Revealing the coexistence of differentiation and communication in an endemic hare, Lepus yarkandensis (Mammalia, Leporidae) using specific-length amplified fragment sequencing

Abstract

Background The Yarkand hare (Lepus yarkandensis Günther, 1875) is endemic to oasis and desert areas around the Tarim Basin in the Xinjiang Uyghur Autonomous Region of northwest China; however, genome-wide information for this species remains limited. Moreover, the genetic variation, genetic structure, and phylogenetic relationships of Yarkand hare from the plateau mountain regions have not been reported. Thus, we used specific-length amplified fragment sequencing (SLAF-seq) technology to evaluate the genetic diversity of 76 Yarkand hares from seven geographic populations in the northern and southwestern parts of the Tarim Basin to investigate single-nucleotide polymorphism (SNP) marker-based population differentiation and evolutionary processes. Selective sweep analysis was conducted to identify genetic differences between populations. Results Using SLAF-seq, a total of 1,835,504 SNPs were initially obtained, of which 308,942 high-confidence SNPs were selected for further analysis. Yarkand hares exhibited a relatively high degree of genetic diversity at the SNP level. Based on pairwise FST estimates, the north and southwest groups showed a moderate level of genetic differentiation. Phylogenetic tree and population structure analyses demonstrated evident systematic phylogeographical structure patterns consistent with the geographical distribution of the hares. Hierarchical analysis of molecular variation further indicated that genetic variation was mainly observed within populations. Low to moderate genetic differentiation also occurred among populations despite a common genomic background, likely due to geographical barriers, genetic drift, and differential selection pressure of distinct environments. Nevertheless, the observed lineage-mixing pattern, as indicated by the evolutionary tree, principal component analysis, population structure, and TreeMix analyses, suggests a certain degree of gene flow between the north and southwest groups. This may be related to the migration of hares to high-altitude water sources southwest of the basin during glacial climatic oscillations, as well as river re-diffusion and oasis restoration in the basin following the glacial period. We also identified candidate genes, and their associated gene ontology terms and pathways, related to the adaptation of Yarkand hares to different environmental habitats. Conclusions The identified genome-wide SNPs, genetic diversity, and population structure of Yarkand hares expand our understanding of the genetic background of this endemic species and provide valuable insights into its environmental adaptation, allowing for further exploration of the underlying mechanisms.

Population genetics analysis of Tolai hares (Lepus tolai) in Xinjiang, China using genome-wide SNPs from SLAF-seq and mitochondrial markers

“…In this study, we used a set of SLAF-seq genome-wide SNP and mtDNA markers to estimate the genetic diversity of Tolai hares in Xinjiang. At the genome-wide level, the genetic diversity of Tolai hares based on SNPs was higher (Table 2) (π = 0.05926, He = 0.37412, Ho = 0.40226, PIC = 0.2974) than that of other reported species, including rabbits (PIC = 0.2-0.2281, He = 0.2511-0.2857, Ho = 0.3072-0.3418, (Ren et al, 2019), and Yarkand hares (π = 0.0655, He = 0.3130, Ho = 0.2852, PIC = 0.2543 (Ababaikeri et al, 2021). The estimated nucleotide diversity of Tolai hares (π = 0.0442) based on mtDNA was also relatively high compared to other Lepus taxa, such as brown hares (π D-LOOP = 0.030, (Minoudi et al, 2018), Yarkand hares (π D-LOOP = 0.033, π CYTB = 0.008, (Shan et al, 2011), and Italian hares (L. corsicanus, π D-LOOP = 0.018, (Pierpaoli et al, Frontiers in Genetics frontiersin.org 2003).…”

“…This also occurs in Yarkand hare in Xinjiang. The population genetics of Yarkand hares based on SNPs (Ababaikeri et al, 2021) and mtDNA (Shan et al, 2011) showed a systematic geographical distribution pattern and genetic differentiation between the north and southwest populations, which may have been caused by geographical isolation and different living environment. It is concluded that geographical isolation and complex habitats can affect hare populations' genetic structure and differentiation.…”

“…The southwest of Tarim Basin in Xinjiang, China, as the origin of rivers in the basin, was a glacial refugia for Yarkand hares (L. yarkandensis) during the Quaternary climate oscillations, providing a suitable environment for maintaining the relatively high genetic diversity of this species (Shan et al, 2011). In addition, genome-wide SNPs have confirmed differentiation between the southwest and northern populations (Ababaikeri et al, 2021) and higher diversity in the former population.…”

“…SNPs are found throughout the genome, and their distribution can reflect the population's genetic variation. SLAF-seq has been used to analyze several species' genetic diversity and phylogenetic structure (Li et al, 2017;Chang et al, 2019;Qin et al, 2019;Zhang J. et al, 2020a;Fang et al, 2020;Ababaikeri et al, 2021). In addition, mtDNA provides a different perspective of population genetic structure because it is maternally inherited and generally lacks intermolecular recombination (Allendorf, 2017).…”

Expression Regulation of Water Reabsorption Genes and Transcription Factors in the Kidneys of Lepus yarkandensis

“…Compared with Oryctolagus cuniculus and other hares, L. yarkandensis has many specific adaptations to arid environments. These adaptations have been explored using SNP analysis, population structure (Ababaikeri et al, 2021), mitochondrial genome sequencing, phylogenetic tree construction (Shan et al, 2021), as well as aquaporin (AQP) expression in the kidney, gastrointestinal tract, and lungs (Zhang et al, 2019a;Zhang et al, 2019b;Zhang et al, 2020).…”