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
  • 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
  • Fig. 1 Vitamin D metabolism in reindeer.

    (A) Alterations in the vitamin D metabolism pathways of reindeer. The genes involved in this pathway are labeled with different colors. Red genes are under positive selection, orange genes exhibit specific mutations in reindeer, and blue genes exhibit increased Ka/Ks values in reindeer. CoA, coenzyme A; h, Planck’s constant; ν, frequency. (B) Specific mutations in the CYP27B1 gene. There are three specific mutations (table S3), including one (K282N) in the P450 domain of CYP27B1. The CYP27B1 protein sequences of multiple species (indicated with different colors) were aligned, and the alignments of the K282N adjacent region are shown here. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr. (C) 3D structure simulation of reindeer CYP27B1 compared with that of cattle. The 3D structure of POR is provided in fig. S3. (D and E) Enzyme activities of reindeer CYP27B1 and POR compared with those of roe deer and goat in vitro. **P < 0.01 calculated from the t test. Error bars indicate SD. prot, protein.

  • Fig. 2 Androgen receptor affinity sequence 5′-TGTTCT-3′ upstream of CCND1.

    (A) Characteristic antler of a female reindeer. (B) Three 5′-TGTTCT-3′ motifs were identified upstream of the reindeer CCND1 gene. Motif 1 exists only in deer, whereas motif 3 exists only in reindeer. bp, base pairs. (C) ChIP-qPCR assays validated that the androgen receptor binds to both motif 2 and motif 3 of reindeer, but only to motif 2 of roe deer. Error bars indicate SD.

    PHOTO: YIFENG YANG
  • Fig. 3 Mutations in the reindeer circadian rhythm genes and pathways.

    Orange genes have reindeer-specific mutations; blue genes exhibit increased Ka/Ks values in reindeer. (A) Light regulates the molecular clockwork in reindeer SCN neurons. G, G protein; P, phosphorus; nNOS, neuronal nitric oxide synthase; ER, endoplasmic reticulum. (B) The reindeer-specific mutation (P1172T) of PER2 is located within the binding domain of the PER2-CRY complex, as determined by 3D modeling. The site of this mutation is marked in red. (C) Co-IP assays show that reverted PER2-T1172P (P-type) proteins can bind to CRY1, but reindeer PER2-P1172T (T-type) cannot bind. CRY1-Flag was transfected with or without PER2–hemagglutinin (HA) or PER2-T1172P, and Co-IP was conducted. IB, immunoblot. (D) The NOCT gene functional domain has specific mutations (fig. S5). The reindeer NOCT gene has two specific mutations (S276P and Q313R) in the C-terminal deadenylase domain. The amino acid substitution in reindeer is indicated in red.

  • Fig. 4 Genes altered in reindeer play a role in neural crest development, migration, and differentiation.

    Red genes are under positive selection in reindeer, orange genes have reindeer-specific mutations, and blue genes exhibit increased Ka/Ks values in reindeer. Five genes (CAD6, BCAT1, ID3, CAD11, and MSX2) participating in the development of NCCs, four genes (TCOF1, BCAT1, NOTCH2, and NOTCH3) involved in the migration of NCCs, and two genes (SI and KIT) related to the differentiation of NCCs into melanocytes were found to have specific mutations in reindeer. In addition, one gene (ASCL1) related to the differentiation of NCCs into neurons and one gene (GEM) involved in the development of NCCs showed increased Ka/Ks values in reindeer. One gene (COL2A1) related to the differentiation of NCCs into chondrocytes was under positive selection in reindeer.

Supplementary Materials

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

    Zeshan Lin, Lei Chen, Xianqing Chen, Yingbin Zhong, Yue Yang, Wenhao Xia, Chang Liu, Wenbo Zhu, Han Wang, Biyao Yan, Yifeng Yang, Xing Liu, Kjersti Sternang Kvie, Knut Håkon Røed, Kun Wang, Wuhan Xiao, Haijun Wei, Guangyu Li, Rasmus Heller, M. Thomas P. Gilbert, Qiang Qiu, Wen Wang, Zhipeng Li

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Figs. S1 to S7
    • Tables S1 to S7
    • Captions for Tables S8 to S11
    • References
    Table S8
    The reindeer positively selected genes.
    Table S9
    The reindeer specific mutation in 84 genes.
    Table S10
    All reindeer specific mutation genes.
    Table S11
    The reindeer rapidly evolving genes.

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