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Chemosensory genes in Leptinotarsa decemlineata

Citation

Schoville, Sean et al. (2021), Chemosensory genes in Leptinotarsa decemlineata, Dryad, Dataset, https://doi.org/10.5061/dryad.8sf7m0cmk

Abstract

Plants and plant-feeding insects comprise the majority of global species diversity, and their coevolutionary dynamics provide an important window into the mechanisms that mediate niche evolution. In particular, there is considerable interest in understanding the nature of genetic changes that allow host-plant shifts to occur and to determine whether functional genomic diversity varies predictably in relation to host-plant breadth. Insect chemosensory proteins play a central role in mediating insect-plant interactions, as they directly influence plant detection and sensory stimuli during feeding. This large group of gene families is known to evolve rapidly, yet it remains unclear how these genes evolve in response to host-shifts and host specialization. Here we investigate whether selection at chemosensory genes is linked to host-plant expansion in the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), and whether rates of selection vary among ten closely related Leptinotarsa species. To develop functional hypotheses of chemosensory genes involved in the detection of potato host-plants, we combine gene expression analysis of the antennae and maxillary-labial palps using RNA sequencing with genomic evidence of natural selection. We show that expression of chemosensory genes differs among pest populations of Leptinotarsa decemlineata and numerous genes are under positive selection. We also find that rates of positive selection on olfactory receptors are higher in host-plant generalists, whereas rates are higher for gustatory receptors and olfactory binding proteins in host-plant specialists.

Methods

Chemosensory annotations: Building upon prior genes models (Liu et al. 2015, Schoville et al. 2018, Mitchell et al. 2019), chemosensory genes were manually edited using the tissue-specific RNA sequence data. We focused on identifying new genes and resolving known problems in the annotation of OR and GR families.

Population genomic analysis: We used whole-genome resequencing data (NCBI PRJNA580490) to compare nucleotide diversity and signatures of positive selection in olfactory genes between pest and non-pest lineages of L. decemlineata. We first used SNP genotypes identified by Pélissié et al. (2021) as input for BEAGLE 4.1 (Browning and Browning 2016) to generate phased, genome-wide haplotype sequences (two per individual) and then isolated chemosensory loci of the annotated families.

Phylogenomic analysis: Among the ten Leptinotarsa species (NCBI PRJNA580490), gene models were isolated from de novo genomes of each Leptinotarsa species following the procedures described therein. In brief, chemosensory orthologs were first identified using a multiphase heuristic algorithm implemented by the spALN v2.3.3 program (Gotoh 2008), which efficiently maps cDNA sequences onto whole genomes (options -M4 -O6 -S0 -Q7 -LS were selected). These sequences were subsequently aligned to each other, using the CPB reference ortholog sequence, via a custom C program CATaNNN v4.0 (Weibel and Cohen 2018) and MAFFT v7.450 (Katoh and Standley 2013). We corrected for misalignment and quality using Guidance v2.02, at high stringency, with 30 bootstrap replicates per alignment (Penn et al. 2010).

Usage Notes

Please refer to the readme file.

Funding

U.S. Department of Agriculture, Award: 2015-67030-23495: NIFA AFRI

U.S. Department of Agriculture, Award: WIS02004: Hatch Formula Funds

Wisconsin Potato and Vegetable Growers Association