Whole-genome sequencing provides novel insights into the evolutionary history and genetic adaptation of reindeer populations in northern Eurasia

Abstract

Domestic reindeer (Rangifer tarandus) play a vital role in the culture and livelihoods of indigenous people across northern Eurasia. These animals are well adapted to harsh environmental conditions, such as extreme cold, limited feed availability and long migration distances. Therefore, understanding the genomics of reindeer is crucial for improving their management, conservation and utilisation. In this study, we have generated a new genome assembly for the Fennoscandian domestic reindeer with high contiguity, making it the most complete reference genome for reindeer to date. The new genome assembly was utilised to explore genetic diversity, population structure and selective sweeps in Eurasian Rangifer tarandus populations which was based on the largest population genomic dataset for reindeer, encompassing 58 individuals from diverse populations. Phylogenetic analyses revealed distinct genetic clusters, with the Finnish wild forest reindeer (Rangifer tarandus fennicus) standing out as a unique subspecies. Divergence time estimates suggested a separation of ~ 52 thousand years ago (Kya) between the northern European Rangifer tarandus fennicus and Rangifer tarandus tarandus. Our study identified four main genetic clusters: Fennoscandian, the eastern/northern Russian and Alaskan group, the Finnish forest reindeer, and the Svalbard reindeer. Furthermore, two independent reindeer domestication processes were inferred, suggesting separate origins for the domestic Fennoscandian and eastern/northern Russian reindeer. Notably, shared genes under selection, including retroviral genes, point towards molecular domestication processes that aided adaptation of this species to diverse environments.

Figure 1

Jupiter consistency plot showing genome alignment between the reindeer assembly and cattle reference genome. The top 37 scaffolds (all above 10 Mb) represented 95% of the reindeer assembly and covered the entire 30 (29 autosomes and Chr X) chromosomes of the cattle reference genome. Coloured bands represent synteny between two genomes, and the crossing lines indicate possible genomic rearrangements or break points in the scaffolds.

Figure 2

Sample distribution. (a) Principal component analysis (PCA) plot based on filtered and LD-pruned SNPs of all 59 samples. (b) Geographic sites of reindeer populations included in this study. The 12 main populations are as follows: (1) Svalbard wild arctic reindeer (Sv-W-A – Svalbard, Norway): (2) Norwegian domestic tundra reindeer (No-D-R – Finmark and Filefjell, Norway); (3) Norwegian wild tundra reindeer (No-W-T – Hardangervidda, Norway); (4) Finnish domestic reindeer (Fi-D-R – Ivalo and Inari, Finland); (5) Finnish wild forest reindeer (Fi-F-R – Kuhmo, Finland); (6) Nenets domestic reindeer (Ar-D-R – Arkhangelsk, Russia); (7) Russian wild tundra-mountain reindeer (Ru-W-A – Novaja Zemlya, Russia); (8)—Russian wild tundra reindeer (Ru-W-T – Yamal and Taymyr, Russia); (9) Russian domestic forest reindeer (Ru-D-F – ZaiBaikal, Russia); (10) Eveny domestic reindeer (Ya-D-R – Yakutia, Russia); (11) Alaskan wild caribou (Al-W–C – Alaska, USA); (12) Alaskan domestic reindeer (Al-D-R – Alaska, USA).

Figure 3

Genetic relationships between 59 animals. Neighbour-joining (NJ) tree constructed to show genetic relationships between 59 animals, calculated from the single nucleotide polymorphism (SNP) data. Bootstrap confidence values obtained from 100 bootstrap replicates are shown at each branch. Seven main populations are highlighted by colour.

Figure 4

Population structure analysis of the twelve populations using ADMIXTURE. The bars represent individuals in a population and are segmented into colours based on the cluster assignment. The estimated proportion of the individual’s genome that belongs to a given cluster is indicated by the length of the coloured segment. The analysis was repeated with different assumed numbers of clusters (K) that are indicated on the y-axis. Population codes and domestication status of the individuals are indicated on the x-axis. Individuals have been sorted within the population based on the cluster assignment values.

Figure 5

Distribution of genes under selection in five major groups: the Finnish forest reindeer, the Norwegian wild tundra reindeer, the Fennoscandian domestic reindeer, the Nenets domestic reindeer and the Eveny domestic reindeer.