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

Abstract

Evergreen sclerophyllous oak forests (ESOFs) in southwestern China are a special vegetation type developed in response to the expansion of arid habitats after the uplift of the Himalayas. Here, we used chloroplast (cp) DNA and nuclear ribosomal (nr) DNA to investigate the fine-scale genetic variation patterns of six sympatric oaks (Quercus, Fagaceae) in the hot-dry valley ESOFs of the Jinsha River, southwestern China. Three cp genomes were assembled for each species. Nine cp genome haplotypes and 16 nrDNA haplotypes were identified based on single-nucleotide variants and indels. Our results demonstrated that discordance existed between the cpDNA and nrDNA phylogenies of the sclerophyllous oaks in section Ilex. The nrDNA phylogeny was consistent with species boundaries, while the cpDNA phylogeny was decoupled from taxonomy. Interspecific sharing of closely related cp genome haplotypes was detected between Quercus cocciferoides and the other two sclerophyllous oaks, Q. longispica and Q. franchetii. Specifically, Q. cocciferoides and Q. longispica sampled in a mixed stand exhibited two haplotypes that differed by a 9 bp indel. The local distribution of the two highly similar haplotypes suggested that they may have arisen from ancient introgression. Given that the two species have diverged for a long time, it is possible that the ancestral cp genome of one species was captured by another species through asymmetric introgression in early times, and an indel event occurred subsequently. Phylogenetic analyses using more previously published cp genome sequences indicated that Q. cocciferoides and Q. franchetii shared multiple cpDNA lineages of Ilex oaks, which may be caused by shared ancestral polymorphism and/or ancient introgression. Our study showed that at least three highly variable regions (ψycf1, ndhF-rpl32, and trnKUUU-rps16 or rpl32-trnLUAG) can distinguish the nine haplotypes identified by whole-cp genome sequences. These markers are useful for the evolutionary studies of the maternal lineages of oaks in hot-dry valley ESOFs.