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.