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Unravelling life-history responses and underlying mechanisms to environmental stress in wild populations

Periodic Reporting for period 4 - META-STRESS (Unravelling life-history responses and underlying mechanisms to environmental stress in wild populations)

Reporting period: 2019-10-01 to 2020-12-31

Organisms in the wild are challenged by environmental variation for example in resource quality. The goal of the META-STRESS project was to move beyond laboratory experiments to understand the mechanisms that allow organisms in the wild to cope with environmental stress, more specifically variation in host plant quality. We are utilizing the large metapopulation of the Glanville fritillary butterfly to study processes operating from genes within individuals all the way to metapopulation-level dynamics. We will effectively couple laboratory and field-based studies. The ecological studies will be integrated with molecular approaches to unravel the significance of different mechanisms – candidate genes, epigenetic inheritance and intestinal microbial communities – potentially influencing individual responses to environmental challenges. The proposed project has potential for groundbreaking results in evolutionary ecology, as the results will increase our understanding of 1) how individual responses to unfavorable environmental conditions and the underlying mechanisms vary within and among local populations in a spatially and temporally heterogeneous environment, and 2) how the consequent life-history variation influences the ecological and microevolutionary dynamics of wild populations.
ERC StG META-STRESS project aims to understand the mechanisms that allow organisms in the wild to cope with environmental stress.
At the core of this project is the analyses of the weather in impacting the long-term (> 25 years) of population dynamics of the Glanville fritillary butterfly in the Åland islands over the 4,000 habitat patches and the changes we observe in the metapopulation synchrony. This completed analysis is accompanied with a detailed assessment of a set of local populations that have experienced contrasting environmental conditions in regards to environmental stress, drought, over several summers. These results indicated clear preference for drought prone microhabitat sites for egg oviposition, which benefit offspring survival on most years. However, in an extreme dry summer selection of these sites resulted in high mortality of larval families, which resulted in extreme decline in metapopulation occupancy.
We’ve successfully conducted several experiments to assess phenotypic responses of plants to drought and how this as well as other environmental stressors, alone and in combination, translate to larval performance. We find strong genotype-environment interactions in both plants and in larvae in these responses, and also some indication of the potential role of local adaptation. In the butterflies, we have revealed strong family and life-stage – specific responses, and trade-offs in regards to stress tolerance. The benefits of feeding on water stressed host plant diet during post diapause developmental stage further translate to adult performance.
We have performed a gene expression analyses on the larval responses to host plant drought, which have allowed us to to discover substantial inter-population variation in these stress response programmes but also identify genes underlying stress tolerance. We have used whole-genome resequencing of individuals from selected population across the Åland islands over few years to assess whether variation in neutral genetic diversity and/or in alleles related to stress response pathways show differential patterns between populations in bad (decrease in population occupancy), stable, or good (increase in populations occupancy and abundance) years. We find genetic diversity to be considerably high in the butterfly metapopulation despite the severe population declines. The habitat patches with high connectivity also had high heterozygosity indicating that connectivity could be contributing towards rescue of genetic diversity after a demographic bottleneck. This is in contrast with our studies on another, seasonally polyphenic species, where we observed reduced genetic variation for plasticity related genes, which is likely to limit adaptive potential under climate change, where the deteriorating accuracy of predictive cues will increase maladaptive phenotype-environment mismatches.
We’ve demonstrated that the butterfly larvae in the wild present a poor bacterial community structure at the family level with most of the variability observed at the individual level. The host plant microbiota is less variable and its variation is strongly correlated with the variation in the host plant metabolites. However, neither the plant microbiota nor the plant metabolites impacted the global composition of the larvae microbiota. We have also more experimentally tested the role of microbiota on individual performance across in different life stages.
With this project, we gain ground-breaking results on how environmental conditions and ecological factors interact with allelic variation, epigenetics and composition of larval microbiota to influence variation in how individuals mitigate stress in natural populations. The unique synthesis of processes operating within individual level as well as within the metapopulation scale, and inclusion of molecular and experimental approaches has the potential for breakthrough discoveries in the field of ecology and evolutionary biology. This is possible only due to the infrastructure around which this project has been built: the ability to sample large numbers of individuals from a natural metapopulation for which long-term ecological data are available, the capacity to rear the species in the laboratory in large numbers and exceptional molecular and genomic tools available for a non-model species. Laboratory studies investigating the drought stress response have advance far ahead of work in the wild: the proposed empirical research will establish stress tolerance in an ecologically relevant context, thereby facilitating the interpretation of some of the previously obtained information on model organisms. A key innovation of this research is the integration of phenotypic and genetic data of individuals in the laboratory and in the wild into the context stress tolerance in response to climate change. This project has developed major advances in our knowledge in how natural populations deal with environmental stressors, including extreme climatic events, which are only possible because of the integration of molecular understanding with a study system, where ecological factors are studied at a large spatial scale. Studies like this, linking environmental conditions, developmental responses and demographic processes in populations experiencing natural selection, are rare and can provide novel insight into the selective forces maintaining life-history variation in the wild and into the consequences of that variation on population dynamics. Finally, the obtained results are answering questions that are not only central to our understanding of ecology and evolution but they are crucially important in the context of human-induced environmental change: in particular in predicting the likely consequences of deteriorating environmental conditions for populations, species and communities.