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Study of extreme phenotypic traits and novel structures provides insights into forces mediating evolution and diversification. Sexual selection is often implicated as the evolutionary driver of trait exaggeration, while examples invoking natural selection are scarce. Heretofore overlooked examples include outlandishly exaggerated spines produced by the non-reproductive castes of various ant lineages. Ant spines are conjectured to be defensive weapons, but factors shaping their evolution are poorly understood. Here we assess the evolution, ecology and biomechanics of spine exaggeration in the hyperdiverse genus Pheidole. We suggest ant spines are novel structures among Hymenoptera. We ask how many times spinescence evolved in Pheidole, the extent to which correlations between spinescence and other morphological traits can inform our understanding of spine function and whether spinescence is associated with evolution into high-elevation habitats. We address these questions by mapping spinescence onto a 145-species phylogeny. We determined that spinescence evolved independently at least seven times in Pheidole and that all six extant spinescent lineages are restricted to the Asia-Pacific region. Our results support hypotheses proposing that elongated dorsal spines serve as defence against vertebrate predation and invertebrate attack and that task division is especially pronounced within the worker caste of spinescent species. [ABSTRACT FROM AUTHOR]