Evolution of metabolic rate in a parasitic wasp: The role of limitation in intrinsic resources

https://doi.org/10.1016/j.jinsphys.2012.04.018Get rights and content

Abstract

Metabolic rate, a physiological trait closely related to fitness traits, is expected to evolve in response to two main environmental variables: (1) climate, low metabolic rates being found in dry and hot regions when comparing populations originating from different climates in a common garden experiment and (2) resource limitations, low metabolic rates being selected when resources are limited. The main goal of this study was to investigate if differences in intrinsic resource limitations may have disrupted the expected evolution of metabolic rate in response to climate in a parasitic wasp.

We compared CO2 production of females from 4 populations of a Drosophila parasitoid, Leptopilina boulardi, as an estimate of their metabolic rate. Two populations from a hot and dry area able to synthesise lipids de novo at adult stage were compared with two populations originating from a mild and humid climate where no lipid accumulation during adult life was observed. These last females are thus more limited in lipids than the first ones.

We observed that a high metabolic rate has been selected in hot and dry environments, contrarily to the results of a great majority of studies. We suggest that lipogenesis occurring there may have allowed the selection of a higher metabolic rate, as females are less limited in energetic resources than females from the mild environment. A high metabolic rate may have been selected there as it partly compensates for the long distances that females have to cross to find laying opportunities in distant orchards. We suggest that intrinsic resources should be integrated when investigating geographical variations in metabolism as this factor may disrupt evolution in response to climate.

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

References (41)

  • J.H. Brown et al.

    Toward a metabolic theory of ecology

    Ecology

    (2004)
  • J.M. Cano et al.

    Temperature, metabolic rate, and constraints on locomotor performances in ectotherm vertebrates

    Functional Ecology

    (2006)
  • Y. Carton et al.

    Adaptive significance of a temperature induced diapause in a cosmopolitan parasitoid of Drosophila

    Ecological Entomology

    (1982)
  • M.A. Chappell

    Metabolism and thermoregulation in desert and montane grasshoppers

    Oecologia

    (1983)
  • A. Clarke

    Seasonal acclimatization and latitudinal compensation in metabolism: do they exist?

    Functional Ecology

    (1993)
  • A. Clarke et al.

    Why does metabolism scale with temperature?

    Functional Ecology

    (2004)
  • A. Clarke et al.

    Scaling of metabolic rate with body mass and temperature in teleost fish

    Journal of Animal Ecology

    (1999)
  • P. Crnokrak et al.

    Trade-offs to flight capability in Gryllus firmus: the influence of whole-organism respiration rate on fitness

    Journal of Evolutionary Biology

    (2002)
  • J. Ellers et al.

    Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction

    Journal of Evolutionary Biology

    (1997)
  • J. Ellers et al.

    A field study of size-fitness relationships in the parasitoid A. tabida

    Journal of Animal Ecology

    (1998)
  • Cited by (9)

    • Effects of daily fluctuating temperatures on the Drosophila–Leptopilina boulardi parasitoid association

      2016, Journal of Thermal Biology
      Citation Excerpt :

      However, thermoperiods can have profound effects on the development time of insects in comparison to constant temperatures (reviewed in Colinet et al. (2015)), with an accelerating effect of fluctuating thermal regimes in many cases (Beck, 1983; Ratte, 1984; Fischer et al., 2011; Ragland and Kingsolver, 2008; Kingsolver et al., 2009; Radmacher and Strohm, 2011; Bahar et al., 2012; Kjaersgaard et al., 2013). In our study, we used a thermal fluctuation around a mean temperature of 20 °C, which is much colder than the optimal temperature for this species (around 25 °C) (Fleury et al., 2009; Moiroux et al., 2012), and thus is situated in the convex part of its performance curve. Our results (i.e., a significant reduction in the development time of 3 days on average between constant and fluctuating temperatures) under a fluctuating thermal regime are thus consistent with the predictions that can be made following Jensen's inequality (Schoolfield et al., 1981; Niehaus et al., 2012; Foray et al., 2014).

    • Ovigeny index increases with temperature in an aphid parasitoid: Is early reproduction better when it is hot?

      2018, Journal of Insect Physiology
      Citation Excerpt :

      Non-stressful temperatures may have several influences on parasitoid reproduction strategy. First, higher egg maturation rate may occur because of higher metabolic rate with increasing temperature (Berger et al., 2008; Brown et al., 2004; Moiroux et al., 2012). Second, such influence of temperature on insect physiology implies that more energy is needed to sustain metabolism (Brown et al., 2004); the amount of energy available for delayed reproduction would thus decrease and the ovigeny index increase.

    View all citing articles on Scopus
    View full text