Whole-genome sequencing of Tarim red deer (Cervus elaphus yarkandensis) reveals demographic history and adaptations to an arid-desert environment

Abstract

Background: The initiation of desert conditions in the Tarim Basin in China since the late Miocene has led to the significant genetic structuring of local organisms. Tarim Red Deer (Cervus elaphus yarkandensis, TRD) have adapted to the harsh environmental conditions in this basin, including high solar radiation and temperature, aridity, and poor nutritional conditions. However, the underlying genetic basis of this adaptation is poorly understood.

Results: We sequenced the whole genomes of 13 TRD individuals, conducted comparative genomic analyses, and estimated demographic fluctuation. The ∂a∂i model estimated that the TRD and Tule elk (Cervus canadensis nannodes) populations diverged approximately 0.98 Mya. Analyses revealed a substantial influence of the Earth's climate on the effective population size of TRD, associated with glacial advances and retreat, and human activities likely underlie a recent serious decline in population. A marked bottleneck may have profoundly affected the genetic diversity of TRD populations. We detected a set of candidate genes, pathways, and GO categories related to oxidative stress, water reabsorption, immune regulation, energy metabolism, eye protection, heat stress, respiratory system adaptation, prevention of high blood pressure, and DNA damage and repair that may directly or indirectly be involved in the adaptation of TRD to an arid-desert environment.

Conclusions: Our analyses highlight the role of historical global climates in the population dynamics of TRD. In light of ongoing global warming and the increasing incidence of droughts, our study offers insights into the genomic adaptations of animals, especially TRD, to extreme arid-desert environments and provides a valuable resource for future research on conservation design and biological adaptations to environmental change.

Keywords: Arid-desert environment; Cervus elaphus; Environmental adaptability; Population demographic history; Tarim red deer; Whole genome sequencing.

Fig. 1

Distributional map of Tarim red deer in Xinjiang, China. The map shows the distribution of TRD populations (areas marked with white lines) and the origin of samples used in this study, and depicts annual average precipitation in the study area

Fig. 2

Population histories of Tarim red deer (TRD_Y) and Tule elk (TE_S) populations. a PSMC analysis inferring variation in N_e over the last 10⁶ years for the Tarim red deer and Tule elk populations. Generation time (g) = 6.3 years, and neutral mutation rate per generation (μ) = 1.5 × 10 ^− 8. b ∂a∂i analysis showing effective population sizes for the ancestral population and the Tarim red deer and Tule elk populations from ~ 1.17 × 10 ⁷ years ago to the present. The average number of migrants per year between the two populations in each time interval is indicated by the labeled arrows

Fig. 3

Linkage disequilibrium (LD) patterns for the Tarim red deer (TRD-Y) and Tule elk (TE-S) populations

Fig. 4

Genomic regions with strong selective signals in Tarim red deer. a Distribution of F_ST values calculated in 10-kb sliding windows. b Distribution of XP-EHH values calculated in 10-kb sliding windows. The dotted line above the figure corresponds to the top 5% of outliers with XP-EHH values > 2.1376. c Distribution of log₂ (θπ•control/θπ•Tarim red deer) and the top 5% highest Z(F_ST) values calculated in 40-kb sliding windows with 20-kb increments between Tarim red deer and the control Tule elk population. Data points in red [corresponding to the top 5% of the empirical log₂ (θπ ratio) with values > 0.827 and the top 5% of the empirical Z(F_ST) distribution with values > 0.734] are genomic regions under selection in Tarim red deer. The genes visualized in (a) and (b) are candidate genes in the Tarim red deer. d Venn diagram of candidate genes screened by F_ST-θπ and XP-EHH in Tarim red deer

Fig. 5

Enriched GO terms (a) and KEGG pathways (b) for genes detected in the selective sweep F_ST-θπ ratio (above) and XP-EHH (lower) analyses