Genomic architecture reflects geographic divergence and adaptation
Divergence between northern and southern Canadian populations of mountain pine beetle has been shown in several population genetic studies (Batista et al., 2016; Cullingham et al., 2011; Janes et al., 2014). Using available genome-wide pool-seq data (Keeling et al., 2013c) and our newly assembled genomes, we evaluated this genetic differentiation at the chromosome level. The mountain pine beetle genome displayed two notable regions of elevated genetic divergence. The first divergent region is on the terminal end of the neo-X chromosome (Fig. 4c; Fig. 5a). This 18 Mb region represents the ancestral-X portion of the neo-X chromosome. Genes in this region were significantly enriched in GO terms associated with transport, chromatin remodeling, gap junctions, and catalytic activity (Supp. file 1).
Previous work by Bracewell et al. (2017) on mountain pine beetle populations in the northern US contrasts with our findings on genetic divergence in Canadian populations, as they did not identify differences in genetic divergence between the ancestral-autosomal and ancestral-X regions of the neo-X chromosome. However, that study reported higher genetic diversity in the ancestral-autosomal region. This differs from our findings where the ancestral-X region had the lowest levels of nucleotide diversity (Tab. 2). We also found the ancestral-autosomal region of neo-X had relatively similar levels of diversity to those of the other autosomes, but also showed the lowest levels of differentiation. In each chromosome and sub-region, we saw a higher level of genetic diversity compared to Bracewell et al. (2017), which may be explained by the recent population expansion in Canadian populations.
The second region with substantially increased divergence involves 4 Mb near the beginning of chromosome 4 (Fig. 4d). This region shows a north-south difference in Tajima’s D , with the southern population having positive Tajima’s D values compared to the negative-shifted values in the northern population that are typical of most of the rest of chromosome 4 and other chromosomes. Positive Tajima’s D values in the southern population suggest that genes within this region are undergoing balancing selection, while negative Tajima’s D values in the north highlight an excess of rare alleles in this region. It remains unknown if these polymorphisms play a role in population expansion or local adaptation of mountain pine beetles in northern British Columbia and Alberta. It is possible that this pattern of differentiation indicates a chromosomal inversion between the northern and southern populations, with both inversion variants being present in the southern population. This could alter the selection occurring on genes within this genomic region and could also alter patterns of gene expression near the inversion breakpoints (Durmaz et al., 2021). However, our linkage mapping results did not indicate patterns of recombination on chromosome 4 that were consistent with an inversion, and so the differentiated FST and Tajima’s D in this region may instead reflect the recent expansion and establishment of mountain pine beetle populations north and east of their historical Canadian range. Given the size of this differentiated region and the biological importance of the genes involved in protein synthesis and gene regulation found to be enriched in this part of the chromosome, it presents an interesting target for investigating differences in local adaptation between populations of the mountain pine beetle.