Thermal biology of flight in a butterfly: genotype, flight metabolism, and environmental conditions

Anniina L K Mattila

doi:10.1002/ece3.1758

Abstract

Knowledge of the effects of thermal conditions on animal movement and dispersal is necessary for a mechanistic understanding of the consequences of climate change and habitat fragmentation. In particular, the flight of ectothermic insects such as small butterflies is greatly influenced by ambient temperature. Here, variation in body temperature during flight is investigated in an ecological model species, the Glanville fritillary butterfly (Melitaea cinxia). Attention is paid on the effects of flight metabolism, genotypes at candidate loci, and environmental conditions. Measurements were made under a natural range of conditions using infrared thermal imaging. Heating of flight muscles by flight metabolism has been presumed to be negligible in small butterflies. However, the results demonstrate that Glanville fritillary males with high flight metabolic rate maintain elevated body temperature better during flight than males with a low rate of flight metabolism. This effect is likely to have a significant influence on the dispersal performance and fitness of butterflies and demonstrates the possible importance of intraspecific physiological variation on dispersal in other similar ectothermic insects. The results also suggest that individuals having an advantage in low ambient temperatures can be susceptible to overheating at high temperatures. Further, tolerance of high temperatures may be important for flight performance, as indicated by an association of heat‐shock protein (Hsp70) genotype with flight metabolic rate and body temperature at takeoff. The dynamics of body temperature at flight and factors affecting it also differed significantly between female and male butterflies, indicating that thermal dynamics are governed by different mechanisms in the two sexes. This study contributes to knowledge about factors affecting intraspecific variation in dispersal‐related thermal performance in butterflies and other insects. Such information is needed for predictive models of the evolution of dispersal in the face of habitat fragmentation and climate change.

Highlights

Loss and fragmentation of natural habitats is the main cause of biodiversity loss and species extinctions (Baillie et al 2004; IUCN 2014)
In the study of Niitepo~ld et al (2009), phosphoglucose isomerase (Pgi) genotype had no significant effect on the probability of flight activity within a short period of time, but individuals with high FMR were significantly more active and less likely to stop flying than low-FMR butterflies. These results suggest that while Pgi genotype, FMR and body temperature at flight are all correlated, body temperature at flight is causally affected by FMR rather than by Pgi genotype
Contrary to what is commonly expected for small butterflies, flight metabolic rate significantly influenced the dynamics of body temperature during flight in male Glanville fritillaries, with likely consequences for fitness and dispersal in varying environmental conditions

Summary

Introduction

Loss and fragmentation of natural habitats is the main cause of biodiversity loss and species extinctions (Baillie et al 2004; IUCN 2014). A key challenge for predicting the biological consequences of habitat fragmentation is to develop mechanistic understanding of individual movements and dispersal, as sufficient dispersal is imperative for population viability in highly fragmented landscapes (Hanski 1999; Ronce 2007). Specific questions in this context include how dispersal is affected by morphological, physiological, and behavioral traits, to what extent, the variation in dispersal rate is governed by genetic versus environmental factors (and genotype 9 environment interactions), and does natural selection affect relevant traits under changing environmental conditions (Nathan et al 2008; Clobert et al 2012).

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Conclusion