Extensive sharing of chloroplast haplotypes among East Asian Cerris oaks: The imprints of shared ancestral polymorphism and introgression

Abstract

Shared ancestral polymorphism and introgression are two main causes of chloroplast DNA (cpDNA) haplotype sharing among closely related angiosperms. In this study, we explored the roles of these two processes in shaping the phylogeographic patterns of East Asian Cerris oaks by examining the geographic distributions of randomly and locally distributed shared haplotypes, which coincide with the expectations of shared ancestry and introgression, respectively. We sequenced 1340 bp of non‐coding cpDNA from Quercus acutissima ( n = 418) and Q. chenii ( n = 183) and compiled previously published sequence data of Q. variabilis ( n = 439). The phylogenetic relationships among haplotypes were examined using a median‐joining network. The geographic patterns of interspecifically shared haplotypes were assessed to test whether nearby populations have a higher degree of interspecific cpDNA sharing than distant ones. We identified a total of 27 haplotypes that were grouped into three non‐species‐specific lineages with overlapping distributions. Ancestral haplotypes were extensively shared and randomly distributed across populations of the three species. Some young haplotypes were locally shared in mountainous areas that may have been shared refugia. The local exchange of cpDNA resulted in an excess of similar haplotypes between nearby populations. Our study demonstrated that the haplotype sharing pattern among East Asian Cerris oaks reflected the imprints of both shared ancestral polymorphism and introgression. This pattern was also associated with the relatively stable climates and complex landscapes in East Asia, which not only allowed the long‐term persistence of ancestral lineages but also connected the survived populations across refugia.

Niche evolution in a northern temperate tree lineage: biogeographical legacies in cork oaks (Quercus section Cerris)

“…3 ) is also supported by evidence from previous molecular studies. First, all modern Cerris share the same, section-unique plastid lineage, indicative of a single point of origin and quick dispersal, with the East Asian subsection Campylolepides showing the overall highest plastid divergence ( Simeone et al , 2018 ; Zhang et al , 2020 ; Li et al , 2022 ). Second, the Cerris plastomes are part of a haplotype lineage shared with a group of section Ilex species thriving in modern-day Japan and the mountains of northern and central China (East Asian clade in Figs 1 and 3 ; Simeone et al , 2016 : Quercus engleriana Seemen, Q. phillyreoides and Q. spinosa David; Zhou et al , 2022 : Quercus dolicholepis , Q. engleriana , Q. spinosa and Q. pseudosetulosa Q.S.Li & T.Y.Tu), i.e.…”

Ensemble species distribution modeling and multilocus phylogeography provide insight into the spatial genetic patterns and distribution dynamics of a keystone forest species, Quercus glauca

“…Genomic and anatomic data analysis indicated that oaks might have different defense mechanisms against pathogens [ 29 ]. Chloroplast DNA (cp.DNA) markers from Q. acutissima , Q. chenii , and Q. variabilis revealed haplotype sharing within section Cerris in East Asian EBLFs that was associated with locally stable climates and complex landscapes [ 30 ]. Based on SSR and phenotypic data in two oak species indicated that asymmetric inter-specific selection pressures could contribute to the asymmetric trait divergence where species coexist [ 31 ].…”

Interspecific Sharing of Closely Related Chloroplast Genome Haplotypes among Sclerophyllous Oaks in the Hot-Dry Valley of the Jinsha River, Southwestern China

“…Chloroplast (cp) DNA has been widely used to track the historical gene flow among closely related oaks [6,[17][18][19][20][21][22][23][24][25][26][27][28][29]. It is expected to be more frequently introgressed than nuclear DNA because maternally inherited cpDNA is dispersed only by seeds and thus experiences a low level of intraspecific gene flow, which would hinder the immediate dilution of introgressed genotypes [30,31].…”

“…Consequently, cpDNA variation patterns of oaks, more likely reflecting the imprints of localized interspecific gene flow, are largely influenced by geography rather than by taxonomy [31,32]. Previous studies have shown that interspecific sharing of geographically restricted cpDNA haplotypes occurred within section Quercus [18][19][20][21], section Lobatea [22], section Virentes [23], section Cerris [6,[24][25][26], section Ilex [6,[27][28][29], and section Cyclobalanopsis [29]. Chloroplast capture events between sections were rare but also reported for sections Quercus and Ponticae, sections Quercus and Virentes, and sections Quercus and Protobalanus [17,32], probably tracking the history of ancient introgression between ancestral populations of oaks.…”

“…Chloroplast capture events between sections were rare but also reported for sections Quercus and Ponticae, sections Quercus and Virentes, and sections Quercus and Protobalanus [17,32], probably tracking the history of ancient introgression between ancestral populations of oaks. Other processes, like the retention of ancestral polymorphism, may also result in the interspecific sharing of cpDNA haplotypes, but those shared ancestral haplotypes are expected to be randomly and widely distributed across the ranges of the descendant species [26].…”