Protein accumulation underlying lifespan extension via ovariectomy in grasshoppers is consistent with the disposable soma hypothesis but is not due to dietary restriction

Abstract

Reduced reproduction extends lifespan in many experimental animals, but the mechanism by which this occurs is unclear. The disposable soma hypothesis suggests that when reproduction is reduced, more nutrients are allocated to the soma and lifespan is extended. Alternatively, the reproductive tissues or the process of reproduction may have a direct (i.e., non-nutritional) negative effect on lifespan. We used ovariectomized grasshoppers to examine the effects of reduced reproduction throughout the lifespan at the physiological level. We focused on protein, the limiting nutrient for egg production. Ovariectomized females lived significantly longer than sham females. Because both groups ingested similar amounts, the effect was independent of dietary restriction. Despite this, ovariectomized females gained less body mass than sham females. Ovariectomized grasshoppers produced the egg yolk-precursor protein vitellogenin. At the time sham females laid their first clutch, cumulative reproductive protein was similar in ovariectomized and sham females. By advanced ages, however, ovariectomized females had produced about 5-fold less cumulative reproductive protein than sham females. In contrast, old ovariectomized females had at least 2-fold more hemolymph storage protein. These results are consistent with ovariectomy extending lifespan in part via enhanced protein allocation to storage at the expense of reproduction.

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

“…Direct reduction in reproduction can be accomplished many ways, including ovariectomy in lubber grasshoppers and brown anole lizards (Hatle et al 2008; Cox et al 2010), mutations leading to halted ovarian development (Flatt et al 2008) or irradiation (Sgró et al 1999) in Drosophila , and surgical ablation of the germ-line stem cells in C. elegans (Arantes-Oliveira et al 2002). In each of these manipulations, lifespan was increased over controls.…”

“…These animals have easily determined feeding rates, are amenable to surgery, and are large enough to allow serial sampling of hemolymph. We can directly reduce reproduction by ovariectomy (Hatle et al 2003), which increases lifespan by ~20% and reduces feeding by ~50% (Hatle et al 2008; Drewry et al 2011). Ovariectomy has been shown to double fat body mass and hemolymph volume (Hatle et al 2013).…”

“…Ovariectomy has been shown to double fat body mass and hemolymph volume (Hatle et al 2013). Ovariectomized females still produce vitellogenin; however, there is no ovary to sequester the vitellogenin, so instead there is a 5- to 10-fold increase of vitellogenin in the hemolymph (Hatle et al 2003, 2008). This represents a substantial investment of resources to reproduction by females despite failing to produce mature eggs (Tokar et al 2014).…”

“…Lubber grasshoppers have three hexamerins (Hex-90, Hex-270, Hex-500) that account for 80% of the non-vitellogenin proteins in the hemolymph (Hathaway et al 2009). Ovariectomized females accumulate high levels of non-vitellogenic protein in the hemolymph in old age (Hatle et al 2008). Knockdown of the most abundant storage protein (Hex-90) does not affect reproduction through the first clutch (Tokar et al 2014).…”

The long-lived queen: reproduction and longevity in female eusocial Damaraland mole-rats (Fukomys damarensis)

“…Supporting this hypothesis, the relaxation of the physiological demands of reproduction by inhibiting or reducing reproductive effort can result in an increase in lifespan. Ovariectomized brown anole lizards (Anolis sagrei) and eastern lubber grasshoppers (Romalea microptera) exhibit increased survival relative to sham ovariectomized females (Hatle et al 2008;Cox & Calsbeek 2010), and decreased reproduction increases lifespan in Drosophila (e.g. Flatt 2011).…”