The monarch butterfly, Danaus plexippus, is famous for its spectacular annual migration across North America, recent worldwide dispersal, and orange warning coloration. Despite decades of study and broad public interest, we know little about the genetic basis of these hallmark traits. By sequencing 101 monarch genomes from around the globe, we uncover the history of the monarch's evolutionary origin and global dispersal, characterize the genes and pathways associated with migratory behavior, and identify the discrete genetic basis of warning coloration. The results rewrite our understanding of this classic system, showing that D. plexippus was ancestrally migratory and dispersed out of North America to occupy its broad distribution. We find the strongest signatures of selection associated with migration center on flight muscle function, resulting in greater flight efficiency among migratory monarchs, and that variation in monarch warning coloration is controlled by a single myosin gene not previously implicated in insect pigmentation.
Dispersal is a key life-history trait, especially in species inhabiting fragmented landscapes. The process of dispersal is affected by a suite of morphological, physiological, and behavioral traits, all of which have a more or less complex genetic basis and are affected by the prevailing environmental conditions. To be able to identify genetic and phenotypic effects on dispersal, movements have to be recorded over relevant spatial and temporal scales. We used harmonic radar to track free-flying Glanville fritillary butterflies (Melitaea cinxia) released in the field and reconstructed their flight tracks for several hours. Flight track lengths for individual butterflies ranged from tens of meters to several kilometers. Butterflies were most mobile at midday and in intermediate temperatures. Flight metabolic rate (MR), measured prior to the tracking, explained variation in mobility at all scales studied. One-third of the variation in the distance moved in one hour could be attributed to variation in flight MR. Heterozygous individuals at a single nucleotide polymorphism in the phosphoglucose isomerase (Pgi) gene moved longer distances in the morning and at lower ambient temperatures than homozygous individuals. A similar genotype x temperature interaction was found to affect the metabolic rate. Our results establish connections from molecular variation in a single gene to flight physiology and movement behavior at the landscape level. These results indicate a fitness advantage to the heterozygous genotype in low temperatures and suggest a mechanism by which varying environmental conditions maintain genetic polymorphism in populations.
Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences.Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal‐related phenotypes or evidence for the micro‐evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment‐dependent.By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non‐additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non‐equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context‐dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.
We used harmonic radar to track freely flying Glanville fritillary butterfly (Melitaea cinxia) females within an area of 30 ha. Butterflies originated from large and continuous populations in China and Estonia, and from newly established or old (> 5 years) small local populations in a highly fragmented landscape in Finland. Caterpillars were raised under common garden conditions and unmated females were tested soon after eclosion. The reconstructed flight paths for 66 individuals comprised a total distance of 51 km with high spatial resolution. Butterflies originating from large continuous populations and from old local populations in Finland exhibited similar movement behaviors, whereas butterflies originating from newly established local populations in the fragmented landscape in Finland moved significantly more than the others. There was no difference in the lengths of individual flight bouts, but the new-population females flew more frequently, resulting in longer daily movement tracks. The flight activity of all individuals was affected by environmental conditions, peaking at 19 -23°C (depending on population type), in the early afternoon, and during calm weather. Butterflies from all population types showed a strong tendency to follow habitat edges between the open study area and the neighboring woodlands.evolution of dispersal ͉ Glanville fritillary ͉ fight behavior ͉ edge-following ͉ fragmented habitat
SUMMARYMetabolic 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.
SUMMARYHigh peak metabolic rates may provide a 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 therefore be 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 ʻlive fast, die youngʼ may be too simple to explain the complex processes affecting ageing and lifespan.Supplementary material available online at
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.
Stressful conditions can affect resource allocation among different life-history traits. The effect of dietary restriction (DR) on longevity and reproduction has been studied in many species, but we know little about its effects on energetics, especially in flying animals that have high energy demand. We assessed the effects of DR on metabolic rate throughout the entire adult life span in two butterfly species, Colias eurytheme and Speyeria mormonia. We cut the food intake of adult females in half and measured resting metabolic rate (RMR) and flight metabolic rate (FMR) together with body mass repeatedly throughout life. In both species, DR reduced body mass, but mass-corrected FMR was not affected, indicating that flight capacity was retained. DR lowered RMR and reduced fecundity but had no effect on life span. FMR declined with age, but the rate of senescence was not affected by DR. In contrast, aging had a strong negative effect on RMR only in control females, whereas food-restricted females had more stable RMR throughout their lives. The results suggest that flight capacity is conserved during nutritional stress but that investment in flight and survival may negatively affect other important physiological processes when resources are limited.
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