Genomic analysis of xerophyte Salweenia species provides insights into the alpine dry–warm valleys divergence and survival history

Salweenia species are evergreen shrubs capable of preventing desertification and maintaining the health of alpine dry-warm ecosystems in the Hengduan Mountains. However, both the narrowly distributed S. bouffordiana and its more widespread close relative S. wardii are endemic and endangered. Furthermore, their small population sizes render each of these species at risk of extinction. To infer how past climate changes have shaped the evolutionary history of these species, we developed a chromosome-level S. bouffordiana genome (788 Mb) and compared the two species' evolutionary histories, genetic loads and the genomic adaptions to local environmental conditions using whole-genome resequencing data. Our findings reveal a sharp population decline from the Pliocene to the Quaternary. However, populations of S. bouffordiana then started to recover before declining further, while S. wardii populations continued to decline until recently. Abundant homozygous-derived variants accumulated in the two species, particularly in S. bouffordiana, while the species with the most heterozygous variants was S. wardii. Accumulated extensive inbreeding effects but possessed few LOF mutations and few highly deleterious variants in the S. bouffordiana that have experienced the most severe demographic bottlenecks, most likely because of purging effects. This accelerating decline cascade will likely be detrimental to the consequences for the species' future viability and adaptive potential. Overall, this study improves our understanding of the evolutionary history of Salweenia shrubs tolerant to extreme environments and offers a genetic resource for future breeding and conservation efforts.