J Integr Plant Biol. ›› 2023, Vol. 65 ›› Issue (5): 1183-1203.DOI: 10.1111/jipb.13466

• Molecular Ecology and Evolution • Previous Articles     Next Articles

Climate‐influenced boreotropical survival and rampant introgressions explain the thriving of New World grapes in the north temperate zone

Ze‐Long Nie1, Richard Hodel2, Zhi‐Yao Ma2,3, Gabriel Johnson2, Chen Ren4, Ying Meng1, Stefanie M. Ickert‐Bond5,6, Xiu‐Qun Liu7, Elizabeth Zimmer2 and Jun Wen2*   

  1. 1. College of Biology and Environmental Sciences, Jishou University, Jishou 416000, China;
    2. Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA;
    3. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, China;
    4. Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China;
    5. Herbarium (ALA), University of Alaska Museum of the North, University of Alaska Fairbanks, Fairbanks, AK 99775, USA;
    6. Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK 99775, USA;
    7. Key Laboratory of Horticultural Plant Biology, College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan 430070, China
    *Correspondence Jun Wen (wenj@si.edu)
  • Received:2022-07-28 Accepted:2023-02-08 Online:2023-03-24 Published:2023-05-01

Abstract: The north temperate region was characterized by a warm climate and a rich thermophilic flora before the Eocene, but early diversifications of the temperate biome under global climate change and biome shift remain uncertain. Moreover, it is becoming clear that hybridization/introgression is an important driving force of speciation in plant diversity. Here, we applied analyses from biogeography and phylogenetic networks to account for both introgression and incomplete lineage sorting based on genomic data from the New World Vitis, a charismatic component of the temperate North American flora with known and suspected gene flow among species. Biogeographic inference and fossil evidence suggest that the grapes were widely distributed from North America to Europe during the Paleocene to the Eocene, followed by widespread extinction and survival of relicts in the tropical New World. During the climate warming in the early Miocene, a Vitis ancestor migrated northward from the refugia with subsequent diversification in the North American region. We found strong evidence for widespread incongruence and reticulate evolution among nuclear genes within both recent and ancient lineages of the New World Vitis. Furthermore, the organellar genomes showed strong conflicts with the inferred species tree from the nuclear genomes. Our phylogenomic analyses provided an important assessment of the wide occurrence of reticulate introgression in the New World Vitis, which potentially represents one of the most important mechanisms for the diversification of Vitis species in temperate North America and even the entire temperate Northern Hemisphere. The scenario we report here may be a common model of temperate diversification of flowering plants adapted to the global climate cooling and fluctuation in the Neogene.

Key words: boreotropical refugia, introgression, New World grapes, phylogenomics, temperate diversification

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