Grasping convergent evolution in syngnathids: a unique tale of tails

Abstract

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, lCTscanning 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.

Structure and mechanical properties of selected protective systems in marine organisms

“…The tail skeleton is composed of several articulating segments arranged into cross-sectional squares, each composed of four bony plates that surround a central vertebra (Fig. 17b) [147][148][149][150][151][152][153][154]. These plates are connected by overlapping joints that allow them sufficient flexibility for grasping as well as added strength for armored protection [154].…”

First live records of the ruby seadragon (Phyllopteryx dewysea, Syngnathidae)

“…The fish would often be exposed to much stronger surge, and then may well use their tails to stop from being swept off the very limited reefal habitats. A prehensile tail is found across a range of Syngnathidae and appears to have evolved at least five times from an ancestral state where the tail possessed a tail fin (Neutens et al 2014). With regards to seadragons, the phylogeny and transformation for tail shown by Neutens et al (2014) shows the leafy and common seadragon as a clade tail lacking a tail fin and without grasping capacities.…”

“…A prehensile tail is found across a range of Syngnathidae and appears to have evolved at least five times from an ancestral state where the tail possessed a tail fin (Neutens et al 2014). With regards to seadragons, the phylogeny and transformation for tail shown by Neutens et al (2014) shows the leafy and common seadragon as a clade tail lacking a tail fin and without grasping capacities. This condition was reasonably interpreted as a single loss of prehensile ability by Neutens et al (2014) since pipehorses (Solegnathus and Syngnathoides) have prehensile tails and are the closest relatives of the seadragon clade.…”

“…With regards to seadragons, the phylogeny and transformation for tail shown by Neutens et al (2014) shows the leafy and common seadragon as a clade tail lacking a tail fin and without grasping capacities. This condition was reasonably interpreted as a single loss of prehensile ability by Neutens et al (2014) since pipehorses (Solegnathus and Syngnathoides) have prehensile tails and are the closest relatives of the seadragon clade. In these pipehorses, the ability to curl the tail appears to be facilitated by a reduction of the plates, either ventrally (Solegnathus) or entirely (Syngnathoides) (Neutens et al 2014).…”

“…This condition was reasonably interpreted as a single loss of prehensile ability by Neutens et al (2014) since pipehorses (Solegnathus and Syngnathoides) have prehensile tails and are the closest relatives of the seadragon clade. In these pipehorses, the ability to curl the tail appears to be facilitated by a reduction of the plates, either ventrally (Solegnathus) or entirely (Syngnathoides) (Neutens et al 2014). The ruby seadragon holotype (Stiller et al 2015) lacks the very tip of the tail (ca.…”