Grasping convergent evolution in syngnathids: a unique tale of tails

Seahorses and pipehorses both possess a prehensile tail, a unique characteristic among teleost fishes, allowing them to grasp and hold onto substrates such as sea grasses. Although studies have focused on tail grasping, the pattern of evolutionary transformations that made this possible is poorly understood. Recent phylogenetic studies show that the prehensile tail evolved independently in different syngnathid lineages, including seahorses, Haliichthys taeniophorus and several types of so-called pipehorses. This study explores the pattern that characterizes this convergent evolution towards a prehensile tail, by comparing the caudal musculoskeletal organization, as well as passive bending capacities in pipefish (representing the ancestral state), pipehorse, seahorse and H. taeniophorus. To study the complex musculoskeletal morphology, histological sectioning, μCT-scanning and phase contrast synchrotron scanning were combined with virtual 3D-reconstructions. Results suggest that the independent evolution towards tail grasping in syngnathids reflects at least two quite different strategies in which the ancestral condition of a heavy plated and rigid system became modified into a highly flexible one. Intermediate skeletal morphologies (between the ancestral condition and seahorses) could be found in the pygmy pipehorses and H. taeniophorus, which are phylogenetically closely affiliated with seahorses. This study suggests that the characteristic parallel myoseptal organization as already described in seahorse (compared with a conical organization in pipefish and pipehorse) may not be a necessity for grasping, but represents an apomorphy for seahorses, as this pattern is not found in other syngnathid species possessing a prehensile tail. One could suggest that the functionality of grasping evolved before the specialized, parallel myoseptal organization seen in seahorses. However, as the grasping system in pipehorses is a totally different one, this cannot be concluded from this study.