The role of structural variants in pest adaptation and genome evolution of the Colorado potato beetle, Leptinotarsa decemlineata (Say)

Abstract

Structural variation has been associated with genetic diversity and adaptation. Despite these observations, it is not clear what their relative importance is for evolution, especially in rapidly adapting species. Here, we examine the significance of structural polymorphisms in pesticide resistance evolution of the agricultural super-pest, the Colorado potato beetle, Leptinotarsa decemlineata. By employing a parent offspring trio sequencing procedure, we develop highly contiguous reference genomes to characterize structural variation. These updated assemblies represent >100-fold improvement of contiguity and include derived pest and ancestral nonpest individuals. We identify >200,000 structural variations, which appear to be nonrandomly distributed across the genome as they co-occur with transposable elements and genes. Structural variations intersect with exons in a large proportion of gene annotations (~20%) that are associated with insecticide resistance (including cytochrome P450s), development, and transcription. To understand the role structural variations play in adaptation, we measure their allele frequencies among an additional 57 individuals using whole genome resequencing data, which represents pest and nonpest populations of North America. Incorporating multiple independent tests to detect the signature of natural selection using SNP data, we identify 14 genes that are probably under positive selection, include structural variations, and SNPs of elevated frequency within the pest lineages. Among these, three are associated with insecticide resistance based on previous research. One of these genes, CYP4g15, is coinduced during insecticide exposure with glycosyltransferase-13, which is a duplicated gene enclosed within a structural variant adjacent to the CYP4g15 genic region. These results demonstrate the significance of structural variations as a genomic feature to describe species history, genetic diversity, and adaptation.

Exploring polymorphic interspecies structural variants in Eucalyptus: Unravelling Their Role in Reproductive Isolation and Adaptive Divergence

“…Duplications are known to be highly common and an important source of evolutionary novelty (Cohen et al, 2023; Hanada et al, 2008), and were the most common type of SV in our analysis. Most duplications were found to be fixed, with the remainder being almost entirely polymorphic.…”

Transposable elements differ between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

“…However, TEs may have an unknown role in in adaptation, as the TE abundance and diversity of transposable elements does not provide a direct measure of adaptive evolution. Indeed, Cohen et al (2023) identify several insecticide resistance genes in L. decemlineata with TE insertions that are identified in genome scans of selection.…”

“…At the scale of the entire genome, we did not find that overall TE abundance and diversity were associated with recent contemporary adaptation to new host plants, insecticides, and geography. Instead, the TE community was concordant with demographic history (Pelissie et al 2023; Cohen et al 2023). It is possible that while transposable elements contribute to differences in the genomes of beetle populations, they are broadly unrelated to the phenotypic differences that we examined.…”

“…As our analysis was dependent on short read sequencing, we expect that our estimate of TE diversity and ability to detect specific gene-TE interactions will likely increase with the adoption of long-read sequencing methods, as they allow the analyses of structural variations (SV) such as deletions, insertions, and inversions, which may not be detectable in short read analyses. Indeed, Cohen et al (2023) found that SV are “nonrandomly distributed across the genome as they co-occur with transposable elements and genes”. Analyses of the relationship between transposable elements and these SV may reveal more about the specific role of TEs in the evolution of adaptive traits such as insecticide resistance.…”

Long‐read sequencing in ecology and evolution: Understanding how complex genetic and epigenetic variants shape biodiversity

“…This is consistent with a complex genetic architecture for this trait, which can at least partially be attributed to past whole genome duplication events (Zhu et al, 2023). Finally, Cohen et al (2023) investigate the genetics of pesticide resistance in Colorado potato beetle. The authors used PacBio sequencing and a trio‐binning approach to obtain three new haploid assemblies with considerably improved contiguity, as compared to the existing reference genome for this pest species.…”