Disentangling environmental effects on adult life span in a butterfly across the metamorphic boundary
Introduction
Investigating the factors affecting lifespan is a recurrent issue in both, biological and medical research, having promoted combined efforts across disciplines (Monaghan et al., 2008, Partridge and Gems, 2007). Environmental factors such as food availability or temperature may greatly contribute to variation in life span. The factor that has been most thoroughly studied seems to be food access. While malnutrition or severe starvation lead to a clear decrease in longevity (Masoro, 1998, Fadamiro et al., 2005), low to moderate levels of dietary restriction often cause an extension of longevity (which has recently been challenged and may reflect differences in the qualitative dietary composition rather than the caloric content per se; Mockett et al., 2006, Phelan and Rose, 2006, Partridge and Gems, 2007, Speakman and Hambly, 2007, Kulminski et al., 2009). This pattern might be general and holds at a variety of different approaches (e.g., moderate continuous caloric restriction, low dietary protein:carbohydrate ratio, restriction of protein or certain amino acids or short periods of starvation; Mair et al., 2005, Min and Tatar, 2006, Karl et al., 2007, Lee et al., 2008, Skorupa et al., 2008).
Although we now have a quite extensive knowledge on the effects of food availability (including both the beneficial effects of low to moderate restriction and the adverse effects of malnutrition/starvation) on lifespan in general, we need to keep in mind that life histories often consist of distinct developmental stages that may differ quite dramatically in their dietary requirements (e.g., in holometabolous insects). Butterflies for instance feed on a protein-rich diet during the larval stage, but usually switch to a carbohydrate-rich diet in the adult stage (e.g., Boggs, 1997a). Thus, restriction in any of these stages may differentially affect longevity and may involve very different mechanistic pathways. In such species the roles of larval- and adult-derived resources need to be distinguished, yet, only few studies have investigated nutritional effects across metamorphic boundaries. Moreover, they have often exclusively focussed on reproductive traits (e.g., Boggs, 1997a, Boggs, 1997b, O’Brien et al., 2002, Bauerfeind and Fischer, 2005a). For butterflies, a large impact of adult-derived carbohydrates on longevity is well documented (e.g., Bauerfeind and Fischer, 2005b) and thus expected, while effects of food restriction in the larval stage is less easy to predict. As larval starvation is likely to reduce fat stores, negative effects similar to adult food stress can be expected. Generally, little is currently known about interactive effects of food restriction in different life stages on longevity (Brakefield et al., 2005, Burger et al., 2007, Monaghan et al., 2008, Boggs, 2009).
The above considerations do not only apply to effects across life stages and metamorphic boundaries, but also to interactive effects with environmental factors other than food availability. Compared to the effects of food availability on life span, other environmental variables (such as temperature, photoperiod, population density, etc.; Piper and Partridge, 2007) have received much less attention. Any such variable may interact with the feeding regime mitigating or enhancing its effect on longevity. For example, the life span of ectotherms depends on the thermal environment, and typically increases with decreasing temperatures (within the normal, non-lethal temperature range; e.g., Clark and Kidwell, 1967, Sestini et al., 1991, Dhileepan et al., 2005, Kuo et al., 2006). Dietary treatment and temperature may interact in a complex manner affecting life history traits such as body size or growth rate (Bochdanovits and De Jong, 2003, Kingsolver et al., 2006), suggesting that longevity may also be subject to such interactive effects. While this may have important implications for individual life span, there is an obvious lack of empirical data.
Consequently, we here set out to investigate the interactive effects of temperature and food stress in different life stages (larval and adult stage) on longevity using the tropical butterfly Bicyclus anynana (Butler, 1879). We realise that the contribution of each of these factors on variation in longevity is fairly well known, so that the respective results will be hardly novel. However, our main aim here is to specifically address interactive effects both across the metamorphic boundary as well as among different environmental factors. Therefore, a rather complicated experimental design is needed. We here used a full-factorial design with two developmental and two adult temperatures (20 °C and 27 °C), two developmental feeding groups (control/food stress) and three adult feeding groups (banana/water only/no food).
Section snippets
Study organism
Bicyclus anynana is a tropical, fruit-feeding butterfly ranging from Southern Africa to Ethiopia (Larsen, 1991). The species exhibits striking phenotypic plasticity (two seasonal morphs), which is thought to function as an adaptation to alternate wet–dry seasonal environments and the associated changes in resting background and predation (Brakefield, 1997, Lyytinen et al., 2004). Reproduction is essentially confined to the warmer wet season when oviposition plants are abundantly available, and
Effects of larval temperature, food stress and sex on pupal mass
As expected, pupal mass was significantly affected by larval rearing temperature (F1,1147 = 120.3, p < 0.001), food stress (F1,1147 = 99.3, p < 0.001) and sex (F1,1147 = 476.7, p < 0.001). A low rearing temperature resulted in a higher pupal mass than a high temperature (20 °C: 166.7 ± 1.1 mg; 27 °C: 153.9 ± 1.1 mg), larval food stress reduced pupal mass relative to controls (no food stress: 163.0 ± 1.2 mg; food stress: 157.7 ± 1.1 mg), and males had a lower pupal mass than females (male: 145.0 ± 1.0 mg; female: 174.5 ± 0.9
Effects of larval temperature, food stress and sex on body size
Patterns of body size variation imposed by the factors rearing temperature, larval food stress and sex were generally as expected from previous results in the same species (Fischer et al., 2003, Fischer et al., 2004, Bauerfeind and Fischer, 2005a, Bauerfeind and Fischer, 2005b). The documented plastic increase in pupal mass at the lower rearing temperature follows a widespread pattern in ectotherms, generally referred to as the temperature-size-rule (e.g., Atkinson, 1994, Karl and Fischer, 2008
Conclusions
Our study shows that in a holometabolous insect, where life stages differ tremendously in morphology, physiology and function, life span varied primarily due to changes in the adult environment. However, environmental conditions experienced in the adult stage not only interacted with one another, but also reflected developmental conditions. The main implications are as follows. (1) Equal environmental conditions experienced in different life stages do not necessarily affect longevity in the
Acknowledgements
Financial support was provided by the German Research Council (DFG Grant Nos. Fi 846/1-3 and 846/1-4 to K.F.). We thank three anonymous reviewers for helpful comments on earlier versions of the manuscript.
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