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 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.

现有明确证据表明，涵盖广泛分类群（taxa）的物种，其扩散性状均存在广泛的可遗传变异。尽管已有研究显示这类变异可促进种群扩张、生物入侵等种群动态结果，但极少有研究探讨扩散过程中的种内变异，对破碎化景观中遗传变异的维持与分布格局的影响。本研究以格纹蛱蝶（Glanville fritillary butterfly）的基因组与空间数据为研究材料，解析景观特征与个体扩散变异如何共同作用以预测种群遗传结构。研究采用线性模型与潜因子混合模型（latent factor mixed models），筛选出可最优预测与扩散相关的葡萄糖磷酸异构酶（phosphoglucose isomerase, Pgi）基因等位基因空间分选模式的景观特征；随后借助结构方程模型（structural equation modeling），检验Pgi基因的变异是否介导了以推定中性位点的种群分化系数（Fst）衡量的基因流水平。在种群经历大规模衰退后发生扩张的年份中，携带与更高扩散能力相关基因型的个体，在被水体与森林阻隔的种群中出现的频率显著更高，且这类种群的中性位点遗传分化水平更低。而在集合种群密度较高的次年，上述关联消失，这表明个体扩散变异的效应具有情境依赖性。综合而言，本研究结果明确两点核心结论：其一，除生境配置外，景观结构的更多复杂特征，对维持扩散性状的空间变异同样具有重要意义；其二，个体扩散变异在破碎化景观的遗传变异维持中发挥关键作用。