Patterns of genomic divergence in sympatric and allopatric speciation of three Mihoutao (Actinidia) species

Abstract

Isolation by geographic distance involves in the formation of potential genomic islands and the divergence of genomes, which often result in speciation. The mechanisms of sympatric and allopatric speciation associated with geographic distance remain a topic of interest to evolutionary biologists. Here we examined genomic divergence in three Actinidia species from large-scale sympatric and allopatric regions. Genome sequence data revealed that hexaploid A. deliciosa originated from A. chinensis, and supported the speciation-with-gene-flow model in sympatric regions. The common ancestor of A. setosa and A. deliciosa migrated from the mainland to the Taiwan Island ~2.91 Mya and formed A. setosa ~ 0.92 Mya, and the speciation of A. setosa is consistent with the divergence-after-speciation model with selective sweeps. Geographic isolation resulted in population contraction and accelerated the process of lineage sorting and speciation due to natural selection. Genomic islands contained genes associated with organ development, local adaptation, and stress resistance, indicating selective sweeps on a specific set of traits. Our results highlight the patterns of genomic divergence in sympatric and allopatric speciation, with the mediation of geographic isolation in the formation of genomic islands during Actinidia speciation.

Chromosome‐level genome of putative autohexaploid Actinidia deliciosa provides insights into polyploidisation and evolution

“…Polyploidisation can promote the ability of polyploid plants to adapt to stressful conditions including temperature and water stress (Van de Peer et al., 2021); compared to diploid A. chinensis , hexaploid A. deliciosa grows at high altitudes and is adapted to cold temperatures (Song et al., 2020). Expanded genes were enriched in trichome differentiation (GO: 0090376) and elongation (GO: 0090378) (Table S12); trichome traits are associated with cold tolerance (Liu, Yu, et al., 2022). The gene families unique to A. deliciosa included 73 genes involved in flavone and flavonol biosynthesis (Figure S8, Table S14), a process that is also associated with cold‐tolerance (Kim, Warpeha, et al., 2019).…”

“…chinensis and A. deliciosa (Liu et al., 2010), and tetraploid A . chinensis and tetraploid A. deliciosa are often observed together in nature (Li et al., 2010; Liu, Yu, et al., 2022). The coexistence of cytotypes (2 x and 4 x , 4 x and 6 x and 4 x , 5 x and 6 x ) is prevalent for the expanded A. chinensis Planchon complex in nature (Li et al., 2010), indicating the complexity of this system.…”

“…In addition, A. setosa seems a possible candidate parent of the hexaploid because of its close phylogenetic relationship and similar nucleotide diversity to A. deliciosa . The common ancestor of A. deliciosa and A. setosa diverged from A. chinensis at ~10.1 mya (Liu, Yu, et al., 2022), which occurred after Ad‐α event (~18.4–22.3 mya) for all the species examined of Actinidia . Although our genomic analyses have been insightful, the formation and ancestry of hexaploid A. deliciosa are still unclear and require more genomic evidence (e.g.…”

“…Compared to diploid A. chinensis , natural hexaploid A. deliciosa is distributed at higher altitudes in western China and is adapted to colder environments (Huang, 2014). The success of the hexaploid A. deliciosa was presumably related to the cold temperatures during the last glacial maximum (1.9–2.65 mya); the trichome traits of hexaploid A. deliciosa were likely involved in adaptation to cold temperatures (Liu, Yu, et al., 2022). We found that genes involved in the biosynthesis of plant hormones and defence against biotic and abiotic stimuli showed high expression in plant tissues; such genes are likely involved in the cold tolerance of A. deliciosa at high altitudes (Li et al., 2019).…”

“…We sampled the three Actinidia species from five regions, two hexaploid A. deliciosa populations in Sichuan (ZLC) and Hubei (JZP), two diploid A. chinensis populations in Henan (TPZ) and Zhejiang (YMC) and one diploid A. setosa population in Taiwan island (TWI) (Table S18) (Liu, Yu, et al., 2022; Yu et al., 2020). The ploidy of individual plants was determined by flow cytometry at 1–2 days after leaf collection (Phivnil et al., 2005).…”