Genome sequences and population genomics reveal climatic adaptation and genomic divergence between two closely related sweetgum species

SUMMARY Understanding the genetic basis of population divergence and adaptation is an important goal in population genetics and evolutionary biology. However, the relative roles of demographic history, gene flow, and/or selective regime in driving genomic divergence, climatic adaptation, and speciat...

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Published in:The Plant journal : for cell and molecular biology 2024-06, Vol.118 (5), p.1372-1387
Main Authors: Xu, Wu‐Qin, Ren, Chao‐Qian, Zhang, Xin‐Yi, Comes, Hans‐Peter, Liu, Xin‐Hong, Li, Yin‐Gang, Kettle, Christopher J., Jalonen, Riina, Gaisberger, Hannes, Ma, Ya‐Zhen, Qiu, Ying‐Xiong
Format: Article
Language:English
Subjects:
Adaptation
Adaptation, Physiological - genetics
Biological evolution
Breeding
China
Climate
Climate adaptation
Climate change
climatic adaptation
demographic modeling
Demographics
Demography
Developmental biology
Divergence
divergent selection
Flora
Gene Flow
Gene sequencing
Genetic Speciation
Genetic Variation
Genetics
Genetics, Population
Genome, Plant - genetics
Genomes
Genomic islands
Genomics
Holocene
Hybridization
Liquidambar
Miocene
Phylogeny
Plant species
Population genetics
population genomics
Quaternary
Recombination
Reproductive Isolation
Sibling species
Speciation
sweetgum
Sympatric populations
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Summary:SUMMARY Understanding the genetic basis of population divergence and adaptation is an important goal in population genetics and evolutionary biology. However, the relative roles of demographic history, gene flow, and/or selective regime in driving genomic divergence, climatic adaptation, and speciation in non‐model tree species are not yet fully understood. To address this issue, we generated whole‐genome resequencing data of Liquidambar formosana and L. acalycina, which are broadly sympatric but altitudinally segregated in the Tertiary relict forests of subtropical China. We integrated genomic and environmental data to investigate the demographic history, genomic divergence, and climatic adaptation of these two sister species. We inferred a scenario of allopatric species divergence during the late Miocene, followed by secondary contact during the Holocene. We identified multiple genomic islands of elevated divergence that mainly evolved through divergence hitchhiking and recombination rate variation, likely fostered by long‐term refugial isolation and recent differential introgression in low‐recombination genomic regions. We also found some candidate genes with divergent selection signatures potentially involved in climatic adaptation and reproductive isolation. Our results contribute to a better understanding of how late Tertiary/Quaternary climatic change influenced speciation, genomic divergence, climatic adaptation, and introgressive hybridization in East Asia's Tertiary relict flora. In addition, they should facilitate future evolutionary, conservation genomics, and molecular breeding studies in Liquidambar, a genus of important medicinal and ornamental values. Significance Statement We assembled a chromosome‐scale genome of Liquidambar formosana and resequenced 160 individuals of L. formosana and its high‐altitude sister species L. acalycina. Benefiting from advanced analytical methods and robust evidence, we found that multiple “genomic islands” mainly evolved as a result of divergence hitchhiking and recombination rate variation, as likely fostered by long‐term refugial isolation and recent differential introgression in low‐recombination genomic regions; and identified some candidate genes associated with climatic adaptation and reproductive isolation.
ISSN:0960-7412
1365-313X
DOI:10.1111/tpj.16675