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. 2023 May 3;12(5):675.
doi: 10.3390/pathogens12050675.

Comparative Genomic Analysis and Species Delimitation: A Case for Two Species in the Zoonotic Cestode Dipylidium caninum

Jeba R J Jesudoss Chelladurai  1 , Aloysius Abraham  2 , Theresa A Quintana  1 , Deb Ritchie  1 , Vicki Smith  1
Affiliations

Comparative Genomic Analysis and Species Delimitation: A Case for Two Species in the Zoonotic Cestode Dipylidium caninum

Jeba R J Jesudoss Chelladurai et al. Pathogens. .

Abstract

Dipylidium caninum (Linnaeus, 1758) is a common zoonotic cestode of dogs and cats worldwide. Previous studies have demonstrated the existence of largely host-associated canine and feline genotypes based on infection studies, differences at the 28S rDNA gene, and complete mitochondrial genomes. There have been no comparative genome-wide studies. Here, we sequenced the genomes of a dog and cat isolate of Dipylidium caninum from the United States using the Illumina platform at mean coverage depths of 45× and 26× and conducted comparative analyses with the reference draft genome. Complete mitochondrial genomes were used to confirm the genotypes of the isolates. Genomes of D. caninum canine and feline genotypes generated in this study, had an average identity of 98% and 89%, respectively, when compared to the reference genome. SNPs were 20 times higher in the feline isolate. Comparison and species delimitation using universally conserved orthologs and protein-coding mitochondrial genes revealed that the canine and feline isolates are different species. Data from this study build a base for future integrative taxonomy. Further genomic studies from geographically diverse populations are necessary to understand implications for taxonomy, epidemiology, veterinary clinical medicine, and anthelmintic resistance.

Keywords: Dipylidium caninum; cat and dog; cestode; flea tapeworm; genome comparison; species delimitation.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Figures

Figure 1
Figure 1
Whole genome coverage plot of Dipylidium caninum canine isolate FL1 (red-orange), and Dipylidium caninum feline isolate KS1 (teal) mapped to the reference Dipylidium caninum draft genome (grey). The average depth of coverage was 46.5× for the canine FL1 isolate and 25.8× for the feline KS1 isolate.
Figure 2
Figure 2
Genetic variants in the genomes D. caninum canine FL1 and D. caninum feline KS1 compared to the reference genome of D. caninum. (A) Scatterplot showing the number of genetic variants (SNPs, Indels) at each scaffold location. (B) Boxplots showing the distribution of the number of variants in each genome. (C) Boxplots showing the distribution of the mean number of variants per 1000 base pairs of reference scaffold.
Figure 3
Figure 3
Summary of genetic variants in D. caninum canine FL1 and feline KS1 genomes from this study compared to the D. caninum canine reference genome. (A) Total counts of variants in the genomes by type is shown. (B) Counts of transitions and transversions in each genome are shown. (C) Counts of specific nucleotide base changes from reference for each compared genome are shown.
Figure 4
Figure 4
(A) Venn diagram of overlapping complete BUSCO genes among the three genomes. (B) BUSCO assessment results of the three genomes of D. caninum. (C) Percentages of BUSCO genes.
Figure 5
Figure 5
Heatmap of distance matrices at 503 complete BUSCO loci calculated with the Tamura-Nei 1993 model. Each line in the heatmap represents one gene. Color legend indicates genetic distance. A. BUSCO genes of D. caninum canine FL1 compared to D. caninum feline KS1 and D. caninum Reference canine China. B. BUSCO genes of D. caninum feline KS1 compared to D. caninum canine FL1 and D. caninum Reference canine China. C. BUSCO genes of D. caninum Reference canine China compared to D. caninum feline KS1 and D. caninum canine FL1.
Figure 6
Figure 6
Principal component analysis plot of SNPs in the 503 BUSCO genes. 95% confidence intervals are shown as ellipses.
Figure 7
Figure 7
Maximum likelihood phylogenetic trees of 128 BUSCO genes of Dipylidium caninum genomes from this study and cestode genomes derived from GenBank, constructed using IQ Tree with gene-specific partition models. Accession numbers for genomes derived from GenBank and used in the BUSCO analysis are available in Table S2. Genomes from this study are highlighted in red. Species delimitation of the genus Dipylidium is highlighted.
Figure 8
Figure 8
Maximum likelihood nucleotide phylogenetic tree of 12 mitochondrial protein-coding genes of Dipylidium caninum mitochondrial genomes from this study and those derived from GenBank, constructed using IQ Tree with gene-specific partition models. Each leaf of the tree has the GenBank accession and cestode species name. Mitochondrial genomes from this study are highlighted in red. Species delimitation of the genus Dipylidium is highlighted. A tree with branch lengths is available in Figure S8.
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