Dimorphism throughout the European eel's life cycle: are ontogenetic changes in head shape related to dietary differences?

A well-known link exists between an organism's ecology and morphology. In the European eel, a dimorphic head has been linked to differences in feeding ecology, with broad-headed eels consuming harder prey items than narrow-headed ones. Consequently, we hypothesized that broad-heads should exhibit a cranial musculoskeletal system that increases bite force and facilitates the consumption of harder prey. Using 3D-reconstructions and a bite model, we tested this hypothesis in two life stages: the sub-adult yellow eel stage and its predecessor, the elver eel stage. This allowed us to test whether broad- and narrow-headed phenotypes show similar trait differences in both life stages and whether the dimorphism becomes more pronounced during ontogeny. We show that broad-headed eels in both stages have larger jaw muscles and a taller coronoid, which are associated with higher bite forces. This increased bite force together with the elongated upper and lower jaws in broad-headed eels can also improve grip during spinning behavior, which is used to manipulate hard prey. Head shape variation in European eel is therefore associated with musculoskeletal variation that can be linked to feeding ecology. However, although differences in muscle volume become more pronounced during ontogeny, this was not the case for skeletal features.

Broader head, stronger bite: In vivo bite forces in European eel Anguilla anguilla.

This work examined three different phenotypes of the yellow-eel stage of the European eel Anguilla anguilla, broad-heads, narrow-heads and eels with an intermediate head shape. The aim was to see whether broad-headed A. anguilla, which generally consume harder, larger prey, such as crustaceans and fish, exerted greater bite force than the narrow-headed variant, which mainly consume soft, small prey such as chironomid larvae. It was found that in 99 yellow A. anguilla, in vivo bite force of broad-heads are higher compared with narrow-heads and intermediates.

Ontogenesis of opercular deformities in gilthead sea bream Sparus aurata: a histological description.

The aim of this study was to characterize histological changes during opercular osteogenesis in farmed gilthead sea bream Sparus aurata larvae from 7 to 69 days post hatching (dph) and compare normal osteogenesis with that of deformed opercles. Mild opercular deformities were first detected in 19 dph larvae by folding of the opercle's distal edge into the gill chamber. Here, the variation in the phenotype and the irregular bone structure at the curled part of the opercles is described and compared with the histology of normal opercles. Results indicated that deformed opercles still undergo bone growth with the addition of new matrix by osteoblasts at the opercular surface, especially at its edges. No significant difference was found in bone thickness between deformed and normal opercles. In addition to differences in bone architecture, differences in collagen fibre thickness between normal and deformed opercles were also found.

Differential gene expression in narrow- and broad-headed European glass eels (Anguilla anguilla) points to a transcriptomic link of head shape dimorphism with growth rate and chemotaxis.

One of the major challenges in evolutionary biology is to understand the mechanisms underlying morphological dimorphism and plasticity, including the genomic basis of traits and links to ecology. At the yellow eel stage of the European eel (Anguilla anguilla), two morphotypes are found: broad- and narrow-heads. This dimorphism has been linked to dietary differences, with broad-heads feeding on harder, larger prey than narrow-heads. However, recent research showed that both morphotypes could be distinguished at the glass eel stage, the nonfeeding predecessor of the yellow eel stage, implying that nondietary factors play a role in the development of this head shape dimorphism. Here, we used transcriptome profiling (RNAseq) to identify differentially expressed genes between broad- and narrow-headed glass eels. We found 260 significantly differentially expressed genes between the morphotypes, of which most were related to defence and immune responses. Interestingly, two genes involved in growth (soma and igf2) were significantly upregulated in narrow-heads, while nine genes involved in chemotaxis showed significant differential expression. Thus, we found support for the observation that head shape is associated with somatic growth, with fast-growing eels developing a narrower head. Additionally, observations in the wild have shown that slow-growers prefer freshwater, while fast-growers prefer brackish water. The differential expression of genes involved in chemotaxis seems to indicate that glass eel growth rate and habitat choice are linked. We hypothesize that two levels of segregation could take place in the European eel: first according to habitat choice and second according to feeding preference.

Saddleback syndrome in European sea bass Dicentrarchus labrax (Linnaeus, 1758): anatomy, ontogeny and correlation with lateral-line, anal and pelvic fin abnormalities.

This study focused on the anatomy and ontogeny of saddleback syndrome (SBS) in reared European sea bass. The abnormality was detected at an unusually high frequency (12-94%) during a routine quality control in a commercial hatchery. Anatomically the abnormality was mainly characterized by the loss of 1-5 hard spines and severe abnormalities of the proximal pterygiophores (anterior dorsal fin), size reduction of a few lepidotrichia, missing lepidotrichia and/or lepidotrichia of poor ossification (posterior dorsal fin). SBS was significantly correlated with abnormalities of the anal and pelvic fins in all the examined populations. Moreover, in juvenile fish, SBS was significantly correlated with an abnormal lack of sectors of the lateral line. The examination of early larval samples revealed that SBS was ontogenetically associated with severe abnormalities of the primordial marginal finfold, which developed at the flexion stage (ca 8.5-11.0 mm SL). Histologically, these abnormalities were associated with extensive epidermal erosion. The results are discussed in respect of the critical ontogenetic period and the possible causative factors of SBS in European sea bass. It is suggested that causative factors acted during a wide ontogenetic period including flexion and metamorphosis phases.

Head shape dimorphism in European glass eels (Anguilla anguilla).

The life cycle of the European eel (Anguilla anguilla) remained a mystery until the 20th century, when Schmidt discovered that the Sargasso Sea was its spawning area. However, many aspects of the eel's life cycle remain poorly understood. Among these is the bimodal distribution in head shape, with broad- and narrowheaded phenotypes reported in the yellow eel stage. Although this has been linked to dietary preferences of the yellow eels, very little is known about why, how and when this dimorphism arises during their ontogeny. To determine whether this dimorphism indeed appears in relation to trophic niche segregation, we examined head shape variation at an earlier ontogenetic stage, the glass eel stage, as at this stage eels are considered to be non-feeding. Head shape was studied in a large dataset, containing glass eels captured from the Yser river mouth, the Leopold Canal (Belgium) and from the rivers Severn, Trent and Parret (UK), by both taking measurements (head width/head length) and using an outline analysis. Our results show that there is already considerable variation in broadness and bluntness of the head at the glass eel stage. In most cases, equal support for a unimodal and bimodal head shape distribution is found, whereas some cases support head shape bimodality in glass eels, suggesting that glass eel head shape might be shifting from a unimodal to a bimodal distribution. This, in combination with the observation that variation in head width/head length ratios in non-feeding glass eels shows a similar range as in feeding yellow eels, indicates that head shape in European eel might be at least partially determined through other mechanisms than trophic segregation.

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.

Protocol for quantitative shape analysis of deformities in early larval European seabass Dicentrarchus labrax.

This study established an optimized protocol for quantifying the shape variation of newly hatched larvae of European seabass Dicentrarchus labrax, focusing on the effect of fixatives and mounting on body shape from hatching until 14 days post hatching, while also minimizing the error introduced by handling. This assessment was performed based on both biometric and geometric shape data, with the latter relying on outline based elliptic Fourier analysis. The fixation and mounting effect on the total length and shape of newly hatched larvae of D. labrax was tested for four fixation treatments: (1) 8% formalin, (2) 70% ethanol, (3) 8% formalin for 48 h and then to 70% ethanol and (4) 3% phosphate-buffered glutaraldehyde. The analyses showed that no significant size and shape effect was observed on anaesthetized specimens 5 months post-fixation in glutaraldehyde, and that the glycerol mounting process of specimens fixed in glutaraldehyde provided the best results for further ontogenetic qualitative and quantitative analysis. The protocol proved to be sufficiently sensitive to even quantify and visualize subtle pre-fixation shape differences originating from a different egg batch.

Regional variation in morphology of vertebral centra and intervertebral joints in striped bass, Morone saxatilis.

The vertebral column of fishes has traditionally been divided into just two distinct regions, abdominal and caudal. Recently, however, developmental, morphological, and mechanical investigations have brought this traditional regionalization scheme into question. Alternative regionalization schema advocate the division of the abdominal vertebrae into cervical, abdominal, and in some cases, transitional regions. Here, we investigate regional variation at the level of the vertebrae and intervertebral joint (IVJ) tissues in the striped bass, Morone saxatilis. We use gross dissection, histology, and polarized light imaging to quantify vertebral height, width, length, IVJ length, IVJ tissue volume and cross-sectional area, and vertical septum fiber populations, and angles of insertion. Our results reveal regional differences between the first four (most rostral) abdominal vertebrae and IVJs and the next six abdominal vertebrae and IVJs, supporting the recognition of a distinct cervical region. We found significant variation in vertebral length, width, and height from cranial to caudal. In addition, we see a significant decline in the volume of notochordal cells and the cross-sectional area of the fibrous sheath from cranial to caudal. Further, polarized light imaging revealed four distinct fiber populations within the vertical septum in the cervical and abdominal regions in contrast with just one fiber population found in the caudal region. Measurement of the insertion angles of these fiber populations revealed significant differences between the cervical and abdominal regions. Differences in vertebral, IVJ, and vertical septum morphology all predict greater range of motion and decreased stiffness in the caudal region of the fish compared with the cervical and abdominal regions.

Why the long face? A comparative study of feeding kinematics of two pipefishes with different snout lengths.

This study showed that the mouth of Doryrhamphus dactyliophorus, a species with a relatively long snout, travels a greater distance compared with Doryrhamphus melanopleura, a species with a considerably shorter snout, allowing it to strike at prey that are farther away from the mouth. The long-snouted species also tended to reach significantly higher linear velocities of the mouth approaching the prey. On the other hand, D. melanopleura needed less time to capture its prey. A striking difference in prey-capture success was observed between species: D. melanopleura and D. dactyliophorus had a prey-capture success of 91 and 31%, respectively. The small prey size and the relatively large distance between eyes and prey are potential reasons why directing the mouth accurately to the prey is difficult in D. dactyliophorus, hence possibly explaining the lower prey-capture success in this long-snouted species.

Musculoskeletal structure of the feeding system and implications of snout elongation in Hippocampus reidi and Dunckerocampus dactyliophorus.

A thorough morphological description of the feeding apparatus in Hippocampus reidi, a long-snouted seahorse, and Dunckerocampus dactyliophorus, an extremely long-snouted pipefish, revealed specialized features that might be associated with the fast and powerful suction feeding, like the two ligamentous connections between the lower jaw and the hyoid, the saddle joint of the latter with the suspensorium and the vertebro-pectoral fusion that articulates on three points with the cranium. Despite the conserved morphology of the feeding apparatus, it was found that in H. reidi the orientation of the occipital joint is ventrocaudal, the sternohyoideus and epaxial muscles are more bulky and both have a short tendon. In D. dactyliophorus, on the other hand, the protractor hyoidei muscle is enclosed by the mandibulo-hyoid ligament, the sternohyoideus and epaxial tendons are long and a sesamoid bone is present in the latter. These features were compared to other syngnathid species with different snout lengths to evaluate the implications of snout elongation on the musculoskeletal structure of the cranium. The arched path of the adductor mandibulae and the greater rigidity of the lower jaw might be related to elongation of the snout, as it yields an increased mechanical advantage of the lower jaw system and a reduced torque between the elements of the lower jaw during protractor hyoidei muscle contraction, respectively. Nevertheless, most observed features did not seem to be related to snout length, but might be associated with different force-generating strategies.

Are morphological specializations of the hyolingual system in chameleons and salamanders tuned to demands on performance?

Extremely specialized and long tongues used for prey capture have evolved independently in plethodontid salamanders and chameleons. In both systems, the demands on tongue projection are probably similar: to maximize projection velocity and distance. Consequently, many of the design features of the projection system in these two groups have converged to an astonishing degree. Both involve the use of power amplification systems based on helically wound muscle fibers that load internal connective tissue sheets as illustrated in previous studies. Demands imposed on tongue retraction, however, are different to some degree. Although in both groups there is a clear demand for retraction capacity (given the long projection distances), in chameleons there is an added demand for force because they eat large and heavy prey. As indicated by our data, plethodontid salamanders have extremely long tongue retractors with normal striated muscle. Chameleons, on the other hand, evolved long retractors of the supercontracting type. Interestingly, our data show that at least in chameleons, the extreme design of the tongue in function of prey capture appears to have consequences on prey transport, resulting in an increased dependence on the hyoid. In turn, this has lead to an increase in transport-cycle duration and an increase in the number of cycles needed to transport prey in comparison with closely related agamid lizards. Clearly, extreme morphological specializations are tuned to functional and ecological demands and may induce a reduced performance in other functions performed by the same set of integrated structures.

Ontogeny of the cranial musculature in Corydoras aeneus Callichthyidae, Siluriformes.

A complete study of the early ontogeny of the cranial muscles of Corydoras aeneus (Callichthyidae) was undertaken and results were compared with those for the loricariid Ancistrus cf. triradiatus. This comparison reveals a high degree of similarity in the ontogeny of both species' cranial muscles. Both species lack a musculus protractor hyoidei, and the musculus intermandibularis posterior is divided into two different parts that have partly obtained a novel function (serving the lower lip) in A. cf. triradiatus. A similar increase in muscular complexity in this species is found in the dorsal constrictor of the hyoid muscle plate. This constrictor gives rise to the same muscles in both C. aeneus and A. cf. triradiatus, but in A. cf. triradiatus the musculus levator operculi later hypertrophies. In C. aeneus the musculus extensor tentaculi forms a single muscle diverging posteriorly, whereas in A. cf. triradiatus the musculus extensor tentaculi differentiates into two separate bundles. Also, a loricariid neoformation is present called the musculus levator tentaculi.

Cytochrome b sequence analysis reveals differential molecular evolution in African mole-rats of the chromosomally hyperdiverse genus Fukomys (Bathyergidae, Rodentia) from the Zambezian region.

African mole-rats (Bathyergidae, Rodentia) of the (eu)social genus Fukomys are one of the most speciose mammal genera endemic to Sub-Saharan Africa. Fukomys distributed in the Zambezian phytochorion is characterized by extreme chromosomal variation (2n=40-78). We inferred a molecular phylogeny of Zambezian Fukomys to resolve the interrelationships and the evolutionary history of the known chromosomal races. We sequenced the entire cytochrome b gene (1140bp) for a total of 66 specimens representing 18 karyotypical races from Zambia. An additional 31 sequences were retrieved from GenBank including data on all other chromosomal races. The haplotypes belonging to a small chromosomal race from Salujinga cluster with the Fukomys mechowii (Giant mole-rat) haplotypes. Differential degrees of chromosomal variation are observed among the major mole-rat clades, which is most pertinent when comparing the central Zambezian Fukomys micklemi and the northern Zambezian Fukomys whytei clades. The karyotypically hyper-diverse (12 known chromosomal races) Fukomys micklemi clade shows low levels of cytochrome b sequence divergence. Within the F. whytei clade we find a more conservative pattern of chromosomal diversification (three known chromosomal races) while the levels of sequence divergence are much higher then in the F. micklemi clade. Our results suggest that chromosomal changes may drive phyletic divergence and, eventually, speciation. The observed cladogenetic events during the Plio-Pleistocene within the F. mechowii, F. whytei, F. damarensis and F. micklemi clades appear to coincide with climatically mediated speciation bursts in other savannah dwelling mammals, including hominids. Based on the molecular data presented, combined with morphological and chromosomal data, the taxonomic implication seems to be that Fukomys may contain several (undescribed) cryptic species.

Morphological specializations in heterocongrinae (Anguilliformes: Congridae) related to burrowing and feeding.

The remarkable lifestyle of heterocongrines has drawn the attention of many authors in the past, though no or little attention has been paid to the morphology of the tail and the head of these species. In order to examine the true nature of possible morphological specializations of the head and tail and their relation to their tail-first burrowing habit and/or feeding mode, a detailed myological and osteological study of Heteroconger hassi and Heteroconger longissimus was performed. The osteological similarities of the cranial skeleton between H. hassi and H. longissimus are striking. Most of the cranial muscles show no variation in presence, insertion or origin between these two species except for the adductor mandibulae complex, the adductor hyomandibulae and the intermandibularis. The adductor mandibulae complex is small, compared to that of other anguilliform species, and is probably related to their suction-dominated feeding mode and a diet, comprising mainly small, soft prey items. Heterocongrinae have undergone several morphological specializations in the tail for their tail-first burrowing lifestyle. The skeleton and musculature of the tail of H. hassi and H. longissimus are similar. In both species the caudal skeleton is highly reduced and fortified, forming a firm, pointed burrowing tool. Intrinsic caudal musculature is reduced and some muscles (interradials, supracarinalis) are even absent.

Phylogenetic relationships and divergence time estimate of African anguilliform catfish (Siluriformes: Clariidae) inferred from ribosomal gene and spacer sequences.

The catfish family Clariidae comprises species in which the body shape ranges from fusiform to anguilliform. Recent studies have shown that this body elongation is the result of convergent evolution. This paper aims to study the evolution towards anguilliformity in a phylogenetic framework. Sequences of 29 taxa were analyzed using the neighbor-joining, maximum-likelihood, maximum-parsimony, and Bayesian inference algorithms and the parsimony algorithm in POY. The study yields phylogenetic hypotheses showing well-supported clades. Anguilliformity appears to have arisen at least four times, each time having a sister group relation with a fusiform Clarias-like ancestor. Divergence time estimation indicates that the African Clariidae started radiating between 123 and 56 My ago.

Moringua edwardsi (Moringuidae: Anguilliformes): cranial specialization for head-first burrowing?

The order Anguilliformes forms a natural group of eel-like species. Moringua edwardsi (Moringuidae) is of special interest because of its peculiar fossorial lifestyle: this species burrows head-first. Externally pronounced morphological specializations for a fossorial lifestyle include: reduced eyes, lack of color, low or absent paired vertical fins, elongated, cylindrical body, reduced head pores of the lateral line system, etc. Many fossorial amphibians, reptiles, and even mammals have evolved similar external specializations related to burrowing. The present study focuses on osteological and myological features of M. edwardsi in order to evaluate the structural modifications that may have evolved as adaptations to burrowing. Convergent evolutionary structures and possible relations with head-first burrowing, miniaturization, feeding habits, etc., were investigated. Body elongation, reduction of the eyes, modified cranial lateral line system, and modified skull shape (pointed though firm) can be considered specializations for head-first burrowing. Hyperossification can probably be regarded more as a specialization to both head-first burrowing and feeding, even though an impact of miniaturization cannot be excluded. Hypertrophied adductor mandibulae muscles and the enlarged coronoid process can be associated with both feeding requirements (it enhances bite forces necessary for their predatory behavior) and with a burrowing lifestyle, as well as miniaturization.

Ontogenetic shift in mouth opening mechanisms in a catfish (Clariidae, Siluriformes): a response to increasing functional demands.

During ontogeny, larval fish have to deal with increasing nutritional and respiratory demands as they grow. As early ontogeny is characterized by an increasing complexity of moving structural elements composing a fish skull, some constraints will have to be met when developing mechanisms, which enable feeding and respiration, arise at a certain developmental stage. This article focuses on the presence/absence of a possible functional response in mouth opening during ontogeny in Clarias gariepinus. Some reflections are given, based on morphological data, as well as related function-analysis data from the literature. Starting shortly after hatching, a total of up to five different mouth opening mechanisms may become functional. Of these, three may remain functional in the adult. As could be expected, the apparatuses that enable these mechanisms show an increase in complexity, as well as a putative improvement in mouth opening capacity. Initially, two consecutive mechanisms may allow a restricted depression of the lower jaw (both passively and actively). Synchronously, two more mechanisms may arise, which involve the coupling of the hyoid depression to the mouth opening. At about 11 mm SL a fifth mechanism becomes established, better known as the opercular mouth opening mechanism. An overlapping chronology of functionality of the different mechanisms, as well as differences in efficiencies, could be an indication of the absence of a true critical period in C. gariepinus (at least in relation to mouth opening), as well as the possible presence of a shift in feeding type. Finally, the coupling of the chronology of the shift in mouth opening mechanisms and several morphological, behavioral, and physiological changes during ontogeny, related to feeding and respiration, make it possible to distinguish five important phases in the early life history of C. gariepinus.