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Karyotype diversity plays an important role in speciation and diversification. However, gymnosperms, particularly conifers, exhibit remarkable karyotype uniformity. To explore the evolutionary processes shaping karyotypes in gymnosperms, the karyotype evolutionary history is reconstructed through comparative genomic analyses. Synteny analysis confirms the absence of ancient polyploidy in conifers and its rarity across the gymnosperms as a whole. Further analysis reveals convergent patterns of reciprocal translocations between nonhomologous chromosomes in conifer genomes. Centromeric-centromeric reciprocal translocations (CRTs) have been identified as the primary mechanism of karyotype evolution in conifers, while telomeric-centromeric reciprocal translocations (TRTs) significantly contributed to descending dysploidy within Cupressales. A graph-based method is utilized to infer the detailed evolutionary pathways from the proto-gymnosperm karyotype (n = 12) to modern conifer karyotypes (n = 11–12). In conclusion, the scarcity of both polyploidy and dysploidy contributes to the karyotype uniformity of gymnosperms and potentially also to their lower species richness compared to angiosperms. However, the pervasive CRTs and occasional TRTs underlie this “apparent uniformity”, supporting the “karyotype orthoselection” hypothesis. This study provides new insights into the mechanisms maintaining karyotype uniformity in conifers and the role of karyotype evolution in their diversification.

Hybridization is a driving force in ecological transitions and speciation, yet direct evidence linking it to adaptive differentiation in natural systems remains limited. This study evaluates the role of hybridization in the speciation of Pinus densata, a keystone forest species on the southeastern Tibetan Plateau. By creating artificial interspecific F1s and a long-term common garden experiment on the plateau, we provide in situ assessments on 44 growth and physiological traits across four seasons, along with RNA sequencing. We found significant phenotypic divergence between P. densata and its putative parental species P. tabuliformis and P. yunnanensis, with P. densata demonstrating superior growth and dynamic balance between photosynthesis and photoprotection. The F1s closely resembled P. densata in most traits. Gene expression revealed 19%–10% of 34,000 examined genes as differentially expressed in P. densata and F1s relative to mid-parent expression values. Both additive (4%) and non-additive gene actions (5%–6% in F1s, 10%–12% in P. densata) were common, while transgressive expression occurred more frequently in the stabilized natural hybrids, illustrating transcriptomic reprogramming brought by hybridization and further divergence by natural selection. We provide compelling evidence for hybridization-derived phenotypic divergence at both physiological and gene expression levels that could have contributed to the adaptation of P. densata to high plateau habitat where both parental species have low fitness. The altered physiology and gene expression in hybrids serve both as a substrate for novel ecological adaptation and as a mechanism for the initiation of reproductive isolation.

The genetic base of local adaptation has been extensively studied in natural populations. However, a comprehensive genome-wide perspective on the contribution of structural variants (SVs) and adaptive introgression to local adaptation remains limited. In this study, we performed de novo assembly and annotation of 22 representative accessions of Quercus variabilis, identifying a total of 543,372 SVs. These SVs play crucial roles in shaping genomic structure and influencing gene expression. By analyzing range-wide genomic data, we identified both SNPs and SVs associated with local adaptation in Q. variabilis and Quercus acutissima. Notably, SV-outliers exhibit selection signals that did not overlap with SNP-outliers, indicating that SNP-based analyses may not detect the same candidate genes associated with SV-outliers. Remarkably, 29%-37% of candidate SNPs were located in a 250 kb region on chromosome 9, referred to as Chr9-ERF. This region contains 8 duplicated ethylene-responsive factor (ERF) genes, which may have contributed to local adaptation of Q. variabilis and Q. acutissima. We also found that a considerable number of candidate SNPs were shared between Q. variabilis and Q. acutissima in the Chr9-ERF region, suggesting a pattern of repeated selection. We further demonstrated that advantageous variants in this region were introgressed from western populations of Q. acutissima into Q. variabilis, providing compelling evidence that introgression facilitates local adaptation. This study offers a valuable genomic resource for future studies on oak species and highlights the importance of pan-genome analysis in understating mechanism driving adaptation and evolution.