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.

Characteristics of sound production and associated pharyngeal jaws in the tomtate grunt Haemulon aurolineatum (Cuvier, 1830) in Caribbean reefs

The ability to produce sounds for acoustic communication is well known in different grunt species (Haemulidae). However, most of the sounds have not been described and the sound-producing mechanism of very few grunt species has been deeply studied. Additional data is needed to search for synapomorphy in the sonic mechanism. This study describes acoustic features and branchial anatomy in Haemulon aurolineatum. Correlations were found between some acoustic features and standard length, showing the largest specimens produced shorter, lower-pitched grunts of higher intensity. Examinations of acoustic features and branchial anatomy show that H. aurolineatum uses the same stridulatory mechanism described previously in H. flavolineatum. The unusual feature of Haemulon species concerns the fourth ceratobranchials. These appear to be part of the lower pharyngeal jaws since they possess firmly attached teeth that face the upper pharyngeal jaws. The stridulation results from the rubbing of both pharyngeal and fourth ceratobranchial teeth. This mechanism is probably common to the 23 Haemulon species, but additional information is needed regarding the mechanism of other Haemulinae species to produce stridulatory sounds. Fourth ceratobranchials could constitute a key element of Haemulinae ability to produce sounds providing an eventual synapomorphic aspect of the mechanism in the family.

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 Genomic Cluster Containing Novel and Conserved Genes is Associated with Cichlid Fish Dental Developmental Convergence

The two toothed jaws of cichlid fishes provide textbook examples of convergent evolution. Tooth phenotypes such as enlarged molar-like teeth used to process hard-shelled mollusks have evolved numerous times independently during cichlid diversification. Although the ecological benefit of molar-like teeth to crush prey is known, it is unclear whether the same molecular mechanisms underlie these convergent traits. To identify genes involved in the evolution and development of enlarged cichlid teeth, we performed RNA-seq on the serially homologous-toothed oral and pharyngeal jaws as well as the fourth toothless gill arch of Astatoreochromis alluaudi. We identified 27 genes that are highly upregulated on both tooth-bearing jaws compared with the toothless gill arch. Most of these genes have never been reported to play a role in tooth formation. Two of these genes (unk, rpfA) are not found in other vertebrate genomes but are present in all cichlid genomes. They also cluster genomically with two other highly expressed tooth genes (odam, scpp5) that exhibit conserved expression during vertebrate odontogenesis. Unk and rpfA were confirmed via in situ hybridization to be expressed in developing teeth of Astatotilapia burtoni. We then examined expression of the cluster’s four genes in six evolutionarily independent and phylogenetically disparate cichlid species pairs each with a large- and a small-toothed species. Odam and unk commonly and scpp5 and rpfA always showed higher expression in larger toothed cichlid jaws. Convergent trophic adaptations across cichlid diversity are associated with the repeated developmental deployment of this genomic cluster containing conserved and novel cichlid-specific genes.

An XROMM Study of Food Transport and Swallowing in Channel Catfish

Synopsis Most predatory ray-finned fishes swallow their food whole, which can pose a significant challenge, given that prey items can be half as large as the predators themselves. How do fish transport captured food from the mouth to the stomach? Prior work indicates that, in general, fish use the pharyngeal jaws to manipulate food into the esophagus, where peristalsis is thought to take over. We used X-Ray Reconstruction of Moving Morphology to track prey transport in channel catfish (Ictalurus punctatus). By reconstructing the 3D motions of both the food and the catfish, we were able to track how the catfish move food through the head and into the stomach. Food enters the oral cavity at high velocities as a continuation of suction and stops in the approximate location of the branchial basket before moving in a much slower, more complex path toward the esophagus. This slow phase coincides with little motion in the head and no substantial mouth opening or hyoid depression. Once the prey is in the esophagus, however, its transport is surprisingly tightly correlated with gulping motions (hyoid depression, girdle retraction, hypaxial shortening, and mouth opening) of the head. Although the transport mechanism itself remains unknown, to our knowledge, this is the first description of synchrony between cranial expansion and esophageal transport in a fish. Our results provide direct evidence of prey transport within the esophagus and suggest that peristalsis may not be the sole mechanism of esophageal transport in catfish.

Pharyngeal Jaws Converge by Similar Means, Not to Similar Ends, When Minnows (Cypriniformes: Leuciscidae) Adapt to New Dietary Niches

Convergent evolution is at the forefront of many form-function studies. There are many examples of multiple independent lineages evolving a similar morphology in response to similar functional demands, providing a framework for testing hypotheses of form-function evolution. However, there are numerous clades with underappreciated convergence, in which there is a perceived homogeneity in morphology. In these groups, it can be difficult to investigate causal relationships of form and function (e.g., diet influencing the evolution of jaw morphology) without the ability to disentangle phylogenetic signal from convergence. Leuciscids (Cypriniformes: Leuciscidae; formerly nested within Cyprinidae) are a species-rich clade of fishes that have diversified to occupy nearly every freshwater trophic niche, yet are considered to have relatively low morphological diversity relative to other large freshwater clades. Within the North American leuciscids, many genera contain at least one herbivore, insectivore, and larvaphage. We created 3D models from micro-computed tomography scans of 165 leuciscid species to measure functionally relevant traits within the pharyngeal jaws of these fishes. Using a published phylogeny, we tested these metrics for evolutionary integration, phylogenetic signal, and correlation with diet. Measurements of the pharyngeal jaws, muscle attachment areas, and teeth showed strong positive evolutionary correlation with each other and negative evolutionary correlation with measurements of the inter-ceratobranchial ligament (ICB ligament). Using diet data from published literature, we found extensive dietary convergence within Leuciscidae. The most common transitions we found were between herbivorous and invertivorous taxa and between insectivore types (aquatic vs. terrestrial). We document a trade-off in which herbivorous leuciscids have large teeth, short ICB ligaments, and large muscle attachment areas, whereas insectivorous leuciscids showed the opposite pattern. Inverse patterns of morphological integration between the ICB ligament the rest of the pharyngeal jaw correspond this dietary trade-off, which indicates that coordinated evolution of morphological traits contributes to functional diversity in this clade. However, these patterns only emerge in the context of phylogeny, meaning that the pharyngeal jaws of North American leuciscids converge by similar means (structural changes in response to dietary demands), but not necessarily to similar ends (absolute phenotype).

The Role of Developmental Integration and Historical Contingency in the Origin and Evolution of Cypriniform Trophic Novelties

While functional morphologists have long studied the evolution of anatomical structures, the origin of morphological novelties has received less attention. When such novelties first originate they must become incorporated into an integrated system to be rendered fully functional. Thus, developmental integration is key at the origin of morphological novelties. However, given enough evolutionary time such integration may be broken, allowing for a division of labor that is facilitated by subsequent decoupling of structures. Cypriniformes represent a diverse group of freshwater fishes characterized by several trophic novelties that include: kinethmoid-mediated premaxillary protrusion, a muscular palatal and post-lingual organ, hypertrophied lower pharyngeal jaws that masticate against the base of the neurocranium, novel pharyngeal musculature controlling movement of the hypertrophied lower pharyngeal jaws, and in a few species an incredibly complex epibranchial organ used to aggregate filtered phytoplankton. Here, we use the wealth of such trophic novelties in different cypriniform fishes to present case studies in which developmental integration allowed for the origin of morphological innovations. As proposed in case studies 1 and 2 trophic innovations may be associated with both morphological and lineage diversification. Alternatively, case studies 3 and 4 represent a situation where ecological niche was expanded but with no concomitant increase in species diversity.