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. 2006 Apr 22;273(1589):939-47.
doi: 10.1098/rspb.2005.3388.

No extension of lifespan by ablation of germ line in Drosophila

Andrew I Barnes  1 , James M Boone, Jake Jacobson, Linda Partridge, Tracey Chapman
Affiliations

No extension of lifespan by ablation of germ line in Drosophila

Andrew I Barnes et al. Proc Biol Sci. .

Abstract

Increased reproduction is frequently associated with a reduction in longevity in a variety of organisms. Traditional explanations of this 'cost of reproduction' suggest that trade-offs between reproduction and longevity should be obligate. However, it is possible to uncouple the two traits in model organisms. Recently, it has been suggested that reproduction and longevity are linked by molecular signals produced by specific reproductive tissues. For example, in Caenorhabditis elegans, lifespan is extended in worms that lack a proliferating germ line, but which possess somatic gonad tissue, suggesting that these tissues are the sources of signals that mediate lifespan. In this study, we tested for evidence of such gonadal signals in Drosophila melanogaster. We ablated the germ line using two maternal effect mutations: germ cell-less and tudor. Both mutations result in flies that lack a proliferating germ line but that possess a somatic gonad. In contrast to the findings from C. elegans, we found that germ line ablated females had reduced longevity relative to controls and that the removal of the germ line led to an over-proliferation of the somatic stem cells in the germarium. Our results contrast with the widely held view that it is downstream reproductive processes such as the production and/or laying of eggs that are costly to females. In males, germ line ablation caused either no difference, or a slight extension, in longevity relative to controls. Our results indicate that early acting, upstream reproductive enabling processes are likely to be important in determining reproductive costs. In addition, we suggest that the specific roles and putative patterns of molecular signalling in the germ line and somatic tissues are not conserved between flies and worms.

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Figures

Figure 1
Figure 1
Survivorship of virgin germ cell-less, tudor and genetically matched control males and females against age in days since the emergence of the adult from the pupae. Survivorship is the proportion of the original cohort surviving to a given day. (a) gcl virgin females and controls (the latter being the offspring of gcl heterozygote (1) or homozygote (2) mothers possessing a germ line). (b) tud virgin females and controls. (c) gcl virgin males and controls. (d) tud virgin males and controls.
Figure 2
Figure 2
Germ line-less and WT adult gonads. (a–c): male reproductive organs from (a) WT, (b) gcl germ line-less and (c) tud germ line-less males. tst, testes; vd, vas deferens; ag, accessory gland; ed, ejaculatory duct. The testes are greatly reduced in size in germ line-less flies, but accessory gland size is unaffected (see text). (d–f): paired ovaries from (d) WT, (e) gcl germ line-less and (f) tud germ line-less females. (d) is viewed directly under light microscopy (e) and (f) have been DAPI stained. a, anterior; p, posterior. Ovariole structure is clearly visible at the anterior end of all ovaries, but the mature eggs, which make up the bulk of the WT ovary, are lacking in the germ line-less females.
Figure 3
Figure 3
Germ line-less and WT female ovarioles. Ovarioles are from (a, b) WT, (c, d) gcl germ line-less and (e, f) tud germ line-less females. Each ovariole is shown singly stained with DAPI (top, blue), either (a, c, e) vasa or (b, d, f) FasIII (middle, red) and with the two stains combined (bottom, red and blue). Normal ovarioles develop from the anterior end, which is to the left in all images. Germ stem cells proliferate in region 1, and somatic stem cells are on the border between regions 2a and 2b. In region 3 the somatic cells surround the germ cells to form a nascent egg chamber (EC). (a) Vasa staining (red) indicates the presence of germ cells throughout the early WT ovariole. Vasa staining is completely absent in (b) gcl and (c) tud germ line-less flies. (b) FasIII staining (red) indicates somatically derived cells proliferating posterior of the 2a/2b border. They are confined to the poles of later egg chambers. In (e) gcl and (f) tud germ line-less flies, FasIII staining reaches the anterior end of the germarium, indicating that the whole of the ovariole has become an area of somatic stem cell proliferation (effectively equivalent to the WT region 2b). The white scale bars represent (a–d) 50 μm or (e, f) 25 μm.
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