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Genomic and phenotypic evidence support visual and olfactory shifts in primate evolution

Nature Ecology & Evolution volume 9, pages 721–733 (2025)Cite this article

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Abstract

Sensory trade-offs between vision and olfaction in the evolution and radiation of primates have long been debated. However, insights have been limited by a lack of sensory gene sequences and accompanying functional predictions. Here we conduct large-scale functional analyses of visual and olfactory receptors and related brain regions across extant primates. Our results reveal a visual shift from ultraviolet to violet colour sensitivity in early haplorrhine primates, followed by acceleration in the rhodopsin retinal release rates at the origin of anthropoids, both of which are expected to greatly enhance visual acuity under brighter light conditions. Additionally, we find that the sensitivity of olfactory receptors shifted from narrowly to broadly tuned early in anthropoid evolution. In contrast, strepsirrhines appear to have retained sensitive dim-light vision and underwent functional enhancement of narrowly tuned olfactory receptors. Our models indicate that this would have enhanced odorant discrimination and facilitated olfaction-mediated physiology and behaviour. These differences in tuning patterns of olfactory receptors between major primate lineages mirror well-established morphological differences in external anatomy and brain structures, revealing new mechanisms of olfactory adaptation and evolutionary plasticity. Our multisystem analyses reveal patterns of co-evolution in genomic, molecular and neuroanatomical traits that are consistent with a sensory ‘reallocation’ rather than strict trade-offs.

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Fig. 1: Hypotheses of diel activity shifts of early primates based on opsin evidence.
Fig. 2: Divergent evolution of differently tuned ORs.
Fig. 3: Variation of the speculated odorant recognition code by NTORs in primate evolution.
Fig. 4: Co-evolution between visual and olfactory genotypes and phenotypes and neuroanatomical traits.

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Data availability

All sequence and phenotypic data are listed in the text and Supplementary Information. Source data are provided with this paper.

Code availability

Code to run the analyses is available at https://github.com/GanglabSnnu/OR_identify.

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Acknowledgements

We thank W. J. Murphy for providing valuable comments on earlier versions of this manuscript, R. Crouch from Medical University of South Carolina and L. Neuhold from National Eye Institute, NIH for 11-cis-retinal, H. Jing from Shaanxi Normal University for technical support and M. dos Reis from Queen Mary, University of London, for useful discussions about ancestral sequence reconstruction. We also thank the National Research Facility for Phenotypic & Genetic Analysis of Model Animals (Primate Facility) (https://cstr.cn/31137.02.NPRC) for providing technical support. This work was funded by the National Natural Science Foundation of China grant nos. 32270462 (Y.L.), 32470445 (G.L.), 32270525 (H.L.) and 31822048 (D.-D.W.), the Natural Science Basic Research Programme of Shaanxi grant nos. 2021JM-197 (Y.L.), 2020JM-280 (G.L.) and 2021JM-053 (H.L.), the Fundamental Research Funds for the Central Universities grant nos. GK202102006 (Y.L.), GK201902008 (G.L.), 2020TS050 (H.C.), the Strategic Priority Research Programme of the Chinese Academy of Sciences grant no. XDPB17 (D.-D.W.), Yunnan Provincial Science and Technology Department grant no. 202305AH340006 (D.-D.W.), National Sciences and Engineering Research Council of Canada grant no. RGPIN-2017-03782 (A.D.M.), Canada Research Chairs programme no. 950-231257 (A.D.M.) and were also supported in part by the Intramural Research Programme of the NIH (National Institute of Mental Health and National Institute on Aging) (A.R.D.).

Author information

Author notes

  1. These authors contributed equally: Hai Chi, Jiahui Wan, Amanda D. Melin.

Authors and Affiliations

  1. College of Life Sciences, Shaanxi Normal University, Xi’an, China

    Hai Chi, Yimeng Cui, Xin Guo, Le Zhao, Tianmin Zhang, Yue Zhan, Na Li, Jinqu Guo, Zhe Xu, Wenhui Hou, Yumin Cao, Jiaqing Yuan, Jinhong Wang, Shengjing Song, Yang Liu & Gang Li

  2. School of Life Sciences, Northwestern Polytechnical University, Xi’an, China

    Jiahui Wan, Sufang Wang, Yudan Zhang, Tianmin Zhang, Qian Li, Jiangmin Zheng & Huimeng Lu

  3. Department of Anthropology and Archaeology, University of Calgary, Calgary, Alberta, Canada

    Amanda D. Melin

  4. Department of Medical Genetics, University of Calgary, Calgary, Alberta, Canada

    Amanda D. Melin

  5. Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada

    Amanda D. Melin

  6. Computational and Evolutionary Neurogenomics Unit, National Institute on Aging, Bethesda, MD, USA

    Alex R. DeCasien

  7. College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang, China

    Yimeng Cui & Yue Zhan

  8. QinLing-Bashan Mountains Bioresources Comprehensive Development C. I. C., School of Bioscience and Engineering, Shaanxi University of Technology, Hanzhong, China

    Le Zhao & Gang Li

  9. School of Biological and Behavioural Sciences, Queen Mary, University of London, London, UK

    Joseph Williamson & Stephen J. Rossiter

  10. State Key Laboratory of Genetic Evolution & Animal Models, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Yong Shao, Guojie Zhang & Dong-Dong Wu

  11. Guangzhou Zoo & Guangzhou Wildlife Research Center, Guangzhou, China

    Wu Chen

  12. School of Life Sciences, Westlake University, Hangzhou, China

    Xiaoli Lu

  13. Shaanxi Key Laboratory for Animal Conservation, College of Life Sciences, Northwest University, Xi’an, China

    Xiaoguang Qi

  14. BGI-Shenzhen, Shenzhen, China

    Guojie Zhang

  15. Villum Center for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark

    Guojie Zhang

  16. National Resource Center for Non-Human Primates, Kunming Primate Research Center, and National Research Facility for Phenotypic & Genetic Analysis of Model Animals (Primate Facility), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Dong-Dong Wu

  17. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China

    Dong-Dong Wu

Authors
  1. Hai Chi
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  2. Jiahui Wan
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  3. Amanda D. Melin
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  4. Alex R. DeCasien
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  5. Sufang Wang
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  6. Yudan Zhang
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  7. Yimeng Cui
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  8. Xin Guo
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  9. Le Zhao
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  10. Joseph Williamson
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  11. Tianmin Zhang
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  12. Qian Li
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  13. Yue Zhan
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  14. Na Li
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  15. Jinqu Guo
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  16. Zhe Xu
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  17. Wenhui Hou
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  18. Yumin Cao
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  19. Jiaqing Yuan
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  20. Jiangmin Zheng
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  21. Yong Shao
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  22. Jinhong Wang
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  23. Wu Chen
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  24. Shengjing Song
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  25. Xiaoli Lu
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  26. Xiaoguang Qi
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  27. Guojie Zhang
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  28. Stephen J. Rossiter
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  29. Dong-Dong Wu
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  30. Yang Liu
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  31. Huimeng Lu
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  32. Gang Li
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Contributions

Y.L., H.L., G.L. and D.-D.W. designed and supervised the research. H.C., A.D.M., Y.L., Y. Cui, X.G., Y. Zhan, N.L., J.G. and Z.X. performed evolutionary analyses and experimental assays for visual pigments. H.L., G.L., J. Wan, S.W., Y. Zhang, L.Z., J. Williamson, T.Z., Q.L., W.H., Y. Cao, J.Y., J.Z., Y.S., J. Wang and W.C. carried out functional modelling analyses for ORs. A.R.D. conducted integrative analyses of genetic, sensory and neuroanatomical data. G.L., Y.L., A.D.M., S.J.R., A.R.D., H.L., D.-D.W., H.C., S.S., X.L., X.Q. and G.Z. wrote the paper with comments from all listed authors.

Corresponding authors

Correspondence to Dong-Dong Wu, Yang Liu, Huimeng Lu or Gang Li.

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Competing interests

The authors declare no competing interests.

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Peer review information

Nature Ecology & Evolution thanks Robert Barton, Robert Meredith, Yoshihito Niimura and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Methods, Text, Figs. 1–16, Tables 1–3 and References.

Reporting Summary

Supplementary Data

Predicted binding odorants for each OR functional cluster.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

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Chi, H., Wan, J., Melin, A.D. et al. Genomic and phenotypic evidence support visual and olfactory shifts in primate evolution. Nat Ecol Evol 9, 721–733 (2025). https://doi.org/10.1038/s41559-025-02651-5

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