Strong phylogeographic structure in major plastid lineages of East Asian Cerris oaks (Quercus subsection Campylolepides, Fagaceae): Insights from a 761-plastome analysis

In angiosperms, plastomes are typically maternally inherited and transmitted primarily through seeds, leading to limited gene flow of plastid DNA. This restriction often results in a stronger geographic structure for plastid DNA compared to nuclear DNA, especially in wind-pollinated plants with large seeds, such as oaks. However, previous studies on East Asian Cerris oaks ( Quercus subsection Campylolepides ; Q. acutissima , Q. chenii , and Q. variabilis ) found only three deep-diverging plastid lineages distributed randomly across their range, obscuring any clear phylogeographic structure. In this study, we performed a comprehensive sampling of whole plastomes to re-examine the phylogeographic pattern of East Asian Cerris oaks. Across 761 samples, we identified 163 haplotypes clustered into 15 clades, 11 of which were shared among species. The crown-group radiation of the Campylolepides core plastid clade appears to predate the formation of modern-day species, suggesting that the previously identified deep-diverging plastid lineages may reflect the retention of ancestral polymorphism. Under this interpretation, these lineages are expected to be randomly distributed across the species’ range. Within eight plastid clades occurring in more than five populations, we detected a significant phylogeographic structure. The consistent east-west differentiation observed in several widely distributed clades reflects allopatric divergence followed by localized gene exchange among sympatric species in multiple isolated refugia. Additionally, we found that different oak species co-occurring at the same site exhibited higher levels of haplotype sharing compared to those in nearby populations. The haplotypes shared within mixed-species populations displayed narrow distributions and were estimated to have originated well after the speciation events, likely due to Pleistocene plastome capture. Our findings highlight that in East Asian Cerris oaks, strong phylogeographic structure is evident primarily within major plastid clades rather than within individual species. Both shared ancestral polymorphism and historical introgression may have contributed to shaping the phylogeographic patterns of these species. • Fifteen plastid clades were identified across 761 samples of East Asian Cerris oaks. • Deep-diverging plastid lineages reflect the retention of ancestral polymorphism. • A clear phylogeographic pattern was detected within major plastid clades. • Plastome capture may explain haplotype sharing within mixed-species populations.