Flight metabolic rate has contrasting effects on dispersal in the two sexes of the Glanville fritillary butterfly

Abstract

Evolution of dispersal is affected by context-specific costs and benefits. One example is sex-biased dispersal in mammals and birds. While many such patterns have been described, the underlying mechanisms are poorly understood. Here, we study genetic and phenotypic traits that affect butterfly flight capacity and examine how these traits are related to dispersal in male and female Glanville fritillary butterflies (Melitaea cinxia). We performed two mark-recapture experiments to examine the associations of individuals' peak flight metabolic rate (MR(peak)) and Pgi genotype with their dispersal in the field. In a third experiment, we studied tethered flight in the laboratory. MR(peak) was negatively correlated with dispersal distance in males but the trend was positive in females, and the interaction between MR(peak) and sex was significant for long-distance dispersal. A similar but nonsignificant trend was found in relation to molecular variation at Pgi, which encodes a glycolytic enzyme: the genotype associated with high MR(peak) tended to be less dispersive in males but more dispersive in females. The same pattern was repeated in the tethered flight experiment: the relationship between MR(peak) and flight duration was positive in females but negative in males. These results suggest that females with high flight capacity are superior in among-population dispersal, which facilitates the spatial spreading of their reproductive effort. In contrast, males with high flight capacity may express territorial behaviour, and thereby increase the number of matings, whereas inferior males may be forced to disperse. Thus, flight capacity has opposite associations with dispersal rate in the two sexes.

High genetic load in an old isolated butterfly population

“…In the Glanville fritillary, FMR and dispersal rate in the field are strongly correlated (66), and hence reduced FMR in PT could be interpreted as being an adaptation to an isolated island, where high dispersal rate is most likely selected against (67,68). However, the local adaptation hypothesis is not supported by the observation that high FMR has contrasting effects on dispersal propensity in the two sexes; only females with high FMR are more likely to disperse, whereas males with high FMR are actually less dispersive than males with low FMR, but the former benefit from high FMR through their superior capacity to acquire mates in the natal population (69). In the PT population, FMR was similarly reduced in both sexes.…”

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

“…Flight motivation can be assumed to be governed by different factors in females and males, for which the function of flight differs greatly (Niitepõld et al. 2011). In short, females fly to find suitable oviposition sites (once mated), while males fly to keep a mating territory and to look for mates (both “perching” and “patrolling” male mate‐location strategies are observed in the Glanville fritillary; Boggs and Nieminen 2004).…”

“…1996; Niitepõld et al. 2011), and the longest recorded distances to newly colonized habitats are 4–5 km (van Nouhuys and Hanski 2002). Movement distances and the FMR (rate of flight metabolism) vary greatly among individuals, but FMR is repeatable within an individual ( r  = 0.46–0.91; Niitepõld and Hanski 2013) and significantly heritable (Mattila and Hanski 2014).…”

Aging, Life Span, and Energetics under Adult Dietary Restriction in Lepidoptera

“…Apart from routine movements during foraging, mate discovery, courtship, and egg laying, flight enables dispersal to potentially more favorable areas (Zera and Denno 1997). Individual variation in flight metabolic rate (FMR) and peak metabolic rate (PMR) have fitness implications and have been shown to be tightly associated with dispersal rate in the Glanville fritillary butterfly (Melitaea cinxia, Nymphalidae; Haag et al 2005;Niitepõld et al 2009;Niitepõld et al 2011). Insect flight energetics is also directly linked to the roles of insects as disease vectors, agricultural pests, and pollinators.…”