Marjo Saastamoinen

Costs of dispersal

Dispersal costs can be classified into energetic, time, risk and opportunity costs and may be levied directly or deferred during departure, transfer and settlement. They may equally be incurred during life stages before the actual dispersal event through investments in special morphologies. Because costs will eventually determine the performance of dispersing individuals and the evolution of dispersal, we here provide an extensive review on the different cost types that occur during dispersal in a wide array of organisms, ranging from micro‐organisms to plants, invertebrates and vertebrates. In general, costs of transfer have been more widely documented in actively dispersing organisms, in contrast to a greater focus on costs during departure and settlement in plants and animals with a passive transfer phase. Costs related to the development of specific dispersal attributes appear to be much more prominent than previously accepted. Because costs induce trade‐offs, they give rise to covariation between dispersal and other life‐history traits at different scales of organismal organisation. The consequences of (i) the presence and magnitude of different costs during different phases of the dispersal process, and (ii) their internal organisation through covariation with other life‐history traits, are synthesised with respect to potential consequences for species conservation and the need for development of a new generation of spatial simulation models.

A candidate locus for variation in dispersal rate in a butterfly metapopulation

Frequent extinctions of local populations in metapopulations create opportunities for migrant females to establish new populations. In a metapopulation of the Glanville fritillary butterfly (Melitaea cinxia), more mobile individuals are more likely to establish new populations, especially in habitat patches that are poorly connected to existing populations. Here we show that flight metabolic rate and the frequency of a specific allele of the metabolic enzyme phosphoglucose isomerase (pgi) were both highest in newly established, isolated populations. Furthermore, genotypes with this pgi allele had elevated flight metabolic rates. These results suggest that genetic variation in pgi or a closely linked locus has a direct effect on flight metabolism, dispersal rate, and thereby on metapopulation dynamics in this species. These results also contribute to an emerging understanding of the mechanisms by which population turnover in heterogeneous landscapes may maintain genetic and phenotypic variation across populations.

Genotypic and Environmental Effects on Flight Activity and Oviposition in the Glanville Fritillary Butterfly

Adverse environmental conditions constrain active flight and thereby limit reproduction in most insects. Butterflies have evolved various adaptations in order to thermoregulate, allowing females to search for nectar and to oviposit under unfavorable thermal conditions. We studied experimentally and with observational data the effect of low ambient temperatures experienced in the morning on the timing of oviposition and clutch size in the Glanville fritillary butterfly (Melitaea cinxia). Comparisons were made between individuals with different forms of the gene Pgi, encoding the glycolytic enzyme phosphoglucose isomerase, since naturally segregating variation at Pgi is known to be correlated with flight metabolic rate, flight performance, and fecundity. Experiencing low temperature in the morning delayed the initiation of oviposition and decreased clutch size. We used a thermal image camera to measure the thoracic surface temperature of butterflies immediately after voluntary flight. Single nucleotide polymorphism at Pgi was associated with thoracic temperature at low ambient temperatures. This has consequences for reproduction because females that are able to fly at lower ambient temperatures generally initiate oviposition earlier in the afternoon, when the environmental conditions are most favorable and the average egg clutch size is generally largest. These results suggest that variation in physiological and molecular capacity to sustain active flight at low ambient temperature has significant fitness‐related consequences in insects.

Life‐history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly

Abstract 1. Glanville fritillary butterfly (Melitaea cinxia) females lay up to 10 clutches of 50–300 eggs in their lifetime. Clutch size is an important life‐history trait as larval group size affects survival throughout larval development.

Predictive Adaptive Responses: Condition-Dependent Impact of Adult Nutrition and Flight in the Tropical Butterfly Bicyclus anynana

The experience of environmental stress during development can substantially affect an organism’s life history. These effects are often mainly negative, but a growing number of studies suggest that under certain environmental conditions early experience of such stress may yield individuals that are less sensitive to environmental stress later on in life. We used the butterfly Bicyclus anynana to study the effects of limited larval and adult food and forced flight on individual performance measured as reproduction and adult life span. Larvae exposed to food stress showed longer development and produced smaller adults. Thus, they were not able to fully compensate for the food deprivation during development. Females that experienced food stress during development did not increase tolerance for adult food limitation. However, females exposed to food stress during development coped better with forced flight compared with the control group. The apparent absence of costs of flight in poor‐quality females may be a by‐product of an altered body allocation, as females experiencing both food stress treatments had increased thorax ratios, compared with controls, and increased flight performances. The results reveal an important plasticity component to variation in flight performance and suggest that the cost of flight depends on an individual’s internal condition.

Significant effects of Pgi genotype and body reserves on lifespan in the Glanville fritillary butterfly

Individuals with a particular variant of the gene phosphoglucose isomerase (Pgi) have been shown to have superior dispersal capacity and fecundity in the Glanville fritillary butterfly (Melitaea cinxia), raising questions about the mechanisms that maintain polymorphism in this gene in the field. Here, we investigate how variation in the Pgi genotype affects female and male life history under controlled conditions. The most striking effect is the longer lifespan of genotypes with high dispersal capacity, especially in non-reproducing females. Butterflies use body reserves for somatic maintenance and reproduction, but different resources (in thorax versus abdomen) are used under dissimilar conditions, with some interactions with the Pgi genotype. These results indicate life-history trade-offs that involve resource allocation and genotype×environment interactions, and these trade-offs are likely to contribute to the maintenance of Pgi polymorphism in the natural populations.

Mobility and lifetime fecundity in new versus old populations of the Glanville fritillary butterfly

Life history theory often assumes a trade-off between dispersal and reproduction, and such a trade-off is commonly observed in wing-dimorphic insects. The results are less consistent for wing-monomorphic species, for which it is more difficult to assess dispersal capacity and rate. Three replicate experiments were carried out in consecutive years on the Glanville fritillary butterfly in a large outdoor population cage to study the relationship between lifetime egg production and mobility. The experimental material included females originating from newly-established and old populations, as previous studies have shown dispersal capacity to depend on population age. There was a consistent and significant interaction between mobility and population age, such that in newly-established populations mobile females had higher fecundity than less mobile females, while in old populations there was no such relationship. As selection favours individuals with the highest fecundity, selection pressure on mobility is likely to be different between the two population types, which may contribute to maintenance of variation in dispersal rate in the metapopulation as a whole. Several other female traits also affected lifetime fecundity, including lifespan, number of matings and date of eclosion, although these effects were not consistent across the years. These results highlight the importance of conducting experiments in more than one year before generalizing about patterns in life history variation.

Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits

Little is known about variation in gene expression that affects life history traits in wild populations of outcrossing species. Here, we analyse heritability of larval development traits and associated variation in gene expression in the Glanville fritillary butterfly (Melitaea cinxia) across three ecologically relevant temperatures. We studied the development of final‐instar larvae, which is greatly affected by temperature, and during which stage larvae build up most of the resources for adult life. Larval development time and weight gain varied significantly among families sampled from hundreds of local populations, indicating substantial heritable variation segregating in the large metapopulation. Global gene expression analysis using common garden‐reared F2 families revealed that 42% of the >8000 genes surveyed exhibited significant variation among families, 39% of the genes showed significant variation between the temperature treatments, and 18% showed a significant genotype‐by‐environment interaction. Genes with large family and temperature effects included larval serum protein and cuticle‐binding protein genes, and the expression of these genes was closely correlated with the rate of larval development. Significant expression variation in these same categories of genes has previously been reported among adult butterflies originating from newly established versus old local populations, supporting the notion of a life history syndrome put forward based on ecological studies and involving larval development and adult dispersal capacity. These findings suggest that metapopulation dynamics in heterogeneous environments maintain heritable gene expression variation that affects the regulation of life history traits.

The Predictive Adaptive Response: Modeling the Life-History Evolution of the Butterfly Bicyclus anynana in Seasonal Environments

A predictive adaptive response (PAR) is a type of developmental plasticity where the response to an environmental cue is not immediately advantageous but instead is later in life. The PAR is a way for organisms to maximize fitness in varying environments. Insects living in seasonal environments are valuable model systems for testing the existence and form of PAR. Previous manipulations of the larval and the adult environments of the butterfly Bicyclus anynana have shown that individuals that were food restricted during the larval stage coped better with forced flight during the adult stage compared to those with optimal conditions in the larval stage. Here, we describe a state-dependent energy allocation model, which we use to test whether such a response to food restriction could be adaptive in nature where this butterfly exhibits seasonal cycles. The results from the model confirm the responses obtained in our previous experimental work and show how such an outcome was facilitated by resource allocation patterns to the thorax during the pupal stage. We conclude that for B. anynana, early-stage cues can direct development toward a better adapted phenotype later in life and, therefore, that a PAR has evolved in this species.

Weight and nutrition affect pre-mRNA splicing of a muscle gene associated with performance, energetics and life history.

SUMMARY A fundamental feature of gene expression in multicellular organisms is the production of distinct transcripts from single genes by alternative splicing (AS), which amplifies protein and functional diversity. In spite of the likely consequences for organismal biology, little is known about how AS varies among individuals or responds to body condition, environmental variation or extracellular signals in general. Here we show that evolutionarily conserved AS of troponin-t in flight muscle of adult moths responds in a quantitative fashion to experimental manipulation of larval nutrition and adult body weight. Troponin-t (Tnt) isoform composition is known to affect muscle force and power output in other animals, and is shown here to be associated with the thorax mass-specific rate of energy consumption during flight. Loading of adults with external weights for 5 days caused an AS response nearly identical to equal increases in actual body weight. In addition, there were effects of larval feeding history on adult Tnt isoform composition that were independent of body weight, with moths from poorer larval feeding regimes producing isoform profiles associated with reduced muscle performance and energy consumption rate. Thus, Tnt isoform composition in striated muscle is responsive to both weight-sensing and nutrition-sensing mechanisms, with consequent effects on function. In free-living butterflies, Tnt isoform composition was also associated with activity level and very strongly with the rate of egg production. Overall, these results show that AS of a muscle gene responds in a quantitative fashion to whole-organism variables, which apparently serves to coordinate muscle strength and energy expenditure with body condition and life history.