Transcriptome Analysis Reveals Signature of Adaptation to Landscape Fragmentation

We characterize allelic and gene expression variation between populations of the Glanville fritillary butterfly (Melitaea cinxia) from two fragmented and two continuous landscapes in northern Europe. The populations exhibit significant differences in their life history traits, e.g. butterflies from fragmented landscapes have higher flight metabolic rate and dispersal rate in the field, and higher larval growth rate, than butterflies from continuous landscapes. In fragmented landscapes, local populations are small and have a high risk of local extinction, and hence the long-term persistence at the landscape level is based on frequent re-colonization of vacant habitat patches, which is predicted to select for increased dispersal rate. Using RNA-seq data and a common garden experiment, we found that a large number of genes (1,841) were differentially expressed between the landscape types. Hexamerin genes, the expression of which has previously been shown to have high heritability and which correlate strongly with larval development time in the Glanville fritillary, had higher expression in fragmented than continuous landscapes. Genes that were more highly expressed in butterflies from newly-established than old local populations within a fragmented landscape were also more highly expressed, at the landscape level, in fragmented than continuous landscapes. This result suggests that recurrent extinctions and re-colonizations in fragmented landscapes select a for specific expression profile. Genes that were significantly up-regulated following an experimental flight treatment had higher basal expression in fragmented landscapes, indicating that these butterflies are genetically primed for frequent flight. Active flight causes oxidative stress, but butterflies from fragmented landscapes were more tolerant of hypoxia. We conclude that differences in gene expression between the landscape types reflect genomic adaptations to landscape fragmentation.本研究对北欧两片破碎化景观与两片连续景观中的格兰维尔蛱蝶（Glanville fritillary butterfly，Melitaea cinxia）种群的等位基因变异与基因表达差异进行了表征。该类群的不同种群在生活史性状上存在显著差异：相较于连续景观中的个体，破碎化景观内的格兰维尔蛱蝶拥有更高的飞行代谢速率与野外扩散能力，且幼虫生长速率更快。破碎化景观中的局域种群规模较小，且面临极高的局域灭绝风险，因此景观尺度上的长期种群存续依赖于对空置生境斑块的频繁再定植，而这一过程被预测会选择出更高扩散能力的个体。通过转录组测序（RNA-seq）数据与同质园实验，本研究发现两类景观环境下共有1841个基因存在差异表达。六聚体蛋白基因（Hexamerin genes）的表达此前已被证实具有较高遗传力，且与格兰维尔蛱蝶的幼虫发育时长显著相关；该类基因在破碎化景观种群中的表达量显著高于连续景观种群。在破碎化景观内部，相较于老龄局域种群，新定植种群个体中高表达的基因，在景观尺度上同样在破碎化景观种群中呈现更高的表达水平。这一结果表明，破碎化景观中反复发生的局域灭绝与再定植过程，会筛选出特定的基因表达谱。经实验飞行处理后显著上调的基因，在破碎化景观种群中具有更高的基础表达水平，这表明这些格兰维尔蛱蝶在遗传层面已预先适配频繁飞行活动。主动飞行会引发氧化应激，但破碎化景观中的格兰维尔蛱蝶对缺氧环境具有更强的耐受性。综上，两类景观种群间的基因表达差异，反映了其对景观破碎化的基因组适应性演化。