Improved chromosome-level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) integrating Pacific Biosciences long reads and a high-density linkage map.

BACKGROUND: The Glanville fritillary (Melitaea cinxia) butterfly is a model system for metapopulation dynamics research in fragmented landscapes. Here, we provide a chromosome-level assembly of the butterfly's genome produced from Pacific Biosciences sequencing of a pool of males, combined with a linkage map from population crosses. RESULTS: 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 92-94% of the BUSCO genes in complete and single copies. We predicted 14,810 genes using the MAKER pipeline and manually curated 1,232 of these gene models. CONCLUSIONS: The genome and its annotated gene models are a valuable resource for future comparative genomics, molecular biology, transcriptome, and genetics studies on this species.

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

Predicting how climate change affects biotic interactions 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. To assess the prospects for population persistence under climate change, it is therefore crucial to characterize 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 sequencing 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 variation within the metapopulation, 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 transcripts). The divergent responses in both larval development and transcriptome are associated with differences between families in amino acid catabolism and storage protein production. The results reveal intrapopulation variability in plasticity, suggesting that the Finnish M. cinxia metapopulation harbours potential for buffering against drought-induced changes in host plant quality.

Complex plant quality-microbiota-population interactions modulate the response of a specialist herbivore to the defence of its host plant.

Many specialist herbivores have evolved strategies to cope with plant defences, with gut microbiota potentially participating to such adaptations.In this study, we assessed whether the history of plant use (population origin) and microbiota may interact with plant defence adaptation.We tested whether microbiota enhance the performance of Melitaea cinxia larvae on their host plant, Plantago lanceolata and increase their ability to cope the defensive compounds, iridoid glycosides (IGs).The gut microbiota were significantly affected by both larval population origin and host plant IG level. Contrary to our prediction, impoverishing the microbiota with antibiotic treatment did not reduce larval performance.As expected for this specialized insect herbivore, sequestration of one of IGs was higher in larvae fed with plants producing higher concentration of IGs. These larvae also showed metabolic signature of intoxication (i.e. decrease in Lysine levels). However, intoxication on highly defended plants was only observed when larvae with a history of poorly defended plants were simultaneously treated with antibiotics.Our results suggest that both adaptation and microbiota contribute to the metabolic response of herbivores to plant defence though complex interactions. Read the free Plain Language Summary for this article on the Journal blog.

De nombreux herbivores spécialistes ont évolué vers des stratégies qui leurs permettent de contourner les défenses de leur plantes hôtes. Le microbiote pourrait potentiellement participer à certaines de ces adaptations.Dans cette étude, nous avons essayé de déterminer si l'adaptation d'un herbivore est influencée par son microbiote et l'historique d'utilisation de sa plante hôte (origine de la population).Nous avons testé en quoi le microbiote contribue à la performance de chenilles Melitaea cinxia sur leur plante hôte Plantago lanceolata ainsi que leur capacité à faire face aux glucosides d'iridoïdes (GI), des molécules de défenses produites par P. lanceolata.Comme attendu, la concentration de GI stockée était plus importante chez les chenilles qui étaient nourries avec des plantes produisant de fortes concentrations de GI. Ces chenilles présentaient par ailleurs des signes d'intoxications (i.e. diminution de la concentration de Lysine). Cependant cela n'était visible que lorsque les chenilles étaient issues de populations qui se nourrissaient historiquement sur des plantes peu défendues et lorsqu'elles étaient simultanément traitées par des antibiotiques.Nos résultats suggèrent donc que des processus complexes d'adaptation couplés à l'activité du microbiote contribuent à la réponse des herbivores aux défenses de leurs plante hôtes.

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

The ecological impacts of extreme climatic events on population dynamics and community composition are profound and predominantly negative. Using extensive data of an ecological model system, we tested whether predictions from ecological models remain robust when environmental conditions are outside the bounds of observation. We observed a 10-fold demographic decline of the Glanville fritillary butterfly (Melitaea cinxia) metapopulation on the Åland islands, Finland in the summer of 2018 and used climatic and satellite data to demonstrate that this year was an anomaly with low climatic water balance values and low vegetation productivity indices across Åland. Population growth rates were strongly associated with spatiotemporal variation in climatic water balance. Covariates shown previously to affect the extinction probability of local populations in this metapopulation were less informative when populations were exposed to severe drought during the summer months. Our results highlight the unpredictable responses of natural populations to extreme climatic events.

El Efecto de la Sequía Estival sobre la Previsibilidad de las Extinciones Locales en una Metapoblación de Mariposas Resumen Los impactos ecológicos de los eventos climáticos extremos sobre las dinámicas metapoblacionales y la composición de la comunidad son profundos y predominantemente negativos. Con los extensos datos de un sistema de modelos ecológicos probamos si las predicciones de los modelos ecológicos todavía son sólidos cuando las condiciones ambientales se encuentran fuera de los límites de observación. Observamos una declinación demográfica ocurrir diez veces en la metapoblación de la mariposa Melitaea cinxia en las Islas Aland de Finlandia durante el verano de 2018. Usamos datos climáticos y satelitales para demostrar que ese año fue una anomalía al contar con valores bajos de balance hídrico e índices bajos de productividad de la vegetación en todas las islas. Las tasas de crecimiento poblacional estuvieron fuertemente asociadas con la variación espaciotemporal del balance hídrico climático. Las covarianzas que previamente han afectado a la probabilidad de extinción de las poblaciones locales de esta metapoblación fueron menos informativas cuando las poblaciones estuvieron expuestas a sequías severas durante los meses de verano. Nuestros resultados resaltan las respuestas impredecibles de las poblaciones naturales ante los eventos climáticos extremos.

Metapopulation dynamics in a changing climate: Increasing spatial synchrony in weather conditions drives metapopulation synchrony of a butterfly inhabiting a fragmented landscape.

Habitat fragmentation and climate change are both prominent manifestations of global change, but there is little knowledge on the specific mechanisms of how climate change may modify the effects of habitat fragmentation, for example, by altering dynamics of spatially structured populations. The long-term viability of metapopulations is dependent on independent dynamics of local populations, because it mitigates fluctuations in the size of the metapopulation as a whole. Metapopulation viability will be compromised if climate change increases spatial synchrony in weather conditions associated with population growth rates. We studied a recently reported increase in metapopulation synchrony of the Glanville fritillary butterfly (Melitaea cinxia) in the Finnish archipelago, to see if it could be explained by an increase in synchrony of weather conditions. For this, we used 23 years of butterfly survey data together with monthly weather records for the same period. We first examined the associations between population growth rates within different regions of the metapopulation and weather conditions during different life-history stages of the butterfly. We then examined the association between the trends in the synchrony of the weather conditions and the synchrony of the butterfly metapopulation dynamics. We found that precipitation from spring to late summer are associated with the M. cinxia per capita growth rate, with early summer conditions being most important. We further found that the increase in metapopulation synchrony is paralleled by an increase in the synchrony of weather conditions. Alternative explanations for spatial synchrony, such as increased dispersal or trophic interactions with a specialist parasitoid, did not show paralleled trends and are not supported. The climate driven increase in M. cinxia metapopulation synchrony suggests that climate change can increase extinction risk of spatially structured populations living in fragmented landscapes by altering their dynamics.

Interspecific interactions influence contrasting spatial genetic structures in two closely related damselfly species.

Spatial genetic structure (SGS) is largely determined by colonization history, landscape and ecological characteristics of the species. Therefore, sympatric and ecologically similar species are expected to exhibit similar SGSs, potentially enabling prediction of the SGS of one species from that of another. On the other hand, due to interspecific interactions, ecologically similar species could have different SGSs. We explored the SGSs of the closely related Calopteryx splendens and Calopteryx virgo within Finland and related the genetic patterns to characteristics of the sampling localities. We observed different SGSs for the two species. Genetic differentiation even within short distances in C. splendens suggests genetic drift as an important driver. However, we also observed indication of previous gene flow (revealed by a negative relationship between genetic differentiation and increasing potential connectivity of the landscape). Interestingly, genetic diversity of C. splendens was negatively related to density of C. virgo, suggesting that interspecific interactions influence the SGS of C. splendens. In contrast, genetic differentiation between C. virgo subpopulations was low and only exhibited relationships with latitude, pointing to high gene flow, colonization history and range margin effects as the drivers of SGS. The different SGSs of the two ecologically similar species caution indirect inferences of SGS based on ecologically similar surrogate species.