Dispersal and related life history traits in the Glanville fritillary butterfly

Most studies of life history evolution are based on the assumption that species exist at equilibrium and spatially distinct separated populations. In reality, this is rarely the case, as populations are often spatially structured with ephemeral local populations. Therefore, the characteristics of metapopulations should be considered while studying factors affecting life history evolution. Theoretical studies have examined spatial processes shaping the evolution of life history traits to some extent, but there is little empirical data and evidence to investigate model predictions. In my thesis I have tried to bridge the gap between theoretical and empirical studies by using the well-known Glanville fritillary (Melitaea cinxia) metapopulation as a model system. The long-term persistence of classic metapopulations requires sufficient dispersal to establish new local populations to compensate for local extinctions. Previous studies on the Glanville fritillary have shown that females establishing new populations are not a random sample from the metapopulation, but they are in fact more dispersive than females in old populations. Many other life-history traits, such as body size, fecundity and lifespan, may be related to dispersal rate. Therefore, I examined a range of correlated traits for their evolutionary and ecological consequences. I was particularly interested in how the traits vary under natural environmental conditions, hence all studies were conducted in a large (32 x 26 m) outdoor population cage built upon a natural habitat patch. Individuals for the experiments were sampled from newly-established and old populations within a large metapopulation. Results show that females originating from newly-established populations had higher within-habitat patch mobility than females from old populations. I showed that dispersal rate is heritable and that flight activity is related to variation in a gene encoding the glycolytic enzyme phosphoglucose isomerase. Both among-individual and among-population variation in dispersal are correlated with the reproductive performance of females, though I found no evidence for a trade-off between dispersal and fecundity in terms of lifetime egg production or clutch size. Instead, the results suggest that highly dispersive females from newly-established populations have a shorter lifespan than females from old populations, and that dispersive females may pay a cost in terms of reduced lifetime reproductive success due to increased time spent outside habitat patches. In summary, the results of this thesis show that genotype-dependent dispersal rate correlates with other life history traits in the Glanville fritillary, and that the rapid turnover of local populations (extinctions and re-colonisations) is likely to be the mechanism that maintains phenotypic variation in many life history traits at the metapopulation level.Perinteisissä elinkiertoekologisissa tutkimuksissa oletetaan usein, että lajit esiintyvät toisistaan erillisinä, yksittäisinä populaatioina. Todellisuudessa tämä olettamus pitää vain harvoin paikkansa. Populaatioiden välillä on usein vuorovaikutusta yksilöiden liikkuessa yhdestä populaatiosta toiseen. Metapopulaatioiden erityispiirteet tulisi siis ottaa huomioon myös elinkiertoekologisissa tutkimuksissa. Teoreettisissa tutkimuksissa populaatioiden tilarakenne on jossain määrin huomioitu, mutta näitä teoreettisia tarkasteluja on vain harvoin pyritty testaamaan empiirisesti. Väitöskirjatyössäni olenkin pyrkinyt kuromaan umpeen aukkoa teoreettisten ja empiiristen tutkimusten välillä käyttäen apuna paljon tutkittua täpläverkkoperhosmetapopulaatiota Ahvenanmaalla. Yksittäisillä paikallispopulaatioilla on suuri sukupuutoriski. Metapopulaation selviytymisen edellytyksenä on uusien paikallispopulaatioiden syntyminen, jonka mahdollistaa yksilöiden kyky liikkua elinympäristölaikkujen välillä. Aiemmat täpläverkkoperhostutkimukset ovatkin osoittaneet, että uusissa paikallispopulaatioissa esiintyvät naaraat eivät ole sattumanvarainen otos metapopulaatiosta, vaan uusien populaatioiden naarailla on parempi liikkumiskyky kuin vanhojen populaatioiden naarailla. Väitöskirjatyössäni tutkin mahdollisia korrelaatioita liikkuvuuden ja muiden elinkiertoekologisten ominaisuuksien, kuten ruumiin koon, lisääntymismenestyksen ja eliniän välillä sekä pyrin ymmärtämään näiden korrelaatioiden ekologisen ja evolutiivisen merkityksen. Olen erityisen kiinnostunut ominaisuuksien vaihtelusta luonnonmukaisissa olosuhteissa, minkä vuoksi kokeet suoritettiin lajin luontaisen elinympäristön päälle rakennetussa populaatiohäkissä (32 x 26 m). Tulokset osoittivat, että myös populaatiohäkissä uusien populaatioiden naaraat liikkuivat enemmän kuin vanhojen populaatioiden naaraat. Osoitin myös, että liikkuvuus on periytyvä ominaisuus ja että lentoaktiivisuuteen vaikuttaa vaihtelu geenissä, joka koodaa glykolyysissä tärkeää fosfoglukoosi-isomeraasi -entsyymiä. Sekä populaatioiden sisäinen että niiden välinen vaihtelu liikkuvuudessa korreloi naaraiden lisääntymismenestyksen kanssa. En kuitenkaan havainnut usein oletettua, liikkuvuudesta aiheutuvaa fysiologista elinkiertokustannusta naaraiden elinikäisessä munatuotannossa. Liikkuvuuden kustannukset näkyivät uusien populaatioiden naaraiden lyhyempänä elinikänä. Suuremmalla liikkuvuudella on kuitenkin metapopulaatiotasolla kustannus, sillä liikkuvammat naaraat viettävät enemmän aikaa elinympäristön ulkopuolella, minkä vuoksi niillä on vähemmän aikaa lisääntymiseen kuin vähemmän liikkuvilla naarailla. Väitöskirjatyöni tulokset osoittavat, että paikallispopulaatioiden nopea vaihtuvuus (sukupuutot ja uusien paikallispopulaatioiden syntyminen) Ahvenanmaan täpläverkkoperhosmetapopulaatiossa ylläpitää vaihtelua useissa elinkiertoekologisissa ominaisuuksissa liikkuvuuden ohella

What can the long-term ecological monitoring of the Åland islands meadow network tell us about changes in Finnish nature?

Human induced changes in land use and in climate are having severe impact on natural populations and communities, as evidenced by recently reported declines in insects. Quantifying change and understanding the drivers underlying these changes requires long-term systematically monitored ecological data. The occurrence and abundance of the Glanville fritillary (Melitaea cinxia) butterfly in the Åland islands has been monitored across the 4 000 potential habitat patches continuously since 1993. This classic metapopulation has become an ecological model system in understanding how species persist in fragmented landscape. Due to the systematic long-term survey, we are now beginning to see also how on-going changes related to climate are affecting the ecology and population dynamics of the butterfly. As many other butterflies globally and in Finland, the Glanville fritillary butterfly also shows declining population trends in the Åland islands. In addition, the metapopulation fluctuations have become more synchronous in space with especially dry and warm summers having the most negative effect on the species overall

Sex-dependent effects of larval food stress on adult performance under semi-natural conditions : only a matter of size?

Organisms with complex life-cycles acquire essential nutrients as juveniles, and hence even a short-term food stress during development can impose serious fitness costs apparent in adults. We used the Glanville fritillary butterfly to investigate the effects of larval food stress on adult performance under semi-natural conditions in a population enclosure. We were specifically interested in whether the negative effects observed were due to body mass reduction only or whether additional effects unrelated to pupal mass were evident. The two sexes responded differently to the larval food stress. In females, larval food stress reduced pupal mass and reproductive performance. The reduced reproductive performance was partially mediated by pupal mass reduction. Food stressed females also had reduced within-patch mobility, and this effect was not dependent on pupal mass. Conversely, food stress had no effect on male pupal mass, suggesting a full compensation via prolonged development time. Nonetheless, food stressed males were less likely to sire any eggs, potentially due to changes in their territorial behavior, as indicated by food stress also increasing male within-patch mobility (i.e., patrolling behavior). When males did sire eggs, the offspring number and viability were unaffected by male food stress treatment. Viability was in general higher for offspring sired by lighter males. Our study highlights how compensatory mechanisms after larval food stress can act in a sex-specific manner and that the alteration in body mass is only partially responsible for the reduced adult performance observed.Peer reviewe

Exploring links between climatic predictability and the evolution of within- and transgenerational plasticity

In variable environments, phenotypic plasticity can increase fitness by providing tight environment-phenotype matching. However, adaptive plasticity is expected to evolve only when the future selective environment can be predicted based on the prevailing conditions. That is, the juvenile environment should be predictive of the adult environment (within-generation plasticity) or the parental environment should be predictive of the offspring environment (transgenerational plasticity). Moreover, the environmental predictability can also shape transient responses such as stress response in an adaptive direction. Here, we test links between environmental predictability and the evolution of adaptive plasticity by combining time series analyses and a common garden experiment using temperature as a stressor in a temperate butterfly (Melitaea cinxia). Time series analyses revealed that across season fluctuations in temperature over 48 years are overall predictable. However, within the growing season, temperature fluctuations showed high heterogeneity across years with low autocorrelations and the timing of temperature peaks were asynchronous. Most life-history traits showed strong within-generation plasticity for temperature and traits such as body size and growth rate broke the temperature-size rule. Evidence for transgenerational plasticity, however, was weak and detected for only two traits each in an adaptive and non-adaptive direction. We suggest that the low predictability of temperature fluctuations within the growing season likely disfavors the evolution of adaptive transgenerational plasticity but instead favors strong within-generation plasticity.Peer reviewe

Microclimatic variability buffers butterfly populations against increased mortality caused by phenological asynchrony between larvae and their host plants

Climate change affects insects in several ways, including phenological shifts that may cause asynchrony between herbivore insects and their host plants. Insect larvae typically have limited movement capacity and are consequently dependent on the microhabitat conditions of their immediate surroundings. Based on intensive field monitoring over two springs and on larger-scale metapopulation-level survey over the same years, we used Bayesian spatial regression modelling to study the effects of weather and microclimatic field conditions on the development and survival of post-diapause larvae of the Glanville fritillary butterfly Melitaea cinxia on its northern range edge. Moreover, we assessed whether the observed variation in growth and survival in a spring characterized by exceptionally warm weather early in the season translated into population dynamic effects on the metapopulation scale. While similar weather conditions enhanced larval survival and growth rate in the spring, microclimatic conditions affected survival and growth contrastingly due to the phenological asynchrony between larvae and their host plants in microclimates that supported fastest growth. In the warmest microclimates, larvae reached temperatures over 20 degrees C above ambient leading to increased feeding, which was not supported by the more slowly growing host plants. At the metapopulation level, population growth rate was highest in local populations with heterogeneous microhabitats. We demonstrate how exceptionally warm weather early in the spring caused a phenological asynchrony between butterfly larvae and their host plants. Choice of warmest microhabitats for oviposition is adaptive under predominant conditions, but it may become maladaptive if early spring temperatures rise. Such conditions may lead to larvae breaking diapause earlier without equally advancing host plant growth. Microclimatic variability within and among populations is likely to have a crucial buffering effect against climate change in many insects.peerReviewe

Exploring the dimensions of metapopulation persistence : a comparison of structural and temporal measures

The spatial arrangement of habitat patches in a metapopulation and the dispersal connections among them influence metapopulation persistence. Metapopulation persistence emerges from a dynamic process, namely the serial extinctions and recolonizations of local habitat patches, while measures of persistence are typically based solely on structural properties of the spatial network (e.g., spatial distance between sites). Persistence estimators based on static properties may be unable to capture the dynamic nature of persistence. Understanding the shape of the distribution of extinction times is a central goal in population ecology. Here, we examine the goodness of fit of the power law to patch persistence time distributions using data on a foundational metapopulation system-the Glanville fritillary butterfly in the angstrom land islands. Further, we address the relationship between structural measures of metapopulation persistence (i.e., metapopulation capacity) and our temporal distributional fits to patch persistence times based on a power law. Patch persistence time distributions were well fit by a power law for the majority of semi-independent networks. Power law fits to persistence time distributions were related to metapopulation capacity, linking structural and temporal measures of metapopulation persistence. Several environmental variables and measures of network topology were correlated with both measures of metapopulation persistence, though correlations tended to be stronger for the structural measure of metapopulation persistence (i.e., metapopulation capacity). Together, our findings suggest that persistence time distributions are useful dynamic properties of metapopulations, and provide evidence of a relationship between metapopulation structure and metapopulation dynamics.Peer reviewe

The more the merrier : Conspecific density improves performance of gregarious larvae and reduces susceptibility to a pupal parasitoid

Aggregation can confer advantages in animal foraging, defense, and thermoregulation. There is a tight connection between the evolution of insect sociality and a highly effective immune system, presumably to inhibit rapid disease spread in a crowded environment. This connection is less evident for animals that spend only part of their life cycle in a social environment, such as noneusocial gregarious insects. Our aim was to elucidate the effects of group living by the gregarious larvae of the Glanville fritillary butterfly with respect to individual performance, immunity, and susceptibility to a parasitoid. We were also interested in the role of family relative to common postdiapause environment in shaping life-history traits. Larvae were reared at high or low density and then exposed to the pupal parasitoid wasp Pteromalus apum, either in presence or absence of a previous immune challenge that was used to measure the encapsulation immune response. Surviving adult butterflies were further tested for immunity. The wasp offspring from successfully parasitized butterfly pupae were counted and their brood sex ratios assessed. Larvae reared at high density grew larger and faster than those at low density. Despite high mortality due to parasitism, survival was greater among individuals with high pupal immunity in both density treatments. Moreover, butterfly pupae reared at high density were able to kill a larger fraction of individuals in the parasitoid broods, although this did not increase survival of the host. Finally, a larger proportion of variation observed in most of the traits was explained by butterfly family than by common postdiapause rearing environment, except for adult survival and immunity, for which this pattern was reversed. This gregarious butterfly clearly benefits from high conspecific density in terms of developmental performance and its ability to fight a parasitoid. These positive effects may be driven by cooperative interactions during feeding.Peer reviewe

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 nonreproducing 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.Non Peer reviewe

The importance of trans-generational effects in Lepidoptera

The importance of trans-generational effects in shaping an individuals' phenotype and fitness, and consequently even impacting population dynamics is increasingly apparent. Most of the research on trans-generational effects still focuses on plants, mammals, and birds. In the past few years, however, increasing number of studies, especially on maternal effects, have highlighted their importance also in many insect systems. Lepidoptera, specifically butterflies, have been used as model systems for studying the role of phenotypic plasticity within generations. As ectotherms, they are highly sensitive to environmental variation, and indeed many butterflies show adaptive phenotypic plasticity in response to environmental conditions. Here, we synthesize what is known about trans-generational effects in Lepidoptera, compile evidence for different environmental cues that are important drivers of trans-generational effects, and point out which offspring traits are mainly impacted. Finally, we emphasize directions for future research that are needed for better understanding of the adaptive nature of trans-generational effects in Lepidoptera in particular, but potentially also in other organisms.Peer reviewe

Moderate plant water stress improves larval development, and impacts immunity and gut microbiota of a specialist herbivore

While host plant drought is generally viewed as a negative phenomenon, its impact on insect herbivores can vary largely depending on the species involved and on the intensity of the drought. Extreme drought killing host plants can clearly reduce herbivore fitness, but the impact of moderate host plant water stress on insect herbivores can vary, and may even be beneficial. The populations of the Finnish Glanville fritillary butterfly (Melitaea cinxia) have faced reduced precipitation in recent years, with impacts even on population dynamics. Whether the negative effects of low precipitation are solely due to extreme desiccation killing the host plant or whether moderate drought reduces plant quality for the larvae remains unknown. We assessed the performance of larvae fed on moderately water-stressed Plantago lanceolata in terms of growth, survival, and immune response, and additionally were interested to assess whether the gut microbial composition of the larvae changed due to modification of the host plant. We found that larvae fed on water-stressed plants had increased growth, with no impact on survival, up-regulated the expression of one candidate immune gene (pelle), and had a more heterogeneous bacterial community and a shifted fungal community in the gut. Most of the measured traits showed considerable variation due to family structure. Our data suggest that in temperate regions moderate host plant water stress can positively shape resource acquisition of this specialized insect herbivore, potentially by increasing nutrient accessibility or concentration. Potentially, the better larval performance may be mediated by a shift of the microbiota on water-stressed plants, calling for further research especially on the understudied gut fungal community.Peer reviewe