Distinct constraints but shared dynamics shape the macroevolution of volatile organic compound chemodiversity.

Complex metabolic systems have evolved across the tree of life, producing remarkable chemodiversity, yet the structure and evolutionary modes underlying this diversity remain poorly understood. Here, we investigate the macroevolution of chemodiversity using a comprehensive dataset of gymnosperm foliage volatile organic compounds (VOCs) collected from the literature. We find that chemodiversity is dominated by a small fraction of "core" compounds. Although few in number, these core VOCs are widespread and abundant. To understand the full picture, we investigate the macroevolution of both high-dimensional global chemodiversity, and the dominant core chemodiversity. We find that both global and core chemodiversity have evolved through similar dynamics: punctuated evolution rather than gradual drift. We also identify a dichotomy in constraint, where global chemodiversity exhibits weak covariance-reflecting high evolutionary lability-and the core chemodiversity is characterized by high covariance and strong integration. We perform ancestral state reconstruction and find that this complex system is not a recent innovation; the major, core VOCs were already established in ancestral lineages prior to the Carboniferous period. These findings not only reveal the hierarchical structure of the gymnosperm VOC system, with its underlying constraints and dynamics, but also provide a framework for exploring the structure and evolutionary dynamics of chemodiversity.