Contrasted effects of suppressing live yeast from food on longevity, aging and resistance to several stresses in Drosophila melanogaster
Introduction
Dietary restriction (DR) increases longevity in many vertebrate or invertebrate species (see, e.g., the issue 9, volume 126 of Mechanisms of Ageing and Development, 2005). However, DR does not increase longevity in DBA/2 mice (Forster et al., 2003) and in all tested species, particularly in the flies Musca domestica (Cooper et al., 2004) and Ceratitis capitata (Carey et al., 2002). There is a debate regarding the effect of DR in Drosophila melanogaster (Le Bourg and Minois, 2005) and in human beings (see the issue 3, volume 7 of Biogerontology, 2006). Besides longevity, the effects of DR on aging have also been studied, mainly in rodents. DR improves motor performance at old age (Ingram et al., 1987, Means et al., 1993, Fitting et al., 2008), delays or decreases the incidence of age-related pathologies (e.g., Cheney et al., 1980, Bronson and Lipman, 1991, Blackwell et al., 1995), and improves resistance to heat (Hall et al., 2000). Either positive effects of DR on learning at old age, absence of effects, and even deleterious effects have been reported (compare, Ingram et al., 1987, Markowska, 1999, Yanai et al., 2004). In contrast, DR decreases resistance to cold (Campbell and Richardson, 1988), to influenza (Gardner, 2005), and to parasite infection (Kristan, 2007). Therefore, the effect of DR on longevity of rodents is mostly positive whereas that on aging can be either positive, negative, or absent (see also Masoro, 2005).
Another model widely used in DR studies is D. melanogaster. Contrasted effects of DR on longevity have been reported. Feeding for a part of the day, i.e., intermittent feeding, did not increase longevity (Kopec, 1928, Le Bourg and Médioni, 1991). Dilution of a rearing medium containing dry yeast had no effect on longevity (David et al., 1971, Soh et al., 2008) or increased it (e.g., Chapman and Partridge, 1996; review in Tatar, 2007). However, fecundity and longevity can be very low on the Chapman and Partridge’s (1996) SY medium containing sugar and yeast but no corn flour (Le Bourg and Minois, 2005, Mockett et al., 2006; see also Partridge et al., 2005). Bass et al. (2007) observed longevity on the SY medium and on the SY medium to which corn flour was added (MSY medium). Mated males and females had a median longevity of ca 35 and 25 days on the SY medium and of 50 and 45 days on the MSY medium, respectively (see Table 2 in Bass et al., 2007). Since Bass et al. (2007) showed that longevity is much lower on the SY medium than on the MSY one, it can be concluded that using the SY medium in DR studies (review in Partridge et al., 2005) is not the best strategy to show that DR really increases longevity (see also Mockett et al., 2006). Using a medium containing corn flour, in addition to dry yeast and sugar, allowed to observe rather high longevities, even in mated flies, and increasing or decreasing the dry yeast component decreased longevity (Min and Tatar, 2006a).
Besides the dilution of the rearing medium procedure, Chippindale et al. (1993) and Le Bourg and Minois (1996) diluted only the live yeast added on the surface of a rearing medium. The first authors observed that decreasing live yeast increased longevity of mated males and females, whereas Le Bourg and Minois (1996) observed no change in virgin flies and mated males and a longevity increase in mated females. This longevity increase in mated females could be linked to the fecundity decrease which is observed when live yeast is diluted (Chippindale et al., 1993, Simmons and Bradley, 1997). However, it remains that Chippindale et al. (1993) and Le Bourg and Minois (1996) observed different effects of DR in mated males: the different media used in these two studies could explain this difference. Chippindale et al. (1993) used a medium containing dry yeast, agar, and sugar, whereas Le Bourg and Minois (1996) used the S101 medium of Pearl et al. (1926) made of sugar, agar, and minerals. When the S101 medium is not supplemented with live yeast, longevity is low (ca 3 weeks: Alpatov, 1930, Le Bourg and Minois, 1996) and flies cannot complete development (unpublished observations of the second author). Good and Tatar (2001) also showed that longevity of several wild-type strains was twice higher in both sexes on an agar-sugar-corn flour-dry yeast medium supplemented with live yeast (ca 40–45 days) than on the same medium without live and dry yeast (ca 25 days).
All these results on D. melanogaster indicate that the quality of the control medium is of importance in DR studies. It can be wondered whether DR would still have positive effects on longevity if the lifespan of DR and control groups would be high, i.e., if it could be sure that a positive effect of DR is not due to a low longevity of the control group. As an attempt to reconcile the results of Chippindale et al. (1993) and of Le Bourg and Minois (1996), in the present study we have thus recorded longevity on the usual agar-sugar-corn flour-dry yeast medium supplemented or not with live yeast. This medium supplemented with live yeast at its surface provides a rather high longevity of ca 40–50 days in males and 50–60 days in females (e.g., Le Bourg et al., 2000) and allows flies to complete development. Our rationale was that removing live yeast would not decrease longevity or impair development, due to malnutrition, because this medium would still contain a source of proteins (dry yeast). Therefore, comparing longevity on the same medium with or without live yeast could show whether removing this important source of proteins can increase longevity. Observing a longevity increase when live yeast is removed would thus be a strong argument for a positive effect of DR on longevity in D. melanogaster. Obviously, it could be argued that removing only one component of the medium, as in the present study, cannot be strictly considered as a DR procedure. However, since other authors have used the generic term “dietary restriction” to describe very different procedures varying the quantity of nutrients (review in Tatar, 2007), it seems of interest to provisionally use this term.
Removing live yeast decreases fecundity (Chippindale et al., 1993, Simmons and Bradley, 1997). As virgin females lay less eggs and live longer than mated females (Boulétreau-Merle, 1988), using both virgin and mated females could thus provide contrasted effects of DR, because the DR effect on longevity is expected to be of a lower magnitude in virgin than in mated females if there is a trade-off between egg-laying and longevity (discussion in e.g., Le Bourg and Minois, 2005, Tatar, 2007; see also Lee et al., 2008). Therefore, in the present study, longevity was recorded in mated and virgin flies of both sexes.
Furthermore, we also observed viability of the eggs and, at various ages, resistance to various stresses (heat, cold, starvation, infection), climbing activity and fecundity.
Live yeast is not expected to increase viability if the standard medium allows completion of development. By contrast, observing a decreased viability when there is no live yeast would show that this medium is poorly nutritious.
Only a few authors have studied the effects of DR on aging. Observing behavioral aging allows to know whether DR has similar effects on aging and longevity or not. For instance, Bross et al. (2005), using the SY medium, observed a longevity increase in each sex when the medium was diluted, but no effect on locomotor activity at 3 weeks of age. Bhandari et al. (2007) observed a longevity increase with dilution of the SY medium, but the age-related decrease of climbing activity (the ability to climb up the vertical side of a vial) was similar in all dilution groups.
Finally, the effects of DR on resistance to stress and on longevity could be similar or not. For instance, Burger et al. (2007) observed a longevity increase when the SY medium was diluted, but DR flies were less resistant at old age to starvation, oxidative stress, or cold.
Section snippets
Flies
The experimental flies were adult males and females of the wild strain Meyzieu caught near Lyon in France at the end of the 1970s. This strain is maintained by mass-mating (several bottles containing hundreds of flies mixed every 2 weeks) on the standard medium (distilled water: 78.9% w/w, agar: 1.5%, sugar: 10.1%, corn meal: 7.9% and killed yeast: 1.2%) containing a mold inhibitor (para-hydroxymethyl-benzoic acid) and enriched with live yeast at the surface of the medium. Experimental flies
Fecundity
The egg-laying curve (Fig. 1) shows that DR decreased egg-laying, particularly at a young age, and that mated females laid more eggs than virgin ones, as usually observed (Chippindale et al., 1993, Boulétreau-Merle, 1988). Moreover, in the control group, the egg-laying peak was higher in mated females than in virgin ones and occurred earlier. In contrast, there was no real peak in the DR group in both mated and virgin females.
The ANOVA analyzing mean daily fecundity confirmed that DR decreased
Discussion
Some studies of DR in D. melanogaster have reported a longevity increase, whereas others did not show such an effect (see Section 1). Such a discrepancy could be due to the use of different DR procedures. Using the dilution of the rearing medium procedure implies that the quantity of food really eaten by the flies decreases with the dilution of the medium, because, if they eat more when the medium is diluted, they could be not under DR (for a discussion, see Mockett et al., 2006, Tatar, 2007).
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Present address: Laboratoire de Psychologie Sociale, UPRES Equipe d’Accueil no 849, Université d’Aix-Marseille 1, 29 avenue Robert-Schuman, F-13621 Aix-en-Provence cedex 1, France.