Near-chromosomal de novo assembly of Bengal tiger genome reveals genetic hallmarks of apex predation

Abstract

The tiger, a poster child for conservation, remains an endangered apex predator. Continued survival and recovery will require a comprehensive understanding of genetic diversity and the use of such information for population management. A high-quality tiger genome assembly will be an important tool for conservation genetics, especially for the Indian tiger, the most abundant subspecies in the wild. Here, we present high-quality near-chromosomal genome assemblies of a female and a male wild Indian tiger (Panthera tigris tigris). Our assemblies had a scaffold N50 of >140 Mb, with 19 scaffolds corresponding to the 19 numbered chromosomes, containing 95% of the genome. Our assemblies also enabled detection of longer stretches of runs of homozygosity compared to previous assemblies, which will help improve estimates of genomic inbreeding. Comprehensive genome annotation identified 26,068 protein-coding genes, including several gene families involved in key morphological features such as the teeth, claws, vision, olfaction, taste, and body stripes. We also identified 301 microRNAs, 365 small nucleolar RNAs, 632 transfer RNAs, and other noncoding RNA elements, several of which are predicted to regulate key biological pathways that likely contribute to the tiger's apex predatory traits. We identify signatures of positive selection in the tiger genome that are consistent with the Panthera lineage. Our high-quality genome will enable use of noninvasive samples for comprehensive assessment of genetic diversity, thus supporting effective conservation and management of wild tiger populations.

Keywords: Bengal tiger; ROH; genome assembly; reference genome.

Figure 1:

Bengal tiger genome assembly. (A, B) Circos plot representing the near-chromosome-level assembly of female (MC) (A) and male (SI) (B) Bengal tiger genomes. The 2 outermost tracks represent the chromosome length (Mb) and ID. Repeat content per 100-kb window per chromosome (red line represents the mean genome-wide mean repeat content ∼36%) is shown in black. Gene density (green lines indicate 1–5 genes per 100-kb window per chromosome, orange 5–10, and red >10 genes) is displayed next. The innermost track represents GC% per 100-kb window per chromosome (blue line represents mean GC%: ∼41%). (C) Y-linked scaffolds from the male tiger genome assembly. Circos plot track as in A and B. (D) Chromosome painting showing synteny between domestic cat genome (FelCat9.0; Genbank: GCA_000181335.4) and the female Bengal tiger (MC) scaffolds. (E) Genomic inbreeding coefficients (F_ROH) derived from runs of homozygosity (ROH) of different lengths (>100 Kb, >1 Mb, and >10 Mb) and (F) boxplot of binned distribution of ROH lengths in the 4 zoo-bred tigers as derived when using the MC, SI, and Malayan tiger genomes as the reference genome.

Figure 2:

Genome annotation and functional genes. (A) Bar plot of the number of predicted genes and corresponding transcripts observed in the MC genome assembly and putative Y-linked scaffolds in the SI genome assembly. (B) Putative genes involved in various key biological pathways important for apex predatory traits. (C) Complete Slc45a gene structure, including the predicted transmembrane (TM) domains. Multiple sequence alignment of the Scl45a C-terminal region showing the A477>V mutation observed in white tiger. (D) Schematic diagram of full-length Corin gene. Multispecies alignment of the Corin LDL receptor domain depicting the known H>Y mutation associated with golden tabby pelage pattern [74].

Figure 3:

Phylogeny and positive selection analysis. (A) Phylogeny tree constructed using single-copy orthologs from selected Panthera and out-group species. (B) Scatterplot of evolutionary rates of single-copy key pattern and pelage-related gene orthologs identified in the Bengal tiger genome. (C) Pathway analysis of single-copy orthologs within the Pantheralineage showing gene network interaction models. cfa, Canis familiaris (dog); eca, Equus caballus (domesticated horse); fca, Felis catus (domestic cat); lca, Lynx canadensis (Canada lynx); nne, Neofelis nebulosa (clouded leopard); ocu, Oryctolagus cuniculus (rabbit); pco, Puma concolor (cougar); ple, Panthera leo (lion); pon, Panthera onca (jaguar); ppa, Panthera pardus (leopard); pta, Panthera tigris altaica (Amur tiger); ptm, Machali Bengal tigress (female); pts, south Indian Bengal tiger (male).