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ABSTRACT: In insects, the length of larval development time typically influences adult body size and individual fitness, and hence development time can be expected to respond in an adaptive manner to variation in environmental conditions. In the wild, larval growth may be influenced by individual condition, which can be affected by population-level parameters such as population density and abundance and quality of resources. We sampled larvae of the Glanville fritillary butterfly (Melitaea cinxia) from 514 local populations across a large metapopulation before the winter diapause and reared the larvae in common garden conditions after diapause. Here, we report that small post-diapause larvae prolonged their development via an extra larval instar, apparently to compensate for their 'bad start' after diapause. The number of instars was additionally a plastic response to environmental conditions, as the frequency of the extra instar increased under cooler thermal conditions. The benefit of the extra instar is clear, as it allows individuals to develop into larger adults, but the cost is delayed adult eclosion, which is likely to select against the extra instar especially in males, in which early eclosion is critical for mating success. In support of this, the frequency of the extra instar was significantly lower in males (7%) than in females (42%). Polymorphisms in three genes, serpin-1, vitellin-degrading protease precursor and phosphoglucose isomerase, which are known to influence development in insects, were associated with the occurrence of the extra instar. At the level of local populations, the frequency of the extra instar was higher in newly established populations than that in old local ones, possibly reflecting maternal effects, as new populations are often established by females with heavy investment in dispersal. The frequency of the extra instar in turn correlated with the change in population size over 1 year and the risk of local extinction in the natural metapopulation of the Glanville fritillary. Our results highlight the importance of the physiological condition of individuals in shaping subsequent life-history events and even population dynamics.
Journal of Animal Ecology 01/2013; · 4.94 Impact Factor
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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.
Journal of Experimental Biology 12/2012; · 3.00 Impact Factor
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ABSTRACT: 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.
Molecular Ecology 03/2012; · 5.52 Impact Factor
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EMBO Reports 11/2011; 12(11):1089-93. · 7.36 Impact Factor
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ABSTRACT: Ecology Letters (2011) 14: 1025-1034 ABSTRACT: Evolutionary changes in natural populations are often so fast that the evolutionary dynamics may influence ecological population dynamics and vice versa. Here we construct an eco-evolutionary model for dispersal by combining a stochastic patch occupancy metapopulation model with a model for changes in the frequency of fast-dispersing individuals in local populations. We test the model using data on allelic variation in the gene phosphoglucose isomerase (Pgi), which is strongly associated with dispersal rate in the Glanville fritillary butterfly. Population-specific measures of immigration and extinction rates and the frequency of fast-dispersing individuals among the immigrants explained 40% of spatial variation in Pgi allele frequency among 97 local populations. The model clarifies the roles of founder events and gene flow in dispersal evolution and resolves a controversy in the literature about the consequences of habitat loss and fragmentation on the evolution of dispersal.
Ecology Letters 07/2011; 14(10):1025-34. · 17.56 Impact Factor
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Ilkka Hanski
AMBIO A Journal of the Human Environment 05/2011; 40(3):248-55. · 2.03 Impact Factor
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ABSTRACT: Summary1. Genetic polymorphism in the gene phosphoglucose isomerase (Pgi) encoding for a glycolytic enzyme has been shown to affect many traits in adult insects, including flight metabolism, running speed, fecundity and longevity, but it is not known to what extent Pgi genotypic effects are consistent across different life stages.2. In the Glanville fritillary butterfly, heterozygous AC adult individuals for a single nucleotide polymorphism (SNP) (AA111) in the coding region of Pgi have superior fitness to the common homozygotes (AA) in practically all life-history traits.3. Here, we studied associations between Pgi SNP AA111 and larval and pupal weights, larval development time in three different temperatures and adult longevity. Small body size and limited mobility of larvae offer little buffer against changes in ambient temperature; hence, temperature is expected to affect greatly larval growth and development.4. In contrast to adults, larval performance was superior in AA homozygotes in two respects. First, survival was higher in AA homozygotes under stressful conditions, represented by the low-temperature treatment in which survival was generally low. Second, the AA homozygotes had heavier pupae. In spite of the latter result, adult life span was longer in the AC heterozygotes, in support of previous studies.5. The results on larval growth are consistent with the hypothesis of a trade-off between thermal stability and kinetic efficiency between the different isoforms of the PGI enzyme, but the results also indicate unexpected differences in the genotypic effects at different life stages.
Functional Ecology 04/2011; 25(5):1032 - 1039. · 4.57 Impact Factor
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ABSTRACT: In fragmented landscapes, small populations frequently go extinct and new ones are established with poorly understood consequences for genetic diversity and evolution of life history traits. Here, we apply functional genomic tools to an ecological model system, the well-studied metapopulation of the Glanville fritillary butterfly. We investigate how dispersal and colonization select upon existing genetic variation affecting life history traits by comparing common-garden reared 2-day adult females from new populations with those from established older populations. New-population females had higher expression of abdomen genes involved in egg provisioning and thorax genes involved in the maintenance of flight muscle proteins. Physiological studies confirmed that new-population butterflies have accelerated egg maturation, apparently regulated by higher juvenile hormone titer and angiotensin converting enzyme mRNA, as well as enhanced flight metabolism. Gene expression varied between allelic forms of two metabolic genes (Pgi and Sdhd), which themselves were associated with differences in flight metabolic rate, population age and population growth rate. These results identify likely molecular mechanisms underpinning life history variation that is maintained by extinction-colonization dynamics in metapopulations.
Molecular Ecology 03/2011; 20(9):1813-28. · 5.52 Impact Factor
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ABSTRACT: Aim We investigated whether the largest river (Mangoro) on the east coast of Madagascar acts as a barrier to dispersal in dung beetles by comparing species composition and genetic differentiation of the most common species on the two banks of the river. Moreover, by analysing the current geographical ranges of all wet forest dung beetle species, possible long-term effects of the largest rivers on the distribution of species were assessed.Location Madagascar.Methods Dung beetles were sampled with baited pitfall traps at a downstream and an upstream locality on the two banks of the Mangoro River. The most common species, Nanos binotatus (Canthonini), was sequenced for cytochrome c oxidase subunit I (COI; 804 bp) to characterize within-population diversity and between-population genetic differentiation. For the analysis of species geographical range boundaries in relation to the position of the largest rivers on the east coast, a database including all the records for 158 wet forest species was used. The congruence of species range boundaries with the positions of the rivers was tested with a randomization test.Results All common species were found on both sides of the Mangoro River. In Nanos binotatus, haplotype and nucleotide diversities ranged from 0.25 to 0.85 and 0.001 to 0.01, respectively. Population differentiation was high and significant in all comparisons (P < 0.01; average FST = 0.61). The differentiation was not significantly higher across than along the river, as would be expected by the riverine barrier hypothesis. There was no indication that the range boundaries of wet forest dung beetle species would generally coincide with the largest rivers in eastern Madagascar.Main conclusions The results provide little support for the riverine barrier hypothesis as an explanation for the current range boundaries of dung beetles in eastern Madagascar. However, extensive deforestation of the coastal regions in eastern Madagascar may have caused a great shrinkage of the ranges of many forest-dwelling species. Thus the present-day distributions may not reflect accurately the patterns of the past geographical ranges of the species.
Journal of Biogeography 02/2011; 38(6):1098 - 1108. · 4.54 Impact Factor
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Insects. 01/2011;
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ABSTRACT: We construct a model that combines extinction-colonization dynamics with the dynamics of local adaptation in a network of habitat patches of dissimilar qualities. We derive a deterministic approximation for the stochastic model that allows the calculation of patch-specific incidences of occupancy and levels of adaptation at steady state. Depending on (i) the strength of local selection, (ii) the amount of genetic variance, (iii) the demographic cost of maladaptation, (iv) the spatial scale of gene flow, and (v) the amount of habitat heterogeneity, the model predicts adaptation at different spatial scales. Local adaptation is predicted when there is much genetic variance and strong selection, while network-level adaptation occurs when the demographic cost of maladaptation is low. For little genetic variance and high cost of maladaptation, the model predicts network-level habitat specialization in species with long-range migration but an intermediate scale of adaptation (mosaic specialization) in species with short-range migration. In fragmented landscapes, the evolutionary dynamics of adaptation may both decrease and enhance metapopulation viability in comparison with no evolution. The model can be applied to real patch networks with given sizes, qualities, and spatial positions of habitat patches.
The American Naturalist 01/2011; 177(1):29-43. · 4.72 Impact Factor
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ABSTRACT: The amount and spatial distribution of genetic variation that is maintained in a metapopulation depends critically on the colonization process. Here, we use molecular markers to determine the number and genetic relatedness of individuals establishing new local populations in a large metapopulation of the Glanville fritillary butterfly Melitaea cinxia. The empirical results are compared with the predictions of a dispersal model based on a diffusion approximation of correlated random walk, which serves as a base-line hypothesis about the rate and pattern of colonization. The results show that half of the new local populations consisted of a single larval group of full sibs and hence necessarily of the offspring of a single female. If the colonization involved two or more larval groups, these were usually oviposited by two different females that were unrelated to each other. The pattern of colonizations is thus intermediate between the propagule pool and the migrant pool models. These results elucidate the generation of genetic stochasticity, which may influence the dynamics of small populations. The dispersal model predicted well the pattern of habitat occupancy and the pattern of colonizations in relation to landscape structure, though which particular habitat patches became colonized was influenced also by measures of habitat quality not included in the model.
Oikos 12/2010; 120(9):1357 - 1365. · 3.06 Impact Factor
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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.
Oecologia 12/2010; 165(4):847-54. · 3.41 Impact Factor
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ABSTRACT: Madagascar has an exceptionally large fauna of more than 250 species of endemic dung beetles. Based on molecular phylogenies, the species descend from eight independent overseas colonisations, of which four have given rise to big radiations. Here, we analyse the tribe Canthonini with three parallel radiations following the respective colonisations at 64-44 Mya (Arachnodes-Epilissus, 101 species), 30-19 Mya (Epactoides, 37 species), and 24-15 Mya (Apotolamprus-Nanos, 61 species). All three radiations have taken place in forests, but there are also substantial differences between them. The oldest radiation exhibits the greatest ecological diversification, including monophyletic groups of primate and cattle dung specialists and multiple shifts to arboreal foraging. Analysis of pairs of sister species suggests allopatric speciation in the oldest and the youngest, apparently non-adaptive, radiations, whereas in Epactoides closely related species have diverged ecologically and have largely overlapping geographical ranges, suggestive of adaptive radiation in parapatry or regional sympatry.
Molecular Phylogenetics and Evolution 11/2010; 57(2):710-27. · 3.61 Impact Factor
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ABSTRACT: Aims We have compared local (alpha) and regional (beta) species diversities of dung beetles in wet forests in the main tropical regions including Madagascar. Madagascar is exceptional in lacking native large herbivorous mammals which produce the key resource for dung beetles elsewhere.Location Central and South America, mainland Africa, Madagascar and Southeast Asia.Methods Trapping data on dung beetles and data on mammalian faunas were obtained from published and unpublished studies. We used our original data for Madagascar.Results Species richness of dung beetles and that of large-bodied (> 15 mm length) species in particular were highly significantly explained by the regional number of large-bodied (> 10 kg) mammals (R2 from 50 to 80%). For a given pairwise spatial distance between two communities, beta diversity was significantly higher in Madagascar than elsewhere, explaining the very high total species richness in Madagascar in spite of low local diversity.Main conclusion The presence and numbers of large herbivorous mammals greatly influence the species richness of dung beetles in tropical wet forests. The lack of native large herbivores rather than a limited species pool explains the low local diversity in Madagascar. Exceptionally high beta diversity in Madagascar suggests a pattern of old radiation involving extensive allopatric speciation.
Global Ecology and Biogeography. 06/2010; 19(6):886 - 894.
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Journal of Tropical Ecology 01/2010; · 1.40 Impact Factor
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ABSTRACT: The high Arctic has the world's simplest terrestrial vertebrate predator–prey community, with the collared lemming being the single main prey of four predators, the snowy owl, the Arctic fox, the long-tailed skua, and the stoat. Using a 20-year-long time series of population densities for the five species and a dynamic model that has been previously parameterized for northeast Greenland, we analyzed the population and community level consequences of the ongoing and predicted climate change. Species' responses to climate change are complex, because in addition to the direct effects of climate change, which vary depending on species' life histories, species are also affected indirectly due to, e.g., predator–prey interactions. The lemming–predator community exemplifies these complications, yet a robust conclusion emerges from our modeling: in practically all likely scenarios of how climate change may influence the demography of the species, climate change increases the length of the lemming population cycle and decreases the maximum population densities. The latter change in particular is detrimental to the populations of the predators, which are adapted to make use of the years of the greatest prey abundance. Therefore, climate change will indirectly reduce the predators' reproductive success and population densities, and may ultimately lead to local extinction of some of the predator species. Based on these results, we conclude that the recent anomalous observations about lack of cyclic lemming dynamics in eastern Greenland may well be the first signs of a severe impact of climate change on the lemming–predator communities in Greenland and elsewhere in the high Arctic.
Global Change Biology 10/2009; 15(11):2634 - 2652. · 6.86 Impact Factor
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ABSTRACT: Summary1. Much of ecological research focuses on the responses of species and species communities to variation in the amount and quality of resources that are required for survival and reproduction. In such research, it is critical to measure the availability of resources in a manner that is relevant in relation to the ecological requirements of the species.2. We have developed a measure for resource availability that integrates the contributions of the number, volume and diversity of resource units to quantify the amount of habitat that is available for a species community. We apply this measure to data on the occurrence of 116 species of wood-decaying polyporous fungi in 47 study plots of boreal forest within an area of 150 × 150 km.3. We show that species richness and pooled abundance of common species is explained well by the number of downed logs, whereas the occurrence of 41 red-listed species is best explained by the total volume of logs and by the abundance of large logs in particular. The occurrence of common species is explained by the local availability of dead wood, whereas the occurrence of red-listed species is additionally affected by the spatial connectivity of the focal forest stand to the surrounding larger expanses of old-growth forest.4. Our results elicit the contrasting ecologies of common and red-listed species in relation to how the number of logs, their size distribution and diversity, and forest connectivity affect species occurrences. The results suggest that the most cost-effective means of preventing further declines of threatened species is to increase the amount of large downed logs through restoration and biodiversity-oriented management in the vicinity of existing areas of natural-like forests.5. Synthesis. Our results illustrate that the most relevant way of measuring resource availability can differ greatly even within a taxonomically coherent community seemingly sharing the same resources. Our approach for modelling resource availability applies to the resources that occur as discrete objects with variation in the size and quality of individual resource units.
Journal of Ecology 09/2009; 97(6):1320 - 1328. · 4.69 Impact Factor
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ABSTRACT: 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.
Ecology 09/2009; 90(8):2223-32. · 4.85 Impact Factor
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ABSTRACT: The Glanville fritillary butterfly (Melitaea cinxia, Nymphalidae) has a large, well-studied metapopulation in the Aland Islands in Finland. Previous studies have found that the common allozyme genotypes at the phosphoglucose isomerase (PGI) locus are associated with individual variation in performance and fitness, with phenotypic data suggesting ongoing balancing selection via heterozygote advantage. Here, we analyze nucleotide polymorphism in the coding region of the Pgi gene. Pgi is exceptionally polymorphic, in contrast to three other metabolic genes (Mdh, Idh, and Gapdh) with low levels of polymorphism. Most of the variation is due to two common haplotype clades, which are highly divergent and exhibit extensive linkage disequilibrium. These two clades correspond to the two most common allozyme alleles previously studied. Molecular tests of selection and coalescence simulations indicate that patterns of nucleotide polymorphism depart from neutrality and are consistent with long-term balancing selection. The split between the two main haplotype clades is estimated to predate the last common ancestor of a clade of five extant Melitaea species. Comparative structural analysis of Pgi polymorphism in M. cinxia and the unrelated Colias eurytheme butterfly suggests a similar but not identical target of balancing selection. Our results indicate convergent evolution between these two species at both the phenotypic and molecular levels.
Molecular Biology and Evolution 09/2009; 27(2):267-81. · 5.55 Impact Factor
