Contribution of GC content to differentiated region formation along a speciation continuum

Abstract

AbstractGenome features can interact with external evolutionary processes and are involved in the formation of highly differentiated regions (i.e., genomic islands) potentially containing adaptation and speciation loci. However, GC content that can elevate both regional recombination and mutation has not been investigated in evolving lineages to test its effects on formation of heterozygous differentiation landscape. Here, we employed the genomes of 499 Asian honey bee (Apis cerana), with a widely-distributed central lineage diverged and admixed with its peripheral lineages at both population genetic and phylogenetic levels, to investigate the effects of GC content on mutation accumulation and lineage divergence along the speciation continuum. We find that genomic islands are generally with low GC content (i.e., lower-than-average), and with lower-than-average divergence (dxy) initially to higher-than-average ones at deeper divergence, corresponding to the suggested evolution models transforming from linked selection to divergent selection. When comparing with high-GC regions however, we find higher mutation load indicating inefficient natural selection in low-GC regions, which thus support the important role of low GC content instead of evolutionary process (e.g., natural selection) in genomic island formation. Finally, low-GC regions possess higher proportion of lineage-specific polymorphisms than high-GC regions due to limited recombination and admixture under the gene-flow scenario, and reconciliate discordance between mitochondrial and nuclear phylogenies inA. cerana. Our results shed light on the contribution of polymorphisms in low-GC regions to divergent region formation along the speciation continuum and their application in reconstruction of intraspecific phylogeny, especially in lineages with gene flow.