Evolution of metabolic rate in a parasitic wasp: The role of limitation in intrinsic resources
Graphical abstract
Highlights
► We compared metabolic rate of parasitoids from a mild humid area with parasitoids from a hot dry area. ► The first ones did not accumulate lipids as adults whereas parasitoids from the hot area did. ► A higher metabolic rate was observed in parasitoids from the hot dry area. ► The higher quantity of intrinsic resources may have allowed the selection of a higher metabolic rate there.
Introduction
Organisms consume energy from their environment, convert it within their bodies, allocate it to fitness-related traits such as fecundity, longevity or growth, and excrete altered forms back into the environment (Brown et al., 2004). All of these processes define metabolism. Metabolic rate (i.e. the rate of energy uptake, transformation and allocation), generally measured as O2 consumption or CO2 production, is thus closely related to the fitness of organisms. For example, an increase in metabolic rate is associated with an increase in growth rate (e.g. Metcalfe, 1998, Nylin and Gotthard, 1998) and a concurrent decrease in development time (Nylin and Gotthard, 1998), longevity (Huey and Stevenson, 1979, Artacho and Nespolo, 2009) or fecundity (Crnokrak and Roff, 2002) as energy used for metabolism is not available for these traits. Thus, understanding the evolution of metabolism is a central element in the comprehension of evolution of life histories.
Metabolism is a biological process that follows physical and chemical laws governing the transformations of energy and materials. Consequently, temperature is a major environmental factor affecting metabolic rate, particularly in ectotherms. An increase in metabolic rate when organisms are placed at higher temperatures, within a certain range (0–40 °C generally), has been universally predicted and observed (Clarke and Fraser, 2004, Gillooly et al., 2001, Nespolo et al., 2007). However, how metabolic rate evolves in response to climate is still highly debated, even if there is clear evidence that local adaptations to climate exist. Two main hypotheses on evolution of metabolic rate in response to climate have been described, leading to converging conclusions.
The most described is the Metabolic Cold Adaptation (MCA) hypothesis, also called Metabolic Compensation hypothesis (Conover and Schultz, 1995). The MCA hypothesis assumes that high metabolic rates have been selected in cold environments to compensate for the negative effect of low temperatures on metabolism. This would result in higher metabolic rates in populations or species from cold climates when compared with warm-adapted populations or species in a common garden, assuming that selection for metabolic rate has not affected thermal sensitivity. Several intraspecific and interspecific comparisons have argued in favour of MCA in fish (Alvarez et al., 2006, Cano and Nicieza, 2006), grasshoppers (Chappell, 1983, Massion, 1983), Drosophila species (Berrigan and Partridge, 1997), beetles (Strømme et al., 1986, Schultz et al., 1992) or more recently in parasitic wasps (Le Lann et al., 2011, Seyahooei et al., 2011), but others did not support it (Clarke and Johnston, 1999, Lardies et al., 2004, Lee and Baust, 1982, Nylund, 1991). Addo-Bediako et al. (2002) provided a strong evidence for the MCA hypothesis in a global-scale analysis on interspecific geographical variations of metabolic rate in insects.
The second hypothesis on evolution of metabolic rate in response to climate suggests that a low one should be selected in hot and dry environments such as deserts (Mueller and Diamond, 2001) as it confers resistance to high temperatures and desiccation by reducing exchanges with a stressful environment (Alvarez et al., 2006, Massion, 1983). Thus comparing populations from different climates reared in a common garden, low metabolic rate genotypes should be observed in hot and dry environments when compared with cooler and wet environments, according to the MCA hypothesis and to the hypothesis on resistance to desiccation.
A second important ecological factor in the evolution of metabolic rate is resource limitations. Indeed, a higher metabolic rate involves a higher amount of energy to maintain the body and thus fewer resources for fitness traits such as fecundity. Consequently, a lower metabolic rate is expected when resources are limited, to reduce the rate of resource consumption (Hoffmann and Parsons, 1997, Mueller and Diamond, 2001). In parasitic wasps, lipids represent the main energy resource allocated to survival, reproduction and dispersal (Ellers and van Alphen, 1997, Ellers et al., 1998, Rivero and Casas, 1999). These organisms were thought to be unable to synthesise lipids during adult life (for a review, see Visser and Ellers, 2008) but Visser et al. (2010) recently described lipogenesis in some species. Moiroux et al. (2010) found intraspecific variations in lipogenesis ability in adults, or at least in lipid accumulation, between populations of a Drosophila parasitoid, Leptopilina boulardi (Hymenoptera: Eucoilidae), originating from different climates. Females from an Iranian hot and dry area were able to synthesise lipids during adult life whereas a strong decrease in lipid quantity was observed in populations from the mild and humid Iranian coast of the Caspian Sea, suggesting that no lipogenesis occurred there. Thus, the differences in the limitation in intrinsic resources between populations from different climates may represent a difference in physiological constraints that is likely to have affected the evolution of metabolic rate. Indeed, the cost of maintaining a high metabolic rate on fitness-related traits should be stronger when resources are limited.
The main goal of this study was precisely to investigate if metabolic rate has mainly evolved in response to climate or was constrained by differences in intrinsic resource limitations. We thus compared the CO2 production of females originating from a hot and dry climate and able to synthesise lipids with females from a mild and humid climate where no lipid accumulation during adult life was observed. Considering the above-mentioned literature, two patterns can be expected (1) if metabolic rate has been mainly selected in response to climate (MCA hypothesis and hypothesis on resistance to desiccation), we should observe a lower metabolic rate in populations from the hot and dry area; (2) if the evolution of metabolic rate was differently constrained by differences in resource limitation, we may observe a higher metabolic rate in populations from the hot and dry area as adult lipogenesis occurs there.
Section snippets
Rearing
Four genetically distinct populations (Seyahooei, 2010) of L. boulardi (Barbotin, Carton & Keiner-Pillault, 1979), a solitary endoparasitoid that mainly attacks Drosophila melanogaster and Drosophila simulans larvae, were collected in July 2006 in Iran–two in a mild and humid region and two in a hot and dry area–using twelve banana bait traps per population. Each open trap (i.e. a plastic container with a 3 cm diameter hole covered with mesh with 2 mm openings) was colonised by five to twenty
Metabolic rate
The sampling site had a significant effect on metabolic rate. Populations from the desert area generally had a higher metabolic rate than those from the mild, humid climate at every temperature, as well as at different times in the photoperiod (Fig. 1). Hot dry 1 and 2 populations had a higher metabolic rate than Mild humid 1 and 2 populations with fresh mass as covariate at 22.5 °C, 25 °C and 27.5 °C during photophase and scotophase (Table 2). Hot dry 2 population had a higher metabolic rate than
Discussion
We observed that females living in the hottest and driest area had the highest metabolic rate, independently of rearing temperature or presence/absence of light, and thus of their locomotor activity level (Fig. 1). Our results are in contradiction with the great majority of studies on evolution of metabolic rate in response to climate where populations/species from temperate climates were found to have a higher metabolic rate than the ones from hot and/or dry climates (e.g. Addo-Bediako et al.,
Acknowledgements
We are grateful to Kees Koops for providing us a part of the insects used for the measures of metabolic rate. We would also like to thank Thiago Andrade Véronique Martel, and two anonymous referees for useful comments. This research was supported by the Ministère français de l′Enseignement Supérieur et de la Recherche (grant to Joffrey Moiroux) and is part of the Marie Curie excellence chair Comparevol (http://www.comparevol.univ-rennes1.fr/), ECOCLIM programme founded by Region Bretagne
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