Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

The impact of key traits on lineage diversity remains a central focus in macroevolutionary research. Seeds, encapsulated within fruits, carry the complete genetic blueprint of their species, and their adaptive evolution to diverse environmental conditions shapes species origination and extinction dynamics. However, the role of specific traits in driving species diversification under changing environmental conditions remains poorly understood, particularly among taxa that produce desiccation-sensitive seeds. In this study, we reconstructed the phylogenetic relationships of Quercus section Cyclobalanopsis based on whole-genome resequencing data from 52 species, covering approximately 50% of the section. We investigated six fruit traits—fruit volume, shape, maturation period, cotyledonary petiole, embryonic axis position and dormancy type—through experimental observations and data collection. Using a synthetic analytical approach, we integrated these traits with climatic variables, phylogenetic data, and their combined influence on diversification rates. Our findings reveal substantial diversity in fruit trait states within Cyclobalanopsis . Climates characterized by hot summers and wet, cold winters provide favorable habitat conditions that promote speciation. Furthermore, ancestral fruit traits, such as small acorns, oblong ellipsoid shapes, normal cotyledonary petioles, and embryonic axes near the apex, along with the derived trait of annual fruit maturation, were associated with increased net diversification rates. These ancestral fruit traits, adapted to the subtropical evergreen broad-leaved forests of East Asia, facilitated rapid evolutionary radiation during the Miocene through climatic niche innovation. In contrast, species inhabiting tropical landscapes appear to adapt to local environmental changes through fruit trait innovations, such as larger fruits and rapid germination. • The East Asian subtropical monsoon climate with high temperature seasonality and high precipitation increases the speciation rate in Quercus section Cyclobalanopsis. • Variations in diversification rates within section Cyclobalanopsis are primarily driven by climatic niche innovation and the evolution of seed traits since the Miocene. • The East Asian subtropical monsoon drove the evolution of several ancestral acorn traits, thereby accelerating species diversification. Meanwhile, the South Asian tropical monsoon facilitated localized coevolutionary dynamics of acorn traits.