The Evolution of Siphonophore Tentilla as Specialized Tools for Prey Capture

Predator specialization has often been considered an evolutionary dead-end due to the constraints associated with the evolution of morphological and functional optimizations throughout the organism. However, in some predators, these changes are localized in separate structures dedicated to prey capture. One of the most extreme cases of this modularity can be observed in siphonophores, a clade of pelagic colonial cnidarians that use tentilla (tentacle side branches armed with nematocysts) exclusively for prey capture. Here we study how siphonophore specialists and generalists evolve, and what morphological changes are associated with these transitions. To answer these questions, we: (1) measured 29 morphological characters of tentacles from 45 siphonophore species, (2) mapped these data to a phylogenetic tree, and (3) analyzed the evolutionary associations between morphological characters and prey type data from the literature. Instead of a dead-end, we found that siphonophore specialists can evolve into generalists, and that specialists on one prey type have directly evolved into specialists on other prey types. Our results show that siphonophore tentillum morphology has strong evolutionary associations with prey type, and suggest that shifts between prey types are linked to shifts in the morphology, mode of evolution, and genetic correlations of tentilla and their nematocysts. The evolutionary history of siphonophore specialization helps build a broader perspective on predatory niche diversification via morphological innovation and evolution. These findings contribute to understanding how specialization and morphological evolution have shaped present-day food webs. Significance StatementPredatory specialization is often associated with the evolution of modifications in the morphology of the prey capture apparatus. Specialization has been considered an evolutionary dead-end due to the constraints associated with these morphological changes. However, in predators like siphonophores, armed with modular structures used exclusively for prey capture, this assumption is challenged. Our results show that siphonophores can evolve generalism and new prey-type specializations by modifying the morphological states, modes of evolution, and genetic correlations between the parts of their prey capture apparatus. These findings demonstrate how studying open-ocean non-bilaterian predators can reveal novel patterns and mechanisms in the evolution of specialization. Understanding these evolutionary processes is fundamental to the study of food-web structure and complexity.