The complex interaction between mammalian herbivores, climate, soil and fire has shaped the evolution and distribution of plant spinescence across biogeographical realms

The evolutionary arms race between plants and herbivores led to numerous plant adaptations, including spinescence. However, the balance between herbivory and abiotic conditions in the evolution of spinescence remains unclear. We integrated phylogenetic, geographic, and trait data for 2686 species of an ecologically diverse and spinescent pantropical lineage, mimosoid legumes, with distribution data on 368 extant and extinct mammalian herbivores ≥ 10 kg. Using structural equation models, we assessed how herbivores, climate, soil, and fire directly and indirectly affected the proportion of spinescent mimosoids across global and continental assemblages. Models incorporating extinct herbivore assemblages explained more variation in the proportion of spiny species than those based solely on extant herbivores. Dry-season length and soil pH increased spinescence both directly and indirectly through their effects on herbivore richness. These abiotic effects exceeded herbivore effects at continental scales. Fire influenced spinescence only indirectly via its positive relationship with herbivore richness. Finally, spinescence evolved repeatedly across mimosoids from c. 35 million years ago, pre-dating the Miocene savanna expansion. Our study suggests that past herbivore communities have left a lasting imprint on present-day plant defence patterns and that long-term climatic transitions and the emergence of open, herbivore-rich landscapes played crucial roles in the evolution and distribution of spinescence.