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Saastamoinen, M.

Publications and source records attributed to Saastamoinen, M..

At least 19 recordsLinked to original sources

The microbiota of a wild butterfly species over three decades of climate change

Thermal stress can disturb microbial communities associated with host species. As microbes can support essential functions related to host metabolism, physiology, nutrition and immunity, changes in microbial communities can have severe fitness consequences for the host. Although the effects of thermal conditions on host-associated microbiomes have been demonstrated in controlled laboratory settings, how climate change might affect the structure and functionality of microbial communities in wild populations remain poorly understood. Here, we took advantage of the well-characterized long-term field survey of the Glanville fritillary butterfly (Melitaea cinxia) metapopulation on the [A]land islands, in the Baltic Sea, to fill this gap. We investigated whether bacterial communities associated with larvae show signs of gradual temporal change in response to slow environmental warming across a 28-year period, or whether these communities responded through abrupt change following a sudden drought event that triggered bottlenecks in their butterfly host population. Using a combination of 16S rRNA metabarcoding and metagenomic sequencing, we first showed that M. cinxia harbours a set of stable resident bacteria, including Pseudomonas, Telluria, and Enterobacteriaceae bacteria. But we also characterized a gradual shift in the M. cinxia associated bacterial community over three decades of increasing temperatures and decreasing precipitations. This shift was not unidirectional for all bacterial taxa, as the dominant Telluria and Pseudomonas showed opposing responses to environmental trends. Additionally, the 2018 extreme drought, which triggered acute host population bottlenecks, was associated with a severe disruption of M. cinxia microbiota, and the loss of key Enterobacteriaceae taxa. However, the M. cinxia bacterial community seemed to be able to recover towards pre-drought structure in subsequent years, suggesting a degree of resilience to acute climatic perturbations in this microbial system.

microbiology↗

Habitat context alters the pace of climate-driven community warming across terrestrial and freshwater ecosystems

As global temperatures rise, ecological communities are increasingly dominated by warm-affiliated species, a process known as community warming or thermophilisation. Yet, why different taxa exhibit different rates of community warming remains unclear. Habitat composition and structure are likely drivers of this variation, as the ecological consequences of warming are filtered by local environmental conditions. Using over 40 years of monitoring data spanning terrestrial (birds, insects, plants) and freshwater (phytoplankton) communities, we show that habitat structure determines how strongly communities track warming. Forest cover systematically slows thermophilisation by reducing communities sensitivity to temperature change, whereas habitat heterogeneity has weak and variable effects that differ among ecosystems. Together, these results demonstrate that uneven thermophilisation arises from habitat-mediated differences in how communities respond to a shared climatic signal. Incorporating these effects is essential for improving predictions of biodiversity change under ongoing climate warming.

ecology↗

Recovering ecological interactions by mining non-target data from whole genome re-sequencing projects

The study of parasitic species can shed light on aspects of their hosts ecology. Such interactions are however often unknown or understudied due to the difficulty to detect and/or quantify many infections. Whole-genome sequencing and re-sequencing data have been generated at an increasing rate and reduced costs over the last two decades. Projects based on whole organisms, like whole insect specimens, provide genomic material for the target taxon, but may also include sequencing reads from associated microbes and other parasites. Here, we screened for the presence of non-host reads in a collection of whole-genome (re-) sequence projects from the Glanville fritillary butterfly, Melitaea cinxia, a model organism in research on the ecology and evolution of species in spatially structured and fragmented landscapes. We identified infections with different bacteria and eukaryotic parasites, which are shared between populations and underly both previously known and new biotic interactions for this butterfly species. The bacterial symbiont Wolbachia, usually common in insects, was found at relatively low prevalence, while Spiroplasma was ubiquitous across samples from several European populations of the butterfly. Additionally, we confirmed expected rates of larval parasitism by at least two parasitoid wasps. Such results provide proof of principle that key ecological interactions can be uncovered efficiently from existing data, an important first step to characterising the role host-associated organisms play in shaping the ecology and evolutionary history of their host species.

ecology↗

Relative Effects of Habitat Amount and Fragmentation Per Se on the Genetic Diversity of The Glanville Fritillary Butterfly

Habitat loss and fragmentation are considered the key drivers of biodiversity loss. Understanding their relative roles is difficult as habitat loss and fragmentation tend to co-occur. It has been proposed that the total habitat amount available in the local landscape mainly drives species richness while fragmentation per se - the breaking apart of habitat independent of habitat amount - has negligible or even a positive effect on biodiversity. Several studies support this at the species richness level. Yet, the potential effects of fragmentation per se on genetic diversity at the landscape scale are understudied. Using the Glanville fritillary butterfly metapopulation in the [A]land islands, we tested the effects of fragmentation per se on genetic diversity using a landscape-based approach and 2,610 individuals genotyped at 40 neutral SNP markers. We assessed the independent effect of habitat amount and fragmentation (i.e. number of patches) within the local landscape on the focal patch genetic diversity. The amount of habitat in the local landscape had a positive effect on genetic diversity, while fragmentation per se had a more negligible impact on the genetic diversity. Our results thus highlight that all fragments, even the small ones, likely contribute to the maintenance of genetic diversity of the focal population.

evolutionary biology↗

Perceived and observed biases within scientific communities: a case study in movement ecology

Who conducts biological research, where, and how the results are disseminated varies among geographies and identities. Identifying and documenting these forms of bias by research communities is a critical first step towards addressing them. We documented perceived and observed biases in movement ecology. Movement ecology is a rapidly expanding sub-discipline of biology, which is strongly underpinned by fieldwork and technology use. First, we surveyed attendees of an international conference, and discussed the results at the conference (comparing uninformed vs informed perceived bias). Although most researchers identified as bias-aware, only a subset of biases were discussed in conversation. Next, by considering author affiliations from publications in the journal Movement Ecology, we found among-country discrepancies between the country of the authors affiliation and study site location related to national economics. At the within-country scale, we found that race-gender identities of postgraduate biology researchers in the USA differed from national demographics. We discuss the role of potential specific causes for the emergence of bias in the sub-discipline, e.g. parachute-science or accessibility to fieldwork. Undertaking data-driven analysis of bias within research sub-disciplines can help identify specific barriers and first steps towards the inclusion of a greater diversity of participants in the scientific process.

ecology↗

Thermal plasticity in protective wing pigmentation is modulated by genotype and food availability in an insect model of seasonal polyphenism.

Developmental plasticity refers to the phenomenon whereby an organisms phenotype depends on the environmental conditions experienced during development. This plasticity can match phenotype to ecological conditions and help organisms to cope with environmental heterogeneity, including differences between alternating seasons. Experimental studies of developmental plasticity often focus on the impact of individual environmental cues and do not take explicit account of genetic variation. In contrast, natural environments are complex, comprising multiple variables with combined effects that are poorly understood and may vary among genotypes. We investigated the effects of multifactorial environments on the development of the seasonally plastic eyespots of Bicyclus anynana butterflies. Eyespot size is known to depend on developmental temperature and to be involved in alternative seasonal strategies for predator avoidance. In nature, both temperature and food availability undergo seasonal fluctuations. However, our understanding of whether thermal plasticity in eyespot size varies in relation to food availability and across genotypes remains limited. To address this, we investigated the combined effects of temperature (T; two levels: 20{degrees}C and 27{degrees}C) and food availability (N; two levels: control and limited) during development. We examined their impact on wing and eyespot size in adult males and females from multiple genotypes (G; 28 families). We found evidence of thermal and nutritional plasticity, and of temperature-by-nutrition interactions (significant TxN) on the size of eyespots in both sexes. Food limitation resulted in relatively smaller eyespots and tempered the effects of temperature. Additionally, we found differences among families for thermal plasticity (significant GxT effects), but not for nutritional plasticity (non-significant GxN effects) nor for the combined effects of temperature and food limitation (non-significant GxTxN effects). Our results reveal the context dependence of thermal plasticity, with the slope of thermal reaction norms varying across genotypes and across nutritional environments. We discuss these results in light of the ecological significance of pigmentation and the value of considering thermal plasticity in studies of the biological impact of climate change.

evolutionary biology↗

Clear effects of population and sex but not rearing temperature on stress tolerance in a temperate butterfly

As temperatures are rising globally, the survival of organisms depends on their tolerance of such rising temperatures as well as resistance to indirect effects such as resource shortage under these new conditions. Genetic background and phenotypic plasticity in the form of acclimation are known to affect stress resistance, but much about genetic variation in plasticity is still unknown, especially in insects other than Drosophila. Here we aim to study the effect of population of origin, developmental temperature, and their interaction on stress tolerance (heat tolerance and starvation resistance). We test the beneficial acclimation hypothesis and how it is influenced by intraspecific differences. For this, we reared Glanville fritillary butterfly larvae originating from Finland and Spain at high and control temperatures, and measured their heat tolerance and starvation resistance. To assess potential costs of acclimation we also measured lifespan under control conditions. Neither adult heat tolerance nor starvation resistance were impacted by thermal conditions during development and thus we found no evidence for the beneficial acclimation hypothesis. Heat tolerance also did not differ between sex or population of origin. In contrast, we found interacting effects of population and sex on adult starvation resistance, with Spanish females outperforming other groups. Spanish females also had a longer lifespan under control conditions. Our study provides no evidence for the beneficial acclimation hypothesis but highlights the importance of population differences in stress tolerance. SUMMARY STATEMENTDespite their importance, the interacting effects of population of origin and developmental acclimation temperature on stress response have not often been studied together, especially in insects other than Drosophila.

evolutionary biology↗

Species-associated bacterial diversity increases along a gradient of habitat degradation

Alterations of microbial communities have evident impacts on development, digestion, fecundity, metabolism, immunity, and diverse other biological functions of their hosts. Yet, the factors affecting microbial communities associated with wild species often remain uncharacterized. For example, the impact of the hosts habitat degradation due to anthropogenic activities has received little attention, which contrasts with the large literature showing how such habitat degradation is at least partly responsible for the on-going global patterns of macro-biodiversity erosion. Here, we use metacommunities of herbivorous insect species specialized in feeding on Plantago lanceolata in the fragmented landscape of the [A]land Islands, Finland, as a model system to test whether and how bacterial communities associated with wild species change along a gradient of habitat degradation. We evaluated microbial species diversity and community composition in two sympatric insect species sampled from local meadow habitats with various levels of human disturbance within or around these habitats (e.g. forests, roads, agriculture fields, buildings). Counter to our expectations, we found that bacterial diversity can increase with habitat degradation, with individuals from more degraded habitats hosting more rare bacterial species. In contrast, as the dominant microbial species remain similar across habitats, the community composition and function of the microbiota persist under habitat degradation. In this system, the strength of human activities might induce changes in habitat heterogeneity rather than changes in overall habitat quality, thus allowing local insects to encounter and host more rare microbes rather than trigger local microbial extinction.

microbiology↗

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). Here, we test links between environmental predictability and 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 is overall predictable. However, within the growing season, temperature fluctuations showed high heterogeneity across years with low autocorrelations and 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 low predictability of temperature fluctuations within the growing season likely disfavours the evolution of adaptive transgenerational plasticity but instead favours strong within-generation plasticity.

evolutionary biology↗

Doors and corners of variance partitioning in statistical ecology

Variance partitioning is a common tool for statistical analysis and interpretation in both observational and experimental studies in ecology. Its popularity has led to a proliferation of methods with sometimes confusing or contradicting interpretations. Here, we present variance partitioning as a general tool in a model based Bayesian framework for summarizing and interpreting regression-like models. To demonstrate our approach we present a case study comprising of a simple occupancy model for a metapopulation of the Glanville fritillary butterfly. We pay special attention to the thorny issue of correlated covariates and random effects, and highlight uncertainty in variance partitioning. We recommend several alternative measures of variance, which jointly can be used to better interpret variance partitions. Additionally, we extend the general approach to encompass partitioning of variance within and between groups of observations, an approach very similar to analysis of variance. While noting that many troublesome issues relating to variance partitioning, such as uncertainty quantification, have been neglected in the literature, we likewise feel that the rather general applicability of the methods as an extension of statistical model-based analyses has not been fully utilized by the ecological research community either.

ecology↗

Alternative developmental and transcriptomic responses to host plant water limitation in a butterfly metapopulation

Predicting how climate change affects biotic interactions and their evolution poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. In order to assess the prospects for population persistence under climate change, it is therefore crucial to characterise response mechanisms to climate change induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA seq analysis of the larval transcriptome. We observed that responses to feeding on water limited plants, in which amino acids and aromatic compounds are enriched, showed marked intrapopulation variation, with individuals of some families performing better on control and others on water limited plants. The transcriptomic responses were concordant with the developmental responses: Families exhibiting opposite developmental responses also produced opposite transcriptomic responses, e.g. in growth associated intracellular signalling. The opposite developmental and transcriptomic responses are associated with between families differences in organic compound catabolism and storage protein production. The results reveal heritable intrapopulation variability in plasticity, suggesting potential for evolutionary responses to drought-induced changes in host plant quality in the Finnish M. cinxia metapopulation.

ecology↗

Improved chromosome level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) based on SMRT Sequencing and linkage map.

The Glanville fritillary (Melitaea cinxia) butterfly is a long-term model system for metapopulation dynamics research in fragmented landscapes. Here, we provide a chromosome level assembly of the butterflys genome produced from Pacific Biosciences sequencing of a pool of males, combined with a linkage map from population crosses. The final assembly size of 484 Mb is an increase of 94 Mb on the previously published genome. Estimation of the completeness of the genome with BUSCO, indicates that the genome contains 93 - 95% of the BUSCO genes in complete and single copies. We predicted 14,830 gene models using the MAKER pipeline and manually curated 1,232 of these gene models. The genome and its annotated gene models are a valuable resource for future comparative genomics, molecular biology, transcriptome and genetics studies on this species.

genomics↗

Multidimensional plasticity in the Glanville fritillary butterfly: larval performance curves are temperature, host and family specific.

Variation in environmental conditions during development can lead to changes in life-history traits with long-lasting effects. Here, we study environmentally induced variation, i.e. the consequences of potential maternal oviposition choices, in a suite of life-history traits in pre-diapause larvae of the Glanville fritillary butterfly. We focus on offspring survival, early growth rates and relative fat reserves, and pay specific attention to intraspecific variation in the responses (GxExE). Globally, we found that thermal performance and survival curves varied between diets of two host plants, suggesting that host modifies the temperature impact, or vice versa. Additionally, we show that the relative fat content has a host-dependent, discontinuous response to developmental temperature. This implies that a potential switch in resource allocation, from more investment in growth at lower temperatures to storage at higher temperatures, is dependent on other environmental variables. Interestingly, we find that a large proportion of the variance in larval performance is explained by differences among families, or interactions with this variable. Finally, we demonstrate that these family-specific responses to the host plant remain largely consistent across thermal environments. Altogether, the results of our study underscore the importance of paying attention to intraspecific trait variation in the field of evolutionary ecology.

evolutionary biology↗

Narrow oviposition preference of an insect herbivore risks survival under conditions of severe drought

O_LIUnderstanding species habitat preferences are crucial to predict organisms responses to the current climate crisis. In many insects, maternal habitat selection for oviposition essentially determines offspring performance. Whether changes in climatic conditions may pose future mismatches in oviposition preference and offspring performance when mothers continue to prefer microhabitats that now threaten offspring survival is an open question. C_LIO_LITo address this, we tested if oviposition preferences put offspring at risk in the Glanville fritillary butterfly (Melitaea cinxia) under drought stress. Mainly, we focus on identifying the microhabitat determinants for oviposition and the variation of conditions experienced by the sessile offspring, using field observations from 12 populations collected over 2015-2018. These data are combined with ten years of larval nest and precipitation data to understand within-population patterns of habitat selection. We tested whether the preferred microhabitats maximized the extended larval performance (i.e. overwinter survival). C_LIO_LIWe found that females preferentially oviposited in microhabitats with higher host plant abundance and higher proportion of host plants with signs of drought stress. In most years, larval nests had higher survival in these drought-stressed microhabitats. However, in an extremely dry year, only two nests survived over the summer. C_LIO_LIOur results highlight that a failure to shift habitat preference under extreme climate conditions may have drastic consequences for the survival of natural populations under changing climatic conditions. C_LI

ecology↗

High evolutionary potential in the chemical defenses of an aposematic 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.

evolutionary biology↗

Summer drought decreases the predictability of local extinctions in a butterfly metapopulation

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 [A]land 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.

ecology↗

Variation in Melitaea cinxia gut microbiota is phylogenetically highly structured but only mildly driven by host plant microbiota, sex or parasitism.

Originality-Significance StatementThe factors contributing to the assembly of microbiota in animals are extremely complex, and thus a comprehensive understanding of the mechanisms shaping host-associated microbial communities in natural ecosystems requires extensive ecological studies and appropriate statistical methods. In this study, we investigated the bacterial microbiota associated with the caterpillars of the Glanville fritillary (Melitaea cinxia), which is a long-term-studied ecological model system. We assessed the structure of variation in both occurrence and abundance of gut microbial communities of individuals collected in the wild with joint-species modelling, with the aim to relate the microbial community structure with multiple potentially impacting covariates: host plant microbiota and metabolites, hosts sex, potential parasitoid infection, and family structure. These covariates exhibited substantial correlation with multiple microbial taxas occurrences, which correlations were consistent for phylogenetically related groups of taxa, but varied across the whole microbial community; on the contrary, only few correlations were found with taxas abundances. The dominating co-occurrence pattern of microbiota assembly, which effectively split caterpillar individuals into two distinct groups, was, however, unrelated to any of the considered covariates.\n\nSummaryUnderstanding of what ecological factors shape intraspecific variation of insect microbiota is still relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe the microbiome and to identify potential factors that determine the structure of the microbial community, including the sex of the host, the impact of parasitoid infection, and the possible link between host plant and caterpillar microbiota. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual. The observed variation in microbiota composition is partially attributed to the measured properties of the host or its plant microbial and chemical composition, and is aligned with microbial phylogenetic structure, with related taxa exhibiting similar patterns. However, the prevailing part of the observed variation was not associated with any of the assessed characteristics, although it followed a pronounced segregation structure: in some caterpillars the microbial communities were dominated by several related Enterobacteriaceae taxa, while in others these taxa were absent. Our results challenge previous findings that the host plant properties are the major drivers of microbiota communities of insect herbivores.

ecology↗

Every cloud has a silver lining: Moderate plant water stress positively impacts development, immunity, and gut microbiota of a specialist herbivore

The ongoing global temperature rise has led to increasing frequency of drought events, negatively impacting vegetation and the living organisms relying on it. 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 Finnish Glanville fritillary butterfly (Melitaea cinxia) has faced reduced precipitation in recent years, which has impacted population dynamics. However, whether the negative effects depend on extreme desiccation killing the host plant or moderate drought impacting plant quality remains unclear. We assessed the performance of larvae fed on moderately water-stressed Plantago lanceolata in terms of growth, gut microbial composition and immune response. We found that larvae fed on water-stressed plants had better growth, a more heterogeneous bacterial community and a shifted fungal community in the gut, and up-regulated the expression of one candidate immune gene (pelle), whereas survival remained unaffected. 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.

ecology↗