Characterization Of Inbreeding Depression In The Genome Of The South China Tiger:a Comparative Study With The Amur Tiger

The South China tiger(Panthera tigris amoyensis)is a tiger subspecies endemic to China.It has been functionally extinct in the wild,leaving a captive population derived from six wild founders.Although a precise studbook has been established based on which genetic management has been applied,reproduction within such small number of founders could not avoid inbreeding.With the gradual increment of inbreeding level,the captive population has suffered from severe inbreeding depression and expressed high juvenile mortality and low adult reproduction ability.In addition,a female wild founder was discovered to carry genes of north Indochinese tiger(P.t.corbetii)and spreaded to all current offspring.In this situation,issues like how to deal with introgressed genes,how to accelerate and completely solve inbreeding depression are the key determinators of the future of the South China tiger.Since 1986,a captive Amur tiger(P.t.altaica)population has been established in China Hengdaohezi Feline Animal Breeding Center and developed to be the core ex situ conservation population of this endangered subspecies.The husbandry and management of this population are similar to that applied to the South China tiger.However,this population preserves high genetic diversity with low inbreeding level and unnoticeable inbreeding depression.These contrasts make it an ideal reference to study inbreeding depression of the South China tiger.In order to substantially reform genetic management strategy,de novo chromosome-level high quality genomes of a South China tiger and an Amur tiger were assembled and characterized,and a small population of each subspecies were re-sequenced subsequently.Based on these,the divergence time between the two subspecies,the effective population dynamic history and inbreeding time were inferred.Genomic signatures of inbreeding,genetic loads and purging strength were also analyzed.The main findings are as follow:1.The two tiger genomes assembled in this study are of the best tiger assemblies available so far,providing the first reference genome for the South China tiger and the improved version of the Amur tiger genome.2.Comparative analysis showed that glucose metabolism related genes are under positive selection in the South China tiger,while genes involving lipid genesis and decomposition and energy storage are under positive selection in Amur tiger,implying the differential adaptation to warm and cold climate of the two subspecies.3.Amur tiger completely separated from South China tiger about 7 kya,both experienced significant effective populations decline since then,and the South China tiger reached bottom700-800 year ago,with no more restoration.4.The number of deleterious non-synonymous SNP and lose of function mutations and the number of genes influenced were all significantly higher in South China tiger than in Amur tiger.However,the rate of these loads in homozygous state was lower than in Amur tiger.This suggests deleterious mutations are widespread across the genome but under moderate purging in South China tiger.5.Numerous long and continuous runs of homozygosity(ROH)and identical by descent(IBD)are highly shared among individuals in the South China tiger with extensive influence on genes,such as the long shared IBD covers 580 genes on Chr B4.This suggests inbreeding had started before establishment of the captive population,and has leaded to numerous chances of deleterious alleles to be homozygous.Quality of offspring would be influenced continuously and high mortality be normalcy.The results above show accuracy of genetic management would be significantly improved given whole genome analysis of ROH,IBD,genetic load and heterozygosity are used;Purifying South China tiger through eliminating individuals possessing introgressed genes from Indo Chinese tiger would further reduce the gene pool and exacerbate inbreeding impacts;There is no option except for genetic rescue to completely solve the inbreeding,but gene donor selection should be based on genomic analysis for reducing ROH and IBD,wrapping deleterious alleles into heterozygous state and minimizing introduction of new genetic loads.This study add fundamental evidence to create effective and feasible rescue strategy for the most endangered South China tiger,but also provides abundant clues and reference genome to understand mechanism of inbreeding depression of large felids represented by tiger.