Céline Neutens

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.

Prehensile and non-prehensile tails among syngnathid fishes: what’s the difference?

All syngnathid fishes are characterized by a tail with a vertebral column that is surrounded by dermal Plates - four per vertebra. Seahorses and pipehorses have prehensile tails, a unique characteristic among teleosts that allows them to grasp and hold onto substrates. Pipefishes, in contrast, possess a more rigid tail. Previous research (Neutens et al., 2014) showed a wide range of variation within the skeletal morphology of different members in the syngnathid family. The goal of this study is to explore whether the diversity in the three-dimensional (3D) shape of different tail types reflects grasping performance, and to what degree grasping tails occupy a different and more constrained diversity. For this, a 3D morphometrical analysis based on surfaces was performed. Four different analyses were performed on the tail skeleton of nine species exhibiting different levels of tail grasping capacities (four pipehorse, three seahorse, one pipefish and one seadragon species) to examine the intra-individual variation across the anteroposterior and dorso-ventral axis. In the two interspecific analyses, all vertebrae and all dermal plates were mutually compared. Overall, intra-individual variation was larger in species with a prehensile tail. The analysis on the vertebrae showed differences in the length and orientation of the hemal spine as well as the inclination angle between the anterior and posterior surface of the vertebral body. This was observed at an intra-individual level across the anteroposterior axis in prehensile species and at an inter-individual level between prehensile and non-prehensile species. Across the anteroposterior axis in prehensile tails, the overall shape of the plates changes from rectangular at the anterior end to square at the posterior end. Across the dorso-ventral axis, the ventral dermal plates carry a significantly longer caudal spine than the dorsal ones in all prehensile-tailed species. It can therefore be concluded that prehensile tails exhibit a larger anteroposterior and dorso-ventral shape variation than non-prehensile ones. However, the hypothesis that there is a more constrained shape variation among prehensile species compared to non-prehensile ones had to be rejected.