Whole-genome sequencing of reindeer (Rangifer tarandus) populations reveals independent origins of dwarf ecotypes and potential molecular mechanisms underpinning cold adaptation

Abstract

Abstract Background Reindeer (Rangifer tarandus) are iconic mammals that inhabit the Arctic and sub-Arctic regions. In these areas, reindeer not only play a vital ecological role, but they also hold cultural and economic significance for indigenous communities. In order to thrive in the harsh conditions of the northernmost areas of the world, reindeer have developed an array of phenotypic adaptations, especially in the ecotypes living in the High Arctic. Therefore, a thorough understanding of population structure, history, and genetic diversity of reindeer is useful for their sustainable management and to guide long-term conservation efforts. Results We conducted whole-genome sequencing of a male R. t. tarandus specimen from Norway's Hardangervidda region, generating a highly continuous and complete genome assembly that can be used as a reference genome for genetic analyses focusing on the Fennoscandian reindeer. We also sequenced reindeer ecotypes from across the globe and generated de novo sequences from two ancient samples. Our analysis suggests an independent evolution of small-sized phenotypes in specific high-arctic ecotypes, such as the Svalbard reindeer (R. t. platyrhynchus) and Peary caribou (R. t. pearyi). We describe how the demographic bottleneck that affected the reindeer in the Svalbard archipelago resulted in reduced genetic variability compared to mainland Norway reindeer. Our data suggests that these two distinct ecotypes were likely independent populations before the last glaciation. Finally, we also observe an enriched number of genes associated with cilium motility and cilium assembly presenting missense variants between these two ecotypes, potentially linked to adaptations in the extreme arctic environment. For instance, some of these genes play a role in respiratory cilia movement, potentially improving respiratory function in cold environments. Conclusions Our findings provide new insights into the genetic basis of small body size adaptations in reindeer ecotypes and highlight the impact of environmental constraints on their populations. Our high-quality reference genome and associated resources will aid in addressing epidemiological, conservation, and management challenges faced by reindeer populations in a rapidly changing world.