Comparative genomics and metagenomics analyses of endangered Père David’s deer (Elaphurus davidianus) provide insights into population recovery

Abstract

The milu (Pere Davids deer, Elaphurus davidianus) has become a classic example of how highly endangered animal species can be rescued. However, the mechanisms that underpinned this population recovery remain largely unknown. As part of this study, we sequenced and analyzed whole genomes from multiple captive individuals. Following this analysis, we observed that the milu experienced a prolonged population decline over the last 200,000 years, which led to an elongated history of inbreeding. This protracted inbreeding history facilitated the purging of deleterious recessive alleles, thereby ameliorating associated threats to population viability. Because of this phenomenon, milu are now believed to be less susceptible to future inbreeding depression occurrences. SNP distribution patterns confirmed inbreeding history and also indicated sign of increased and increasing diversity in the recovered milu population. A selective sweep analysis identified two outlier genes (CTSR2 and GSG1) that were related to male fertility. Furthermore, we observed strong signatures of selection pertaining to the host immune system, including six genes (SERPINE1, PDIA3, CD302, IGLL1, VPREB3, and CD53 antigen), which are likely to strengthen resistance to pathogens. We also identified several adaptive features including the over-representation of gene families encoding for olfactory receptor activity, a high selection pressure pertaining to DNA repair and host immunity, and tolerance to high-salt swamp diets. Moreover, glycan biosynthesis, lipid metabolism, and cofactor and vitamin metabolism were all significantly enriched in the gut microbiomes of milu. We speculate that these characteristics play an important role in milu energy metabolism, immunity, development, and health. In conclusion, our findings provide a unique insight into animal population recovery strategies.