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 harbour 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 expanding 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.\n\nImpact summaryUnderstanding how fragmentation affects dispersal and gene flow across human-modified landscapes has long been a goal in evolutionary biology. It is typically assumed that individuals of the same species respond to the landscape in the same way, however growing evidence suggests that individuals can vary considerably in their dispersal traits. While the effects of this individual dispersal variation on range expansions and invasions have been well-characterized, knowledge of how it might mediate genetic responses to landscape fragmentation are almost entirely lacking. Here we demonstrate that individual variation in dispersal is key to the maintenance of genetic variation during a population expansion following a large decline in a butterfly metapopulation. We further show that spatial variation in dispersal is not maintained by the configuration of habitat patches alone, but by a more complex genotype-environment interaction involving the landscape matrix (i.e. landscape features found between habitat patches). This challenges the simplified landscape representations typically used in studies of dispersal evolution that ignore heterogeneity in the landscape matrix. More broadly, our results highlight the interplay of adaptive and neutral processes across fragmented landscapes, suggesting that an understanding of species vulnerability to landscape fragmentation requires consideration of both.