Fosfoglukoosi-isomeraasilokuksen (Pgi) molekyylivariaation yhteys täpläverkkoperhosen migraatioalttiuteen

Habitat fragmentation produces patches of suitable habitat surrounded by unfavourable matrix habitat. A species may persist in such a fragmented landscape in an equilibrium between the extinctions and recolonizations of local populations, thus forming a metapopulation. Migration between local populations is necessary for the long-term persistence of a metapopulation. The Glanville fritillary butterfly (Melitaea cinxia) forms a metapopulation in the Åland islands in Finland. There is migration between the populations, the extent of which is affected by several environmental factors and variation in the phenotype of individual butterflies. Different allelic forms of the glycolytic enzyme phosphoglucose isomerase (Pgi) has been identified as a possible genetic factor influencing flight performance and migration rate in this species. The frequency of a certain Pgi allele, Pgi-f, follows the same pattern in relation to population age and connectivity as migration propensity. Furthermore, variation in flight metabolic performance, which is likely to affect migration propensity, has been linked to genetic variation in Pgi or a closely linked locus. The aim of this study was to investigate the association between Pgi genotype and the migration propensity in the Glanville fritillary both at the individual and population levels using a statistical modelling approach. A mark-release-recapture (MRR) study was conducted in a habitat patch network of M. cinxia in Åland to collect data on the movements of individual butterflies. Larval samples from the study area were also collected for population level examinations. Each butterfly and larva was genotyped at the Pgi locus. The MRR data was parameterised with two mathematical models of migration: the Virtual Migration Model (VM) and the spatially explicit diffusion model. VM model predicted and observed numbers of emigrants from populations with high and low frequencies of Pgi-f were compared. Posterior predictive data sets were simulated based on the parameters of the diffusion model. Lack-of-fit of observed values to the model predicted values of several descriptors of movements were detected, and the effect of Pgi genotype on the deviations was assessed by randomizations including the genotype information. This study revealed a possible difference in the effect of Pgi genotype on migration propensity between the two sexes in the Glanville fritillary. The females with and males without the Pgi-f allele moved more between habitat patches, which is probably related to differences in the function of flight in the two sexes. Females may use their high flight capacity to migrate between habitat patches to find suitable oviposition sites, whereas males may use it to acquire mates by keeping a territory and fighting off other intruding males, possibly causing them to emigrate. The results were consistent across different movement descriptors and at the individual and population levels. The effect of Pgi is likely to be dependent on the structure of the landscape and the prevailing environmental conditions.Habitat fragmentation produces patches of suitable habitat surrounded by unfavourable matrix habitat. A species may persist in such a fragmented landscape in an equilibrium between the extinctions and recolonizations of local populations, thus forming a metapopulation. Migration between local populations is necessary for the long-term persistence of a metapopulation. The Glanville fritillary butterfly (Melitaea cinxia) forms a metapopulation in the Åland islands in Finland. There is migration between the populations, the extent of which is affected by several environmental factors and variation in the phenotype of individual butterflies. Different allelic forms of the glycolytic enzyme phosphoglucose isomerase (Pgi) has been identified as a possible genetic factor influencing flight performance and migration rate in this species. The frequency of a certain Pgi allele, Pgi-f, follows the same pattern in relation to population age and connectivity as migration propensity. Furthermore, variation in flight metabolic performance, which is likely to affect migration propensity, has been linked to genetic variation in Pgi or a closely linked locus. The aim of this study was to investigate the association between Pgi genotype and the migration propensity in the Glanville fritillary both at the individual and population levels using a statistical modelling approach. A mark-release-recapture (MRR) study was conducted in a habitat patch network of M. cinxia in Åland to collect data on the movements of individual butterflies. Larval samples from the study area were also collected for population level examinations. Each butterfly and larva was genotyped at the Pgi locus. The MRR data was parameterised with two mathematical models of migration: the Virtual Migration Model (VM) and the spatially explicit diffusion model. VM model predicted and observed numbers of emigrants from populations with high and low frequencies of Pgi-f were compared. Posterior predictive data sets were simulated based on the parameters of the diffusion model. Lack-of-fit of observed values to the model predicted values of several descriptors of movements were detected, and the effect of Pgi genotype on the deviations was assessed by randomizations including the genotype information. This study revealed a possible difference in the effect of Pgi genotype on migration propensity between the two sexes in the Glanville fritillary. The females with and males without the Pgi-f allele moved more between habitat patches, which is probably related to differences in the function of flight in the two sexes. Females may use their high flight capacity to migrate between habitat patches to find suitable oviposition sites, whereas males may use it to acquire mates by keeping a territory and fighting off other intruding males, possibly causing them to emigrate. The results were consistent across different movement descriptors and at the individual and population levels. The effect of Pgi is likely to be dependent on the structure of the landscape and the prevailing environmental conditions

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

Aposematic animals advertise their toxicity or unpalatability with bright warning coloration. However, acquiring and maintaining chemical defenses can be energetically costly, and consequent associations with other important traits could shape chemical defense evolution. Here, we have tested whether chemical defenses are involved in energetic trade-offs with other traits, or whether the levels of chemical defenses are condition dependent, by studying associations between biosynthesized cyanogenic toxicity and a suite of key life-history and fitness traits in a Heliconius butterfly under a controlled laboratory setting. Heliconius butterflies are well known for the diversity of their warning color patterns and widespread mimicry and can both sequester the cyanogenic glucosides of their Passiflora host plants and biosynthesize these toxins de novo. We find energetically costly life-history traits to be either unassociated or to show a general positive association with biosynthesized cyanogenic toxicity. More toxic individuals developed faster and had higher mass as adults and a tendency for increased lifespan and fecundity. These results thus indicate that toxicity level of adult butterflies may be dependent on individual condition, influenced by genetic background or earlier conditions, with maternal effects as one strong candidate mechanism. Additionally, toxicity was higher in older individuals, consistent with previous studies indicating accumulation of toxins with age. As toxicity level at death was independent of lifespan, cyanogenic glucoside compounds may have been recycled to release resources relevant for longevity in these long-living butterflies. Understanding the origins and maintenance of variation in defenses is necessary in building a more complete picture of factors shaping the evolution of aposematic and mimetic systems.Peer reviewe

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimetic Heliconius butterfly

Chemical defences against predators underlie the evolution of aposematic coloration and mimicry, which are classic examples of adaptive evolution. Surprisingly little is known about the roles of ecological and evolutionary processes maintaining defence variation, and how they may feedback to shape the evolutionary dynamics of species. Cyanogenic Heliconius butterflies exhibit diverse warning color patterns and mimicry, thus providing a useful framework for investigating these questions. We studied intraspecific variation in de novo biosynthesized cyanogenic toxicity and its potential ecological and evolutionary sources in wild populations of Heliconius erato along environmental gradients, in common-garden broods and with feeding treatments. Our results demonstrate substantial intraspecific variation, including detectable variation among broods reared in a common garden. The latter estimate suggests considerable evolutionary potential in this trait, although predicting the response to selection is likely complicated due to the observed skewed distribution of toxicity values and the signatures of maternal contributions to the inheritance of toxicity. Larval diet contributed little to toxicity variation. Furthermore, toxicity profiles were similar along steep rainfall and altitudinal gradients, providing little evidence for these factors explaining variation in biosynthesized toxicity in natural populations. In contrast, there were striking differences in the chemical profiles of H. erato from geographically distant populations, implying potential local adaptation in the acquisition mechanisms and levels of defensive compounds. The results highlight the extensive variation and potential for adaptive evolution in defense traits for aposematic and mimetic species, which may contribute to the high diversity often found in these systems.Peer reviewe

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

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

Täpläverkkoperhosen lentoaineenvaihdunta ja liikkuminen : perimästä populaatioihin

Loss and fragmentation of natural habitats and changing climate pose severe threats to biodiversity. The ability of populations and species to respond to these challenges by dispersing across landscapes is imperative for their long-term survival. Dispersal is also the main mechanism leading to gene flow, and dispersal is therefore essential for maintaining genetic diversity and adaptive potential of populations. In this thesis, I build upon the vast knowledge gained during more than two decades of research on the Glanville fritillary butterfly (Melitaea cinxia), aiming towards a better understanding of the mechanisms and processes that shape dispersal in this model species. Previous studies have demonstrated a strong positive correlation between flight metabolic rate (FMR) and dispersal distances in the field. Here, I use FMR as a measure of flight and dispersal capacity. I study dispersal from multiple perspectives and use a variety of methods to address questions ranging from the genetic basis and heritability of flight capacity to interactions between genes, physiology and environment in affecting flight and dispersal. Variation in dispersal capacity and how it influences population and metapopulation-level processes are examined. Finally, I use a natural experiment to study the genetic and fitness consequences of complete lack of gene flow into a small isolated island population of the Glanville fritillary. Key findings of the thesis include the demonstration of significant heritable genetic variation in FMR, indicating that FMR and therefore dispersal capacity has the potential to respond to selection due to e.g. habitat fragmentation and climate change. In a genome-wide gene expression study, 755 genes were significantly up- or down-regulated in response to an experimental flight treatment. Differences between sexes and two contrasting populations in flight-induced gene expression in major metabolic pathways were associated with differences in FMR, suggesting that similar molecular mechanisms influence both gender and population differences in flight performance. An experiment examining changes in butterfly body temperature during flight showed that FMR and tolerance of high temperatures may significantly influence flight performance in different thermal environments. At the metapopulation level, male and female butterflies differed in the effects of flight capacity on realized dispersal rate between local populations, with likely consequences for the assortment of dispersive genotypes across fragmented landscapes. The small and completely isolated island population of the Glanville fritillary exhibited significant loss of genetic diversity and substantially reduced fitness. Complete and instant fitness recovery in hybrids strongly suggests that reduced population viability is due to high genetic load. This small isolated population serves as an example of the innumerable remnant populations in human-fragmented landscapes, in which extinction risk may increase due to lack of gene flow. This work contributes to the mechanistic understanding of dispersal (and its importance) in fragmented and isolated populations and in changing environmental conditions in the Glanville fritillary butterfly. Many findings of this thesis are also likely to be applicable to other similar species, particularly those living in fragmented landscapes.Luonnon elinympäristöjen häviäminen ja pirstoutuminen sekä muuttuva ilmasto ovat yhä enenevissä määrin uhka maapallon luonnon monimuotoisuudelle. Eliökantojen ja lajien kyky ja mahdollisuus liikkua elinalueelta toiselle on välttämätön edellytys niiden pitkäaikaiselle selviytymiselle. Yksilöiden liikkuminen eliökantojen välillä mahdollistaa geenivirran, mikä on välttämätöntä populaatioiden geneettisen monimuotoisuuden ja niiden sopeutumiskyvyn säilymiselle. Tässä väitöskirjassa tarkastellaan täpläverkkoperhosen (Melitaea cinxia) liikkumista ja lentokykyyn vaikuttavia tekijöitä. Tutkimus perustuu siihen laajaan tietämykseen, joka on kertynyt tämän ekologisen tutkimuksen mallilajiksi muotoutuneen perhoslajin biologiasta yli kahden vuosikymmenen aikana. Aiemmat tutkimukset ovat osoittaneet, että perhosen lentoaineenvaihdunnan nopeus on vahvasti yhteydessä perhosten maastossa liikkumiin matkoihin. Käytän tässä tutkimuksessa lentoaineenvaihdunnan nopeutta perhosten lento- ja liikkumiskyvyn mittana. Perhosten liikkumista ja lentokykyä tutkitaan useasta eri näkökulmasta monilla eri menetelmillä. Tutkimusten tarkoituksena on selvittää liikkumisen perinnöllistä taustaa, liikkumiseen vaikuttavia geenejä sekä fysiologisia ja ympäristöstä johtuvia tekijöitä. Liikkumisen syy- ja seuraussuhteita tutkitaan myös täpläverkkoperhosen luonnonpopulaatioissa, sekä pirstoutuneessa elinympäristöverkostossa että täysin eristyneessä pienessä saaripopulaatiossa. Tulokset osoittivat, että lentoaineenvaihdunnan nopeus periytyy sukupolvelta toiselle. Luonnon valinta voi siten muokata tätä ominaisuutta sellaiseen suuntaan, joka lisää yksilöiden kelpoisuutta muuttuneissa ympäristöolosuhteissa esimerkiksi elinympäristön pirstoutumisen tai ilmastonmuutoksen seurauksena. Hyönteisten lento kuluttaa erityisen paljon energiaa, ja tulokset osoittivat, että 755 geenin ilmentyminen muuttui merkitsevästi 15 minuutin aktiivisen lennon seurauksena. Solujen tärkeisiin aineenvaihdunta- ja stressivastetoimintoihin liittyvien geenien aktiivisuus lennon jälkeen oli yhteydessä lentoaineenvaihdunnan nopeuteen, mikä viittaa näiden toimintojen merkitykseen lentosuorituksen mahdollistavina ja sitä mahdollisesti rajoittavina tekijöinä. Perhosten lentoaineenvaihdunnan nopeuden ja korkeiden lämpötilojen kestokyvyn osoitettiin vaikuttavan lentokykyyn vaihtelevissa ympäristöoloissa. Lentokykyyn vaikuttavien tekijöiden ja lennon mekanismien parempi ymmärtäminen voi auttaa ennustamaan muuttuvien ympäristöolosuhteiden vaikutuksia perhosten ja muiden samankaltaisten lajien liikkumiskykyyn ja siten niiden populaatioiden menestymiseen. Yksilöiden väliset erot lentokyvyssä vaikuttivat päinvastaisella tavalla koiraiden ja naaraiden liikkeisiin pirstoutuneessa elinympäristössä: naaraat joilla oli hyvä lentokyky liikkuivat enemmän populaatioiden välillä, kun taas lentokyvyltään parhaat koiraat jäivät todennäköisimmin syntymäkedolleen. Sukupuolten väliset erot johtunevat hyvän lentokyvyn erilaisista vaikutuksista koiraiden ja naaraiden kelpoisuuteen, mutta näillä eroilla on myös vaikutusta lentokyvyltään erilaisten yksilöiden jakautumiseen populaatioverkoston alueella. Pitkään täysin eristyksissä olleessa perhospopulaatiossa perimä oli köyhtynyt ja perhosten kelpoisuus merkittävästi alentunut, mikä korostaa populaatioiden välisten liikkeiden ja geenivirran merkitystä populaatioiden elinvoimaisuudelle. Tutkittu saaripopulaatio toimii esimerkkinä sellaisesta kasvaneesta sukupuuttoriskistä, joka uhkaa mitä luultavimmin lukemattomia maankäytössä tapahtuneiden muutosten seurauksena täysin eristyksiin jääneitä pieniä populaatioita

Data_Thermal biology of flight in a butterfly_Ecology and Evolution 2015

Data from: Thermal biology of flight in a butterfly: genotype, flight metabolism and environmental conditions, Mattila, Anniina L. K., Ecology and Evolution, 2015. Data includes butterfly flight metabolic rate data, butterfly body temperature data measured in semi-natural conditions (on two occasions for each individual; denoted by flight1 and flight2), data on environmental conditions during body temperature measurements, and genotype data at candidate gene loci. Experiments were made with field-collected, common garden-reared Glanville fritillary (Melitaea cinxia) butterflies

Mattila_Hanski_Heritability of flight and resting metabolic rate_data

The file includes family and rearing information as well as metabolic rate, morphological and Pgi genotype data for individual butterflies in the first and second generation. Descriptions of data columns are specified in the title row of the data file

Data from: Heritability of flight and resting metabolic rates in the Glanville fritillary butterfly

Dispersal capacity is a key life history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate is known to correlate strongly with dispersal rate. We modeled a two-generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that flight metabolic rate is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus flight metabolic rate has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context-dependent, as in stressful thermal conditions environmentally induced variation dominated over additive genetic effects. There was no heritability in resting metabolic rate, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal-related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats

The effect of summer drought on the predictability of local extinctions in a butterfly metapopulation

Abstract The ecological impacts of extreme climatic events on population dynamics and/or community composition are profound and predominantly negative. Here, using extensive data of an ecological model system, we test whether predictions from ecological models remain robust when environmental conditions are outside the bounds of observation. First, we report a 10-fold demographic decline of the Glanville fritillary butterfly metapopulation on the Åland islands (Finland). Next, using climatic and satellite data we show that the summer of 2018 was an anomaly in terms of water balance and vegetation productivity indices across the habitats of the butterfly, and demonstrate that population growth rates are strongly associated with spatio-temporal variation in climatic water balance. Finally, we demonstrate that covariates that have previously been identified to impact the extinction probability of local populations in this system are less informative when populations are exposed to (severe) drought during the summer months. Our results highlight the unpredictable responses of natural populations to extreme climatic events. Article impact statement: A demographic crash of an iconic metapopulation reveals that extreme climatic events reduce the value of predictive models. This article is protected by copyright. All rights reservedPeer reviewe