MULTITRAIT EVOLUTION IN LINES OFDROSOPHILA MELANOGASTERSELECTED FOR INCREASED STARVATION RESISTANCE: THE ROLE OF METABOLIC RATE AND IMPLICATIONS FOR THE EVOLUTION OF LONGEVITY

Abstract

Abstract. Starvation resistance is a trait often associated with longevity. Animals with increased longevity frequently show elevated starvation resistance and vice versa. Consequently, both life-history traits are thought to share genetic and physiological mechanisms, such as increased fat content and lowered metabolic rate. Here, we present results from 20 generations of selection on Drosophila melanogaster for increased starvation resistance at the time of adult eclosion. We observe that starvation resistance can be the result of more than one mechanism, all associated with an increase in fat resources. In general, metabolic rate is lowered under starved conditions relative to fed conditions. Metabolic rate in the starvation resistant lines is generally higher than in control lines under starved conditions. Starvation resistant flies are able to sustain a higher metabolic rate for a longer period of time when food is unavailable. This implies depletion of the increased fat reserves. However, longevity was not consistently affected by selection for increased starvation resistance. Similarly, paraquat resistance differed between selection lines and did not associate with starvation resistance, but rather with longevity. The results are discussed in relation to previous reported results on starvation resistance and its relation with mechanisms of aging and longevity. Increased stress resistance is often observed in Drosophila melanogaster lines selected for increased longevity (Service et al. 1985;Service 1987;Leroi et al. 1994;Force et al. 1995;Harshman et al. 1999a), in mutants (Lin et al. 1998), and in phenotypic manipulation experiments (e.g., Zwaan et al. 1991;Bouletreau-Merle and Fouillet 2002). This association also holds in other species such as mice and nematodes (Longo and Fabrizio 2002). Similarly, selection for increased adult starvation resistance has been shown to increase longevity (Rose et al. 1992;Chippindale et al. 1996; but see Bubliy and Loeschcke 2005). Selection on shorter longevity also results in decreased starvation resistance (Zwaan et al. 1995a). These results strongly suggest that starvation resistance shares, at least in part, genetic regulatory mechanisms with longevity. Moreover, the selection experiments indicate the presence of standing genetic (co)variation in natural populations. There are strong positive correlations between starvation resistance and longevity as opposed to the negative correlations both traits display with reproductive output. This indicates the presence of a trade-off between maintenance and reproduction, or between the soma and the germ line as has been proposed in the disposable soma theory (Kirkwood 1977;Kirkwood and Holliday 1979). This theory overlaps with the theory of antagonistic pleiotropy (Williams 1957), in which advantages of early life traits are considered to be disadvantageous later in life (Kirkwood and Rose 1991). In pursuit of the validity of this latter theory, reproduction late in life was found to increase longevity considerably (Rose 19...

Transcriptome analysis of a long-lived natural Drosophila variant: a prominent role of stress- and reproduction-genes in lifespan extension

“…Previously, our laboratory has selected four lines for increased starvation resistance (SR) and maintained two control lines (C) in a 20 generation experiment [28]. We chose a single replicate line of each selection regime to perform the microarray experiment.…”

“…In our laboratory, we previously selected Drosophila for increased starvation resistance (SR) and maintained corresponding control lines under optimal food (C) [28]. The selection resulted in SR lines with not only elevated resistance to starvation but also extended lifespan under three other food levels as compared with the C flies.…”

Metabolic rate and hypoxia tolerance are affected by group interactions and sex in the fruit fly (Drosophila melanogaster): new data and a literature survey

“…Collectively, these data suggest that there is little or no specific dynamic action (SDA) in either the short- or long-term. In contrast to these findings, Baldal et al reported lowered metabolic rate as a result of starvation but, in the long-term across generations, elevated metabolic rates associated with starvation resistance (Baldal et al, 2006). Again, variation exists in the literature, with another long-term study reporting no change in metabolic rate produced by chronic diet restriction (Hulbert et al, 2004).…”

“…Investigators have long used the fruit fly as a model for investigations of life span, and accordingly have measured metabolic rate in an often unsuccessful attempt to correlate metabolism to longevity (Arking et al, 1988; Baldal et al, 2006; Hulbert et al, 2004; Khazaeli et al, 2005; Melvin et al, 2007; Miquel et al, 1982; Partridge et al, 2005; Promislow and Haselkorn, 2002; Van Voorhies et al, 2003, 2004b). Metabolic rate in Drosophila has also been investigated in the context of specific genotypes (Hoekstra and Montooth, 2013; Jensen et al, 2014; Jumbo-Lucioni et al, 2010; Montooth et al, 2003; Stone et al, 2013), to reveal how genotype underpins specific metabolic phenotypes.…”

Linking growing up and getting old : plastic and evolutionary effects of developmental diet on adult phenotypes and gene expression in the fruit fly

“…Notably this response is quite different from the evolutionary response to acute starvation during adulthood. Rather than speeding up developmental time and decreasing size, as is the case for larval malnutrition, selection on starvation resistance in young adulthood generally selects for slower development and increased lipid accumulation, resulting in larger adult size (Baldal et al 2006;Bubliy & Loeschcke 2005;Chippindale et al 1996) (but see Hoffmann et al 2005). This difference highlights the fact that similar selection pressures may select for different adaptations depending on when in life they are experienced.…”