Research Article

Biological adaptations in the Arctic cervid, the reindeer (Rangifer tarandus)

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Science  21 Jun 2019:
Vol. 364, Issue 6446, eaav6312
DOI: 10.1126/science.aav6312

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Phylogeny and characteristics of ruminants

Ruminants are a diverse group of mammals that includes families containing well-known taxa such as deer, cows, and goats. However, their evolutionary relationships have been contentious, as have the origins of their distinctive digestive systems and headgear, including antlers and horns (see the Perspective by Ker and Yang). To understand the relationships among ruminants, L. Chen et al. sequenced 44 species representing 6 families and performed a phylogenetic analysis. From this analysis, they were able to resolve the phylogeny of many genera and document incomplete lineage sorting among major clades. Interestingly, they found evidence for large population reductions among many taxa starting at approximately 100,000 years ago, coinciding with the migration of humans out of Africa. Examining the bony appendages on the head—the so-called headgear—Wang et al. describe specific evolutionary changes in the ruminants and identify selection on cancer-related genes that may function in antler development in deer. Finally, Lin et al. take a close look at the reindeer genome and identify the genetic basis of adaptations that allow reindeer to survive in the harsh conditions of the Arctic.

Science, this issue p. eaav6202, p. eaav6335, p. eaav6312; see also p. 1130

Structured Abstract

INTRODUCTION

Reindeer (Rangifer tarandus) are naturally distributed across the Arctic and subarctic regions. Consequently, these animals have evolved to face numerous challenges, including exposure to severe cold, limited food availability in winter, and extremely prolonged light or dark periods. Unlike all other cervid species, both male and female reindeer annually grow deciduous antlers. Furthermore, reindeer are the only fully domesticated species among the Cervidae. However, little is known about the underlying genetic causes of these traits.

RATIONALE

We performed comparative genomic analyses between reindeer, other ruminant species, and a number of mammalian outgroups to identify rapidly evolving genes, positively selected genes, and reindeer-specific mutants. We further resequenced the genomes of three domestic reindeer from northern China and three wild reindeer from Northern Europe to validate that the reindeer-specific mutations are fixed in the species rather than individual polymorphisms. To support our computationally derived insights, we subsequently conducted in vitro functional experiments to investigate possible functional consequences of some of the reindeer-specific mutated genes.

RESULTS

We found two genes (CYP27B1 and POR) involved in the vitamin D metabolism pathway to be under positive selection in reindeer. Furthermore, our functional experiments validated that the two key enzymes (CYP27B1 and POR) exhibit much higher catalytic activity than that of the orthologs in goats and roe deer. We also identified fixed reindeer-specific mutations in genes that play a role in fat metabolism, including APOB and FASN. We showed that a mutation upstream of the reindeer CCND1 gene endows an extra functional binding motif to the androgen receptor and thus may result in female antler growth. In the circadian rhythm pathway, we observed that eight genes have reindeer-specific mutations and that four genes have been rapidly evolving. Among them, the Pro1172→Thr (P1172T) mutation in the reindeer PER2 causes loss of binding ability with CRY1, which can cause arrhythmicity. Finally, we found reindeer-specific mutations in 11 genes relating to development, migration, and differentiation of neural crest cells, probably accounting for the tameness of reindeer.

CONCLUSION

Our results reveal the genetic basis of a broad spectrum of the Arctic deer’s traits and provide a basis for understanding mammalian adaptive strategies to the Arctic. Our comparative genomic studies and functional assays identify a number of genes that exhibit functionality related to circadian arrhythmicity, vitamin D metabolism, docility, and antler growth, as well as genes that are uniquely mutated and/or are under positive selection. Our results may provide insights relevant to human health, including how the genetic response of vitamin D in reindeer affects bone and fat metabolism and how genes can affect circadian arrhythmicity.

Unique mutations explain the biological adaptations of reindeer.

(Left) Two genes (POR and CYP27B1) play an important role in vitamin D metabolism in reindeer. (Middle) A newly identified binding motif of the androgen receptor (AR) evolved upstream of a key antler CCND1 gene, which may result in female antler growth. bp, base pairs. (Right) A key reindeer-specific mutation (P1172T) in PER2 results in loss of binding ability with CRY1, which can cause the observed circadian arrhythmicity in reindeer. The circadian genes highlighted in red are positively selected in reindeer; the ones shown in blue are rapidly evolving genes. PACAP, pituitary adenylate cyclase activating polypeptide; SCN, suprachiasmatic nucleus; ER, endoplasmic reticulum; CREB, cAMP response element–binding protein; nNOS, neuronal nitric oxide synthase; P, phosphorus; G, G protein.

PHOTO: YIFENG YANG

Abstract

The reindeer is an Arctic species that exhibits distinctive biological characteristics, for which the underlying genetic basis remains largely unknown. We compared the genomes of reindeer against those of other ruminants and nonruminant mammals to reveal the genetic basis of light arrhythmicity, high vitamin D metabolic efficiency, the antler growth trait of females, and docility. We validate that two reindeer vitamin D metabolic genes (CYP27B1 and POR) show signs of positive selection and exhibit higher catalytic activity than those of other ruminants. A mutation upstream of the reindeer CCND1 gene endows an extra functional binding motif of the androgen receptor and thereby may result in female antlers. Furthermore, a mutation (proline-1172→threonine) in reindeer PER2 results in loss of binding ability with CRY1, which may explain circadian arrhythmicity in reindeer.

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