The assembled and annotated genome of the pigeon louse Columbicola columbae, a model ectoparasite

Abstract

The pigeon louse Columbicola columbae is a longstanding and important model for studies of ectoparasitism and host-parasite coevolution. However, a deeper understanding of its evolution and capacity for rapid adaptation is limited by a lack of genomic resources. Here, we present a high-quality draft assembly of the C. columbae genome, produced using a combination of Oxford Nanopore, Illumina, and Hi-C technologies. The final assembly is 208 Mb in length, with 12 chromosome-size scaffolds representing 98.1% of the assembly. For gene model prediction, we used a novel clustering method (wavy_choose) for Oxford Nanopore RNA-seq reads to feed into the MAKER annotation pipeline. High recovery of conserved single-copy orthologs (BUSCOs) suggests that our assembly and annotation are both highly complete and highly accurate. Consistent with the results of the only other assembled louse genome, Pediculus humanus, we find that C. columbae has a relatively low density of repetitive elements, the majority of which are DNA transposons. Also similar to P. humanus, we find a reduced number of genes encoding opsins, G protein-coupled receptors, odorant receptors, insulin signaling pathway components, and detoxification proteins in the C. columbae genome, relative to other insects. We propose that such losses might characterize the genomes of obligate, permanent ectoparasites with predictable habitats, limited foraging complexity, and simple dietary regimes. The sequencing and analysis for this genome were relatively low cost, and took advantage of a new clustering technique for Oxford Nanopore RNAseq reads that will be useful to future genome projects.

Keywords: ectoparasitism; genome annotation; genome assembly; insect genomics; ischnocera; phthiraptera.

Figure 1

Slender pigeon louse (Columbicola columbae)—about 2 mm in length—clinging to a rock pigeon feather. The thumblike processes on the antennae of the male louse shown here are used to grasp a female when mating. Dubbed “the bird louse par excellence” (Eichler et al. 1972), C. columbae has long been a model for studies of host-parasite coevolution. Photo by Scott Villa and Juan Altuna.

Figure 2

wavy_choose identifies likely full-length transcripts from clustered Oxford Nanopore reads. Depicted here is a histogram of read lengths (blue) for one carnac-LR-clustered set of reads. wavy_choose is able to identify two length peaks (red lines) in this transcript set, and discards all reads of other lengths. This process simplifies the transcriptome evidence dataset for MAKER, which uses the identified reads for gene annotation.

Figure 3

Jellyfish-derived (Marçais and Kingsford 2011) 21-mer histogram based on Illumina reads from the C. columbae genome.

Figure 4

Cumulative coverage of initial and final (scaffolded) C. columbae genome assemblies, illustrating the improvement in contiguity by scaffolding with Hi-C data. All scaffolds in the assembly are plotted largest to smallest, from left to right. The x-axis indicates cumulative length of an assembly, and the y-axis corresponds to the cumulative portion of the genome covered by initial contigs (red dots) and final scaffolds (blue dots).

Figure 5

Cumulative annotation edit distance (AED) for all genes in the MAKER-derived annotation. 10.3% of genes have an AED of 0, while only 5.6% of genes have an AED above 0.5 (vertical dashed line).

Figure 6

Chromosome-wide feature density in the C. columbae genome. Gene and repeat density in 1 Mb-wide sliding windows across the C. columbae genome show that there are no clear centromeres, and gene and simple repeat density are negatively correlated.

Figure 7

Short range synteny is largely conserved between C. columbae (bottom) and P. humanus (top) genomic scaffolds. Lines connecting scaffolds from each genome assembly represent the positions of orthologous genes. P. humanus contigs were aligned to the C. columbae genome in order and orientation using SynIma. Chromosome-size scaffolds in C. columbae are labeled 1–12.