Endangered Père David's deer genome provides insights into population recovering

Abstract

The Milu (Père David's deer, Elaphurus davidianus) were once widely distributed in the swamps (coastal areas to inland areas) of East Asia. The dramatic recovery of the Milu population is now deemed a classic example of how highly endangered animal species can be rescued. However, the molecular mechanisms that underpinned this population recovery remain largely unknown. Here, different approaches (genome sequencing, resequencing, and salinity analysis) were utilized to elucidate the aforementioned molecular mechanisms. The comparative genomic analyses revealed that the largest recovered Milu population carries extensive genetic diversity despite an extreme population bottleneck. And the protracted inbreeding history might have facilitated the purging of deleterious recessive alleles. Seventeen genes that are putatively related to reproduction, embryonic (fatal) development, and immune response were under high selective pressure. Besides, SCNN1A, a gene involved in controlling reabsorption of sodium in the body, was positively selected. An additional 29 genes were also observed to be positively selected, which are involved in blood pressure regulation, cardiovascular development, cholesterol regulation, glycemic control, and thyroid hormone synthesis. It is possible that these genetic adaptations were required to buffer the negative effects commonly associated with a high-salt diet. The associated genetic adaptions are likely to have enabled increased breeding success and fetal survival. The future success of Milu population management might depend on the successful reintroduction of the animal to historically important distribution regions.

Keywords: Père David's deer; breeding success; population recovering; selective pressure; the high‐salt diet.

Figure 1

The history of the Milu. (a) Paleogeographic distribution history of wild Milu in China. The data for Milu fossils were adopted from Cao, 2005. The color relates to the density of the fossils in specific provinces, and the density was calculated as the number of fossils per million square kilometers. (b) Milu foraging in the coastal shoal habitat of Dafeng Milu Natural Reserve, Jiangsu, China. (c) Large‐scale reintroduction programs since 1985. (c) fawn; F, females; M, males. (d) Demographic history of the Milu. The history of the Milu population and climate change spans from 3 KYA to 4 MYA. We used the default mutation rate of 1.5 × 10^–8 for baiji (μ) and an estimation of 6 years per generation (g). The last glacial maximum (LGM) is highlighted in gray. Tsurf, atmospheric surface air temperature; RSL, relative sea level; 10 m.s.l.e., 10 m sea level equivalent. (e) Box plot of Froh for Milu, crested ibis, panda, and polar bear populations. Froh denotes the proportion of total ROH length. (f) Box plot of length of ROH in each individual from Milu, crested ibis, panda, and polar bear

Figure 2

Genetic diversity of the Milu and other animals. (a) Box plot of heterozygosity for Milu, crested ibis, panda, and polar bear individuals. Only heterozygous SNPs were included. CI, Crested Ibis; ML, Milu; PA: Panda; PB: Polar bear. (b) Bias distribution of SNPs in animal genomes. Each circle denotes a single species as in (a). L, low‐SNP density region; H, high‐SNP density region; kbp, kilobase; the proportion of the total length of L and H regions in the whole genome is represented in green and purple; the percentage of SNPs in the L and H regions to the total SNP number in both L and H regions are light blue and blue. (c) Ratio of heterozygosity in each genomic element. The genomes were subdivided into three regions—exons, introns, and other (regions that were neither exons nor introns). Heterozygosity in each type of genomic element was compared to heterozygosity of the whole genome. (d) Classification of missense variants. DE: deleterious; TO: Tolerated; and OT: Other

Figure 3

The putative positive selective genes involved in high‐salt diet adaptation and breeding success

Figure 4

Positive selective pressure signals on genes putatively involved in sodium channels and high‐salt diet. (a) The positive selection analysis on the epithelial sodium channel (ENaC). Red dot, milu‐specific SAPs (single amino acid polymorphisms); red circle, damaging milu‐specific SAPs predicted by PPH2. Red arrows represent the positive selective sites. (b) The salinity of forage plants in Dafeng Milu Natural Reserve