Efficient purging of deleterious mutations contributes to the survival of a rare conifer

Abstract

Cupressaceae is a conifer family rich in plants of horticultural importance, including Cupressus, Chamaecyparis, Juniperus, and Thuja, yet genomic surveys are lacking for this family. Cupressus gigantea, one of the many rare conifers that are threatened by climate change and anthropogenic habitat fragmentation, plays an ever-increasing role in ecotourism in Tibet. To infer how past climate change has shaped the population evolution of this species, we generated a de novo chromosome-scale genome (10.92 Gb) and compared the species’ population history and genetic load with that of a widespread close relative, C. duclouxiana. Our demographic analyses, based on 83 re-sequenced individuals from multiple populations of the two species, revealed a sharp decline of population sizes during the first part of the Quaternary. However, populations of C. duclouxiana then started to recover, while C. gigantea populations continued to decrease until recently. The total genomic diversity of C. gigantea is smaller than that of C. duclouxiana, but contrary to expectations, C. gigantea has fewer highly and mildly deleterious mutations than C. duclouxiana, and simulations and statistical tests support purifying selection during prolonged inbreeding as the explanation. Our results highlight the evolutionary consequences of decreased population size on the genetic burden of a long-lived endangered conifer with large genome size and suggest that genetic purging deserves more attention in conservation management.

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant/Award Number U20A2080), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (Grant/Award Number 2019QZKK05020110), the Sichuan Science and Technology Program (Grant/Award Number 2023NSFSC0186), the Fundamental Research Funds for the Central Universities of Sichuan University (Grant/Award Numbers SCU2021D006 and SCU2022D003), and the Institutional Research Fund from Sichuan University (2021SCUNL102). We thank Ruth Shaw for constructive comments and Aurora García-Dorado for providing a script to predict derived deleterious mutations.

Author contributions

K.M. and J.Liu designed the research, J.Li, Y.W., J.Luo, H.Y., S.T., and T.J. conducted field surveys and collected samples, Y.W., Y.Y., Z.H., J.Li, J.K., D.W., and S.W. performed data analyses, Y.W., Y.Y., Z.H., J.Luo, and K.M. wrote the draft, all authors read and revised the manuscript, and S.S.R., Y.W., K.M., and J.Liu finalized the manuscript.

Data availability

The C. gigantea genome sequences and newly generated whole-genome sequencing data of the samples produced in this study have been deposited in the National Genomics Data Center (NGDC) with the accession numbers GWHDOOJ00000000 and CRA009774, respectively. The annotation gff3 file has been deposited in Figshare (https://figshare.com/articles/dataset/Cupressus_gigantea_genome_annotation/25264894).

Code availability

The code used in this study is available at https://github.com/Wennie-s/Tibetan-cypress-population-genomics.

Conflict of interest

The authors declare no competing interests.

Supplementary data

Supplementary data are available at Horticulture Research online.

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