Causes of delayed angiosperm diversification: The photosynthetic revolution, increased opportunity costs of anti-herbivore defenses, selection for qualitative toxins, and acceleration of plant-herbivore coevolution.

Why did it take so long for angiosperms to diversify after they arose? Here I consider the indirect but potentially crucial impact of the "photosynthetic revolution" on plant-herbivore coevolution. Increased vein density in fossil leaves implies a doubling in photosynthesis 125-100 million years ago. Higher photosynthetic rates increase the opportunity cost of anti-herbivore defenses, favoring shifts to chemically diverse, low-cost, low-molecular-weight qualitative toxins (e.g., alkaloids) from chemically stereotyped, high-cost, high-molecular-weight quantitative toxins (e.g., tannins). Given the greater functional significance of incremental changes in defensive compounds of lower molecular weight, shifts to qualitative toxins should accelerate plant-herbivore coevolution and species diversification. The large genome and cell sizes of ferns and gymnosperms should drive lower rates of coevolutionary diversification by decreasing vein density and photosynthetic rates; high vein density found in many euasterids, eurosids, and monocots should drive higher diversification rates. This theory might also explain the general restriction of qualitative toxins to herbaceous plants, given the higher photosynthetic rates of herbs vs. woody plants. Lower hydraulic limitation and selection for small genomes in short, fast-growing, short-lived plants should foster evolution of small cells, fine vein networks, high leaf N levels and photosynthetic rates, reliance on qualitative toxins, and high speciation rates.