Low genetic diversity and population connectivity fuel vulnerability to climate change for the Tertiary relict pine Pinus bungeana

• Published in: Journal of systematics and evolution : JSE 2023-01, Vol.61 (1), p.143-156
• Main Authors: Guo, Jing‐Fang, Wang, Baosheng, Liu, Zhan‐Lin, Mao, Jian‐Feng, Wang, Xiao‐Ru, Zhao, Wei
• Format: Article
• Language: English
• Subjects: Adaptation; Assisted migration; Biodiversity; Chloroplast DNA; Chloroplasts; Climate; Climate change; climate relict; Endemic species; Environmental gradient; Evolution; Gene pool; Gene sequencing; Genetic diversity; Genetic drift; genomic offset; Genotyping; Geography; migration barrier; Mitochondrial DNA; Nucleotides; Pinus bungeana; Pleistocene; Pliocene; Population; population bottleneck; Population differentiation; Population genetics; Population growth; Population structure; Risk reduction; Species extinction; Threatened species
• ISSN: 1674-4918; 1759-6831; 1759-6831
• DOI: 10.1111/jse.12821

Endemic species are important components of regional biodiversity and hold the key to understanding local adaptation and evolutionary processes that shape species distributions. This study investigated the biogeographic history of a relict conifer Pinus bungeana Zucc. ex Endl. confined to central China. We examined genetic diversity in P. bungeana using genotyping‐by‐sequencing and chloroplast and mitochondrial DNA markers. We performed spatial and temporal inference of recent genetic and demographic changes, and dissected the impacts of geography and environmental gradients on population differentiation. We then projected P. bungeana's risk of decline under future climates. We found extremely low nucleotide diversity (average π 0.0014), and strong population structure (global FST 0.234) even at regional scales, reflecting long‐term isolation in small populations. The species experienced severe bottlenecks in the early Pliocene and continued to decline in the Pleistocene in the western distribution, whereas the east expanded recently. Local adaptation played a small (8%) but significant role in population diversity. Low genetic diversity in fragmented populations makes the species highly vulnerable to climate change, particularly in marginal and relict populations. We suggest that conservation efforts should focus on enhancing gene pool and population growth through assisted migration within each genetic cluster to reduce the risk of further genetic drift and extinction. Increasing variability of future climate imposes challenges for the persistence of endangered relict species. This study infers the evolutionary history and the impacts of demography and landscape factors on population structure and diversity of the red list pine Pinus bungeana. We show that drastic bottlenecks during the Pliocene and Pleistocene and long‐term isolation in fragmented habitats resulted in extremely low genetic diversity in P. bungeana, which exposes the species to high risk of decline under future climate, particularly in marginal and relict populations.