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

Abstract

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.

Long‐term demographic surveys reveal a consistent relationship between average occupancy and abundance within local populations of a butterfly metapopulation

“…This suggests a habitat quality threshold below which it is unlikely that patches become or stay occupied. In terms of notable land use effects, roads and surrounding agricultural lands increased occupancy, possibly due to increased connectivity between patches (DiLeo et al 2018). A similarly stark contrast was found in relationship between host plant abundance and the presence of the Clouded Apollo (Luoto et al 2001) and Oberthür's grizzled skipper (Fourcade and Öckinger 2017).…”

“…That unexplained variation can come in many guises such as unmeasured variation in landscape structure and habitat, or unaccounted interactions of the covariates with population dynamic processes such as when landscape structure affects dispersal (Conradt et al 2000, Luoto et al 2006, Stasek et al 2008, DiLeo et al 2018. That unexplained variation can come in many guises such as unmeasured variation in landscape structure and habitat, or unaccounted interactions of the covariates with population dynamic processes such as when landscape structure affects dispersal (Conradt et al 2000, Luoto et al 2006, Stasek et al 2008, DiLeo et al 2018.…”

“…We expect less pronounced effects of land use as effects of land use are mediated by direct measures of habitat quality. Still, land use is expected to have a more direct role through effects on dispersal (DiLeo et al 2018). Comparing occupancy and abundance, we expect that occupancy be largely determined by landscape structure, that is, the distribution of habitat and land use, while local variation in the habitat, especially in terms of area and quality would be more important for abundance.…”

The relative importance of local and regional processes to metapopulation dynamics

“…Metapopulation ecology shares numerous conceptual and analytical commonalities with landscape ecology (DiLeo, Husby, & Saastamoinen, ; Howell, Muths, Hossack, Sigafus, & Chandler, ) and network ecology (Box 1 and Urban & Keitt, ; Urban et al, ). Bridging these disciplines can provide conceptual synthesis and lead to a better understanding of patch occupancy patterns (Gilarranz & Bascompte, ; Rozenfeld et al, ; Urban & Keitt, ; Zamborain‐Mason, Russ, Abesamis, Bucol, & Connolly, ).…”

Joint evolution of dispersal and connectivity

“…In wing-dimorphic insects, functional connectivity depends on the frequency of the winged form, a heritable trait (Zera and Denno 1997). In the butterfly Melitaea cinxia, individuals who carry the Pgi-c allele are more mobile, so that different genotypes realize different functional connectivities between the same patches (DiLeo et al 2018). In plants, functional connectivity may depend on the animal vectors that aid seed dispersal, but also on traits of the plant that influence the use of these vectors (Auffret et al 2017).…”