Transcriptome Analysis Reveals Signature of Adaptation to Landscape Fragmentation

Abstract

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.

Predictable allele frequency changes due to habitat fragmentation in the Glanville fritillary butterfly

“…The present study has fulfilled all these criteria: (i) Suitable genetic variation for selection to act upon, which is evidently the case here. (ii) This genetic variation is linked to a specific environmental stress; our SNP panel was selected to include especially markers associated with either flight or habitat fragmentation (32). (iii) Any identified associated alleles vary across generations, which is the case here.…”

“…The genomic resources for the Glanville fritillary include the published genome (33), a high-density linkage map (59), and two RNAseq datasets (32,46), which were used to create a SNP panel using the KASP genotyping platform (LGC Genomics) for large-scale genotyping (Dataset S3). Markers were selected on the basis of previous studies (32,34,46,60), in which candidate genes were associated with flight and dispersal traits or were significantly differentially expressed after an experimental flight treatment. Putatively neutral SNPs were selected from the noncoding regions of the genome (SI Appendix).…”

“…Finally, we characterized the allele frequencies of the outlier loci in four regional populations in the northern Baltic region (Fig. 1), two of which have a highly fragmented landscape and two of which have continuous habitat (28,32). Allele frequencies were obtained from ref.…”

“…To test this hypothesis directly, we compared the allele frequency changes of outlier loci in Sottunga and SW Finland with allele frequencies in four regional populations in the Baltic region (data from ref. 32; Fig. 1 shows their locations).…”

“…In an RNA-seq study of gene expression, 1,841 genes were differentially expressed between fragmented and continuous landscapes. Genes that were systematically up-regulated following an experimental flight treatment had higher basal expression in fragmented than in continuous landscapes (32).…”