Demography and environment modulate the effects of genetic diversity on extinction risk in a butterfly metapopulation.

Linking genetic diversity to extinction is a common goal in genomic studies. Recently, a debate has arisen regarding the importance of genetic variation in conservation as some studies have failed to find associations between genome-wide genetic diversity and extinction risk. However, only rarely are genetic diversity and fitness measured together in the wild, and typically demographic history and environment are ignored. It is therefore difficult to infer whether a lack of an association is real or obscured by confounding factors. To address these shortcomings, we analyzed genetic data from 7,501 individuals with extinction data from 279 meadows and mortality of 1,742 larval nests in a butterfly metapopulation. We found a strong negative association between genetic diversity and extinction when considering only heterozygosity in models. However, this association disappeared when accounting for ecological covariates, suggesting a confounding between demography and genetics and a more complex role for heterozygosity in extinction risk. Modeling interactions between heterozygosity and demographic variables revealed that associations between extinction and heterozygosity were context-dependent. For example, extinction declined with increasing heterozygosity in large, but not currently small populations, although negative associations between heterozygosity, extinction, and mortality were detected in small populations with a recent history of decline. We conclude that low genetic diversity is an important predictor of extinction, predicting >25% increase in extinction beyond ecological factors in certain contexts. These results highlight that inferences about the importance of genetic diversity for population viability should not rely on genomic data alone but require investments in obtaining demographic and environmental data from natural populations.

Effects of environment and genotype on dispersal differ across departure, transfer and settlement in a butterfly metapopulation.

Active dispersal is driven by extrinsic and intrinsic factors at the three stages of departure, transfer and settlement. Most empirical studies capture only one stage of this complex process, and knowledge of how much can be generalized from one stage to another remains unknown. Here we use genetic assignment tests to reconstruct dispersal across 5 years and 232 habitat patches of a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We link individual dispersal events to weather, landscape structure, size and quality of habitat patches, and individual genotype to identify the factors that influence the three stages of dispersal and post-settlement survival. We found that nearly all tested factors strongly affected departure probabilities, but that the same factors explained very little variation in realized dispersal distances. Surprisingly, we found no effect of dispersal distance on post-settlement survival. Rather, survival was influenced by weather conditions, quality of the natal habitat patch, and a strong interaction between genotype and occupancy status of the settled habitat patch, with more mobile genotypes having higher survival as colonists rather than as immigrants. Our work highlights the multi-causality of dispersal and that some dispersal costs can only be understood by considering extrinsic and intrinsic factors and their interaction across the entire dispersal process.

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.

The gravity of pollination: integrating at-site features into spatial analysis of contemporary pollen movement.

Pollen-mediated gene flow is a major driver of spatial genetic structure in plant populations. Both individual plant characteristics and site-specific features of the landscape can modify the perceived attractiveness of plants to their pollinators and thus play an important role in shaping spatial genetic variation. Most studies of landscape-level genetic connectivity in plants have focused on the effects of interindividual distance using spatial and increasingly ecological separation, yet have not incorporated individual plant characteristics or other at-site ecological variables. Using spatially explicit simulations, we first tested the extent to which the inclusion of at-site variables influencing local pollination success improved the statistical characterization of genetic connectivity based upon examination of pollen pool genetic structure. The addition of at-site characteristics provided better models than those that only considered interindividual spatial distance (e.g. IBD). Models parameterized using conditional genetic covariance (e.g. population graphs) also outperformed those assuming panmixia. In a natural population of Cornus florida L. (Cornaceae), we showed that the addition of at-site characteristics (clumping of primary canopy opening above each maternal tree and maternal tree floral output) provided significantly better models describing gene flow than models including only between-site spatial (IBD) and ecological (isolation by resistance) variables. Overall, our results show that including interindividual and local ecological variation greatly aids in characterizing landscape-level measures of contemporary gene flow.

The influence of landscape on gene flow in the eastern massasauga rattlesnake (Sistrurus c. catenatus): insight from computer simulations.

Understanding how gene flow shapes contemporary population structure requires the explicit consideration of landscape composition and configuration. New landscape genetic approaches allow us to link such heterogeneity to gene flow within and among populations. However, the attribution of cause is difficult when landscape features are spatially correlated, or when genetic patterns reflect past events. We use spatial Bayesian clustering and landscape resistance analysis to identify the landscape features that influence gene flow across two regional populations of the eastern massasauga rattlesnake, Sistrurus c. catenatus. Based on spatially explicit simulations, we inferred how habitat distribution modulates gene flow and attempted to disentangle the effects of spatially confounded landscape features. We found genetic clustering across one regional landscape but not the other, and also local differences in the effect of landscape on gene flow. Beyond the effects of isolation-by-distance, water bodies appear to underlie genetic differentiation among individuals in one regional population. Significant effects of roads were additionally detected locally, but these effects are possibly confounded with the signal of water bodies. In contrast, we found no signal of isolation-by-distance or landscape effects on genetic structure in the other regional population. Our simulations imply that these local differences have arisen as a result of differences in population density or tendencies for juvenile rather than adult dispersal. Importantly, our simulations also demonstrate that the ability to detect the consequences of contemporary anthropogenic landscape features (e.g. roads) on gene flow may be compromised when long-standing natural features (e.g. water bodies) co-exist on the landscape.

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.

Landscape permeability and individual variation in a dispersal-linked gene jointly determine genetic structure in the Glanville fritillary butterfly.

There is now clear evidence that species across a broad range of taxa harbor extensive heritable variation in dispersal. While studies suggest that this variation can facilitate demographic outcomes such as range expansion and invasions, few have considered the consequences of intraspecific variation in dispersal for the maintenance and distribution of genetic variation across fragmented landscapes. Here, we examine how landscape characteristics and individual variation in dispersal combine to predict genetic structure using genomic and spatial data from the Glanville fritillary butterfly. We used linear and latent factor mixed models to identify the landscape features that best predict spatial sorting of alleles in the dispersal-related gene phosphoglucose isomerase (Pgi). We next used structural equation modeling to test if variation in Pgi mediated gene flow as measured by Fst at putatively neutral loci. In a year when the population was recovering following a large decline, individuals with a genotype associated with greater dispersal ability were found at significantly higher frequencies in populations isolated by water and forest, and these populations showed lower levels of genetic differentiation at neutral loci. These relationships disappeared in the next year when metapopulation density was high, suggesting that the effects of individual variation are context dependent. Together our results highlight that (1) more complex aspects of landscape structure beyond just the configuration of habitat can be important for maintaining spatial variation in dispersal traits and (2) that individual variation in dispersal plays a key role in maintaining genetic variation across fragmented landscapes.

Highly polymorphic microsatellite markers in Pulsatilla vulgaris (Ranunculaceae) using next-generation sequencing.

PREMISE OF THE STUDY: We developed novel microsatellite markers for the perennial plant Pulsatilla vulgaris (Ranunculaceae) to investigate the effects of fragmentation on gene flow in this imperiled species. METHODS AND RESULTS: We identified microsatellites and developed primers based on 454 shotgun sequences. We identified 14 markers that were polymorphic and produced clean bands. Of these, eight could be analyzed as diploids. Genotyping of 97 individuals across two populations revealed these markers to be highly polymorphic with seven to 17 alleles per locus and observed heterozygosity from 0.41 to 0.83. CONCLUSIONS: The markers are highly informative and will be used to test if the reintroduction of shepherding in southern Germany improves genetic connectivity among fragmented populations of P. vulgaris. The combination of diploid and tetraploid markers presented here will be useful in resolving the polyploidization history of this and related species.