The moment of tooth: rate, fate and pattern of Pacific lingcod dentition revealed by pulse-chase

Tooth replacement rates of polyphyodont cartilaginous and bony fishes are hard to determine because of a lack of obvious patterning and maintaining specimens long enough to observe replacement. Pulse-chase is a fluorescent technique that differentially colours developing mineralized tissue. We present in situ tooth replacement rate and position data for the oral and pharyngeal detentions of Ophiodon elongatus (Pacific lingcod). We assessed over 10 000 teeth, in 20 fish, and found a daily replacement rate of about two teeth (3.6% of the dentition). The average tooth is in the dental battery for 27 days. The replacement was higher in the lower pharyngeal jaw (LPJ). We found no difference between replacement rates of feeding and non-feeding fish, suggesting feeding was not a driver of tooth replacement. Lingcod teeth have both a size and location fate; smaller teeth at one spot will not grow into larger teeth, even if a large tooth nearby is lost. We also found increased rates of replacement at the posterior of the LPJ relative to the anterior. We propose that lingcod teeth do not migrate in the jaw as they develop; their teeth are fated in size and location, erupting in their functional position.

The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley.

Snowflake morays, Echidna nebulosa, exhibit similar feeding kinematics in terrestrial and aquatic treatments

Some species of durophagous moray eels (Muraenidae) have been documented emerging from the marine environment to capture intertidal crabs but how they consume prey out of water is unknown. Here we trained snowflake morays, Echidna nebulosa, to undulate out of the aquatic environment to feed on land. On land, snowflake morays remove prey from the substrate by biting and swallow prey using pharyngeal jaw enabled transport. Although snowflake morays exhibit smaller jaw rotation angles on land when apprehending their prey, transport kinematics involving dorso-ventral flexion of the head to protract the pharyngeal jaws and overall feeding times did not differ between terrestrial and aquatic treatments. We suggest that their elongate body plan, ability to rotate their heads in the dorsoventral and lateral directions, and extreme pharyngeal movements, all contribute to the ability of durophagous morays to feed in the terrestrial environment.

Gene coexpression networks reveal molecular interactions underlying cichlid jaw modularity

Background The oral and pharyngeal jaw of cichlid fishes are a classic example of evolutionary modularity as their functional decoupling boosted trophic diversification and contributed to the success of cichlid adaptive radiations. Most studies until now have focused on the functional, morphological, or genetic aspects of cichlid jaw modularity. Here we extend this concept to include transcriptional modularity by sequencing whole transcriptomes of the two jaws and comparing their gene coexpression networks. Results We show that transcriptional decoupling of gene expression underlies the functional decoupling of cichlid oral and pharyngeal jaw apparatus and the two units are evolving independently in recently diverged cichlid species from Lake Tanganyika. Oral and pharyngeal jaw coexpression networks reflect the common origin of the jaw regulatory program as there is high preservation of gene coexpression modules between the two sets of jaws. However, there is substantial rewiring of genetic architecture within those modules. We define a global jaw coexpression network and highlight jaw-specific and species-specific modules within it. Furthermore, we annotate a comprehensive in silico gene regulatory network linking the Wnt and AHR signalling pathways to jaw morphogenesis and response to environmental cues, respectively. Components of these pathways are significantly differentially expressed between the oral and pharyngeal jaw apparatus. Conclusion This study describes the concerted expression of many genes in cichlid oral and pharyngeal jaw apparatus at the onset of the independent life of cichlid fishes. Our findings suggest that – on the basis of an ancestral gill arch network—transcriptional rewiring may have driven the modular evolution of the oral and pharyngeal jaws, highlighting the evolutionary significance of gene network reuse. The gene coexpression and in silico regulatory networks presented here are intended as resource for future studies on the genetics of vertebrate jaw morphogenesis and trophic adaptation.

Convergent Evolution of Cichlid Fish Pharyngeal Jaw Dentitions in Mollusk-Crushing Predators: Comparative X-Ray Computed Tomography of Tooth Sizes, Numbers, and Replacement

Dental convergence is a hallmark of cichlid fish adaptive radiations. This type of repeated evolution characterizes both the oral jaws of these fishes as well as their pharyngeal jaws that are modified gill arches used to functionally process prey like hard-shelled mollusks. To test several hypotheses regarding the evolution of cichlid crushing pharyngeal dentitions, we used X-ray computed tomography scans to comparatively examine dental evolution in the pharyngeal jaw of a diversity of New World Heroine cichlid lineages. The substantial variation in erupted tooth sizes and numbers as well as replacement teeth found in these fishes showed several general patterns. Larger toothed species tended to have fewer teeth suggesting a potential role of spatial constraints in cichlid dental divergence. Species with larger numbers of erupted pharyngeal teeth also had larger numbers of replacement teeth. Replacement tooth size is almost exactly predicted (r = 0.99) from the size of erupted teeth across all of the species. Mollusk crushing was, therefore, highly associated with not only larger pharyngeal teeth, but also larger replacement teeth. Whether dental divergence arises as a result of environmental induced plasticity or originates via trophic polymorphism as found in the species Herichthys minckleyi, there appear to be general rules that structure interspecific divergence in cichlid pharyngeal erupted and replacement dentitions.

A peacock bass (Cichla) functional novelty relaxes a constraint imposed by the classic cichlid pharyngeal jaw innovation

Innovations may provide access to new resources but often result in significant trade-offs. Pharyngognathy is a classic pharyngeal jaw innovation in which the left and right lower pharyngeal jaw (LPJ) bones are united into a single structure, producing a strong bite but reduced gape. Throughout cichlids, pharyngeal suturing occurs along the entire medial border between LPJ bones, except in peacock bass (Cichla), where these bones are connected by ligaments only in their anterior region. We show that this limited attachment permits the jaw bones to spread apart and we link this feature to an increase in pharyngeal gape that is comparable to non-pharyngognathous species. The capacity of the LPJ bones to spread apart is strongest in juveniles and is mostly lost during development. Juvenile Cichla exhibit size-specific pharyngeal gape similar to non-pharyngognathous percomorphs; however, adults exhibit pharyngeal gape on par with other predatory cichlids. Relaxation of pharyngeal suturing offsets a major deleterious consequence of pharyngognathy by reducing gape limitation and we propose this may accelerate the ontogenetic transition to piscivory. Partial reversal of the classic cichlid pharyngeal jaw innovation highlights the functional trade-offs that often accompany innovations and may be a major cause of variation in their macroevolutionary consequences.