level of whole tissue storage, these results are consistent with a trade‐off between reproduction and longevity. In contrast, our stable isotope data are inconsistent with the prediction that enhanced storage in ovariectomized females results from a physiological shift in allocation of ingested nutrients.

Vitellogenin-RNAi and ovariectomy each increase lifespan, increase protein storage, and decrease feeding, but are not additive in grasshoppers

“…Judd et al (2011) demonstrate that although the body mass of lubber grasshoppers increases upon ovariectomy, and there are increases in somatic storage, there is no increased allocation of ingested nutrients to somatic tissues. Our data shows increases in body mass upon VgRNAi, but OVX VgRNAi treatments did not show larger body masses than any other reduced reproductive group, suggesting that these pathways extending lifespan may overlap mechanistically.…”

“…Reduced reproduction and longevity are often linked with lipid storage, as is the case in C. elegans , mice, and lubber grasshoppers (e.g., Judd et al 2011; Hatle et al 2013; reviewed in Hansen et al 2013). In addition to the ability to store lipids, insects (and crustaceans) are able to store amino acids.…”

“…The hypothesis predicts that, upon reduced reproduction, ingested nutrients are preferentially allocated to the soma, better maintaining the tissues and hence extending lifespan. Experimental tests in the past decade have provided little support for the hypothesis, especially the nutrient allocation predictions (e.g., O’Brien et al 2008; Grandison et al 2009; Speakman and Krol 2010; Judd et al 2011; Lee et al 2014). Hence, a clear underlying mechanism has not been confirmed for this widespread trade-off between reproduction and lifespan (Flatt, 2011), though there has been recent progress on lipid metabolism and autophagy using C. elegans (Goudeau et al 2011; Lapierre et al 2011; McCormick et al 2012; Ghazi 2013; and see recent paper by Labbadia and Morimoto 2015 on the heat shock response).…”

Life-extending ovariectomy in grasshoppers increases somatic storage, but dietary restriction with an equivalent feeding rate does not

“…These animals are sufficiently large so that feeding rate can be easily measured, feeding amount (as opposed to diet quality on an ad libitum diet) can be manipulated, and multiple tissues from a single individual can be tested for biochemical parameters (e.g,. Fronstin et al 2008; Judd et al 2011). This species of grasshopper has potent chemical defenses (e.g., Hatle et al 2002), so they likely have evolved to be relatively long lived, making experimental extensions of the lifespan more remarkable.…”

Nuclear hormone receptors as mediators of metabolic adaptability following reproductive perturbations

“…11,54,55 Even in human populations, while obesity is generally associated with disease, 'Metabolically Healthy Obese' individuals are noteworthy because they retain excessive weight without developing metabolic disorders. 56 Hence, there is accumulating evidence that absolute fat level is not the deterministic factor for health and longevity. Instead, the composition of lipids has a significant bearing on metabolic health.…”