Genotype by temperature interactions in the metabolic rate of the Glanville fritillary butterfly

Department of Biological and Environmental Sciences, University of Helsinki, FI-00014, Helsinki, Finland.
Journal of Experimental Biology (Impact Factor: 2.9). 04/2010; 213(Pt 7):1042-8. DOI: 10.1242/jeb.034132
Source: PubMed


Metabolic rate is a highly plastic trait. Here I examine factors that influence the metabolic rate of the Glanville fritillary butterfly (Melitaea cinxia) in pupae and resting and flying adults. Body mass and temperature had consistent positive effects on metabolic rate in pupae and resting adults but not in flying adults. There was also a consistent nonlinear effect of the time of the day, which was strongest in pupae and weakest in flying adults. Flight metabolic rate was strongly affected by an interaction between the phosphoglucose isomerase (Pgi) genotype and temperature. Over a broad range of measurement temperatures, heterozygous individuals at a single nucleotide polymorphism (SNP) in Pgi had higher peak metabolic rate in flight, but at high temperatures homozygous individuals performed better. The two genotypes did not differ in resting metabolic rate, suggesting that the heterozygotes do not pay an additional energetic cost for their higher flight capacity. Mass-independent resting and flight metabolic rates were at best weakly correlated at the individual level, and therefore, unlike in many vertebrates, resting metabolic rate does not serve as a useful surrogate of the metabolic capacity of this butterfly.

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Available from: Kristjan Niitepõld
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    • "In order for natural populations of ectotherms to respond effectively to a changing thermal environment, there must be sufficient genetic variation in traits under natural selection (Huey and Kingsolver 1993; Loeschcke et al. 1997; Hoffmann et al. 2003; Fasolo and Krebs 2004). Multiple studies have identified the gene phosphoglucose isomerase (Pgi), which codes for a dimeric enzyme (PGI) whose activity is central to glucose metabolism, as one candidate for understanding how natural populations respond to environmental temperature variation (Watt 1992; Mitton 1997; Haag et al. 2005; Karl et al. 2009; Niitepold et al. 2009; Saastamoinen et al. 2009; Niitepold 2010). Variation at Pgi has been associated with differences in metabolic rate, dispersal ability, oviposition, life span, and larval development (Watt 1983, 1992; Watt et al. 1983, 1985; Haag This content downloaded from "
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    ABSTRACT: Abstract Locomotion and mating ability are crucial for male reproductive success yet are energetically costly and susceptible to physiological stress. In the Sierra willow beetle Chrysomela aeneicollis, male mating success depends on locating and mating with as many females as possible. Variation at the glycolytic enzyme locus phosphoglucose isomerase (Pgi) is concordant with a latitudinal temperature gradient in these populations, with Pgi-1 frequent in the cooler north, Pgi-4 in the warmer south, and alleles 1 and 4 in relatively equal frequency in areas intermediate in geography and climate. Beetles experience elevated air temperatures during a mating season that causes differential physiological stress among Pgi genotypes, and running speeds of individuals homozygous for Pgi-4 are more tolerant of repeated thermal stress than individuals possessing Pgi-1. Here the importance of running behavior for male mating activity was examined, and differential effects of thermal stress among Pgi genotypes on male mating activity were measured. In nature, males run more than females, and nearly half of males mate or fight for a mate after running. In the laboratory, mating activity was positively correlated with running speed, and repeated mating did not reduce running speed or subsequent mating activity. Males homozygous for Pgi-4 mated longer and more frequently after heat treatment than 1-1 and 1-4 males. All heat-treated males had lower mating frequencies and higher heat shock protein expression than control males; however, mating frequency of recovering 4-4 males increased throughout mating trials, while treated 1-1 and 1-4 males remained low. These results suggest that effects of stress on mating activity differ between Pgi genotypes, implying a critical role for energy metabolism in organisms' response to stressful temperatures.
    Full-text · Article · Jul 2013 · Physiological and Biochemical Zoology
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    • "Apart from dispersal, virtually all other life-history traits in butterflies depend on flight, which is energetically very expensive (Bartholomew and Casey, 1978) and may lead to physiological trade-offs potentially affecting fitness. Flight metabolic rate is known to be highly variable among local populations in the Glanville fritillary metapopulation and it is associated with molecular variation in the gene phosphoglucose isomerase (Pgi), which encodes for a glycolytic enzyme (Haag et al., 2005; Niitepõld, 2010). Furthermore, molecular variation in Pgi is associated with variation in several other lifehistory traits (Saastamoinen, 2007; Saastamoinen and Hanski, 2008; Niitepõld et al., 2009), including lifespan (Saastamoinen et al., 2009). "
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    ABSTRACT: High peak metabolic may provide performance advantage, but it may also entail a physiological cost. A long-held assumption is that high mass-specific energy expenditure is associated with short lifespan. To examine the relationship between energy expenditure and lifespan we asked two questions. First, do individuals have a consistent rate of metabolism throughout their life? Second, is metabolic rate correlated with lifespan? We analysed the repeatability of measurements of resting (RMR) and peak flight metabolic rate (MR(peak)) throughout the life of the Glanville fritillary butterfly (Melitaea cinxia). Measurements of MR(peak) showed significant repeatability. Senescence occurred only shortly before death. RMR showed a U-shaped relationship with age and very low repeatability. Intraspecific association between metabolic rates and lifespan was tested under three conditions: in the laboratory, under field conditions, and in a laboratory experiment with repeated flight treatments. There was a significant correlation between MR(peak) and lifespan in all three experiments, but the correlation was positive, not negative. RMR was not correlated with lifespan. Both MR(peak) and lifespan may reflect physiological condition and be therefore positively correlated. Individuals with a large resource pool may be able to invest in mechanisms that slow down ageing. Individuals with high metabolic capacity may also possess adaptations against ageing. Molecular polymorphism in the gene phosphoglucose isomerase (Pgi) was significantly associated with both MR(peak) and lifespan, and may have coevolved with defence mechanisms against senescence. Generalisations such as 'live fast, die young' may be too simple to explain the complex processes affecting ageing and lifespan.
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    • "Heterozygous isoforms have enhanced stability and kinetic properties (Watt 2003) and in benign thermal conditions infer benefits such as higher peak metabolic rates and thus higher dispersal (Niitepold 2010), the ability to fly at lower ambient temperatures (Saastamoinen and Hanski 2008), and longer life span (Kallioniemi and Hanski 2011). However, homozygous genotypes are associated with better performance in thermal extremes, for example, maintenance of higher metabolic rates at high temperatures (Dahlhoff et al. 2008; Niitepold 2010), faster CCR (Karl et al. 2008), and increased larval survival at low temperatures (Kallioniemi and Hanski 2011). The effects of PGI genotype differ markedly across life stages (Rank et al. 2007; Kallioniemi and Hanski 2011), meaning that fitness consequences of a particular genotype may not be immediately obvious unless multiple life stages are tested under both stressful (hot and cold) and benign thermal conditions (Kallioniemi and Hanski 2011). "
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    ABSTRACT: Abstract Among-population variation in insect thermal performance is important for understanding patterns and mechanisms of evolution and predicting insect responses to altered climate regimes in future or novel environments. Here we review and discuss several key examples of among-population variation in insect thermal performance, including latitudinal gradients in chill coma recovery time, variation in energy consumption and metabolic biochemistry, rapid changes in thermal biology with range expansion in invasive and introduced species, and potential constraints on variation in thermal performance traits. This review highlights that while there is substantial evidence for among-population variation that is generally correlated with local climate regimes, neither the underlying mechanisms nor the implications for whole-animal fitness in the field are well understood. We also discuss the potential limitations of interpreting evolved variation among populations and argue for a genes-to-environment approach to population-level variation in thermal biology of insects.
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