Premaxillary protrusion and the performance advantages it confers are implicated in the success of diverse lineages of teleost fishes, such as Cypriniformes and Acanthomorpha. Although premaxillary ...protrusion has evolved independently at least five times within bony fishes, much of the functional work investigating this kinesis relates to mechanisms found only in these two clades. Few studies have characterized feeding mechanisms in less-diverse premaxilla-protruding lineages and fewer yet have investigated the distinctive anatomy underlying jaw kinesis in these lineages. Here, we integrated dissection, clearing and staining, histology, micro-CT, and high-speed videography to investigate an isolated and independent origin of jaw protrusion in the hingemouth, Phractolaemus ansorgii, which employs a complex arrangement of bones, musculature, and connective tissues to feed on benthic detritus via a deployable proboscis. Our goals were to provide an integrative account of the underlying architecture of P. ansorgii's feeding apparatus and to assess the functional consequences of this drastic deviation from the more typical teleost condition. Phractolaemus ansorgii's cranial anatomy is distinct from all other fishes in that its adducted lower jaw is caudally oriented, and it possesses a mouth at the terminal end of an elongated, tube-like proboscis that is unique in its lack of skeletal support from the oral jaws. Instead, its mouth is supported primarily by hyaline-cell cartilage and other rigid connective tissues, and features highly flexible lips that are covered in rows of keratinous unculi. Concomitant changes to the adductor musculature likely allow for the flexibility to protrude the mouth dorsally and ventrally as observed during different feeding behaviors, while the intrinsic compliance of the lips allows for more effective scraping of irregular surfaces. From our feeding videos, we find that P. ansorgii is capable of modulating the distance of protrusion, with maximum anterior protrusion exceeding 30% of head length. This represents a previously undescribed example of extreme jaw protrusion on par with many acanthomorph species. Protrusion is much slower in P. ansorgii-reaching an average speed of 2.74 cm/s-compared to acanthomorphs feeding on elusive prey or even benthivorous cypriniforms. However, this reorganization of cranial anatomy may reflect a greater need for dexterity to forage more precisely in multiple directions and on a wide variety of surface textures. Although this highly modified mechanism may have limited versatility over evolutionary timescales, it has persisted in solitude within Gonorynchiformes, representing a novel functional solution for benthic feeding in tropical West African rivers.
Epibranchial organs (EBOs), found in at least five of the eight otomorphan families, are used to aggregate small prey inside the buccopharyngeal cavity and range in morphological complexity from a ...singular, small slit on the pharyngeal roof to several, elongated soft tissue tubes. Despite broad phylogenetic representation, little is known about the origin, development, or evolution of EBOs. We hypothesize that both heterochronic and heterotopic changes throughout the evolution of EBOs are at the root of their morphological diversity. Heterochrony is a foundational explanation in developmental studies, however, heterotopy, a developmental change in spatial or topographical relationships, can have even more profound effects on a given structure but has received relatively little attention. Here, we investigate how developmental mechanisms may drive morphological diversity of EBOs within otomorphan fishes. We compare early pharyngeal development in three species, Anchoa mitchilli (Engraulidae) which has the most basic EBO, B. tyrannus (Clupeidae) which has a more complex EBO, and Hypophthalmichthys molitrix (Cyprinidae) which has the most complex EBO yet described. Using branchial arch growth rates and morphological analyses, we illustrate how both heterochronic and heterotopic mechanisms are responsible for some of the phenotypic diversity seen in otomorphan EBOs. Importantly, we also identify conserved developmental patterns that further our understanding of how EBOs may have first originated and evolved across actinopterygian fishes.
The epibranchial organ (EBO) is a novel feeding structure in several Otomorphan fishes and thought to allow for the efficient aggregation of small prey. EBOs are morphologically diverse ranging from a single, muscular opening to elongated soft tissue tubes. Despite broad phylogenetic representation, little is known about the origin, development, or evolution of EBOs. Using branchial arch growth rates and morphological analyses, we illustrate how both heterochronic and heterotopic mechanisms are responsible for some of EBO phenotypic diversity. We also identify conserved developmental patterns that further our understanding of how EBOs may have first originated and evolved across actinopterygian fishes.
Highlights
This manuscript details the development, origin, and evolution of epibranchial organs (EBOs) in three species of Otomorphan fishes: Anchoa mitchilli, Brevoortia tyrannus, and Hypophthalmichthys molitrix. Through a comparative analysis, we find evidence that both heterochronic and heterotopic mechanisms are responsible for the morphological diversity of EBOs and that a heterotopic shift is likely what allowed this organ in silver carp to be so much more complex than those seen in other fishes.
We review the origins, prominent innovations, and major patterns of diversification in suction feeding by vertebrates. Non-vertebrate chordates and larval lamprey suspension-feed by capturing small ...particles in pharyngeal mucous. In most of these lineages the gentle flows that transport particles are generated by buccal cilia, although larval lamprey and thaliacean urochordates have independently evolved a weak buccal pump to generate an oscillating flow of water that is powered by elastic recovery of the pharynx following compression by buccal muscles. The evolution of jaws and the hyoid facilitated powerful buccal expansion and high-performance suction feeding as found today throughout aquatic vertebrates. We highlight three major innovations in suction feeding. Most vertebrate suction feeders have mechanisms that occlude the corners of the open mouth during feeding. This produces a planar opening that is often nearly circular in shape. Both features contribute to efficient flow of water into the mouth and help direct the flow to the area directly in front of the mouth’s aperture. Among several functions that have been identified for protrusion of the upper jaw, is an increase in the hydrodynamic forces that suction feeders exert on their prey. Protrusion of the upper jaw has evolved five times in ray-finned fishes, including in two of the most successful teleost radiations, cypriniforms and acanthomorphs, and is found in about 60% of living teleost species. Diversification of the mechanisms of suction feeding and of feeding behavior reveals that suction feeders with high capacity for suction rarely approach their prey rapidly, while slender-bodied predators with low capacity for suction show the full range of attack speeds. We hypothesize that a dominant axis of diversification among suction feeders involves a trade-off between the forces that are exerted on prey and the volume of water that is ingested.
Some fishes rely on large regions of the dorsal (epaxial) and ventral (hypaxial) body muscles to power suction feeding. Epaxial and hypaxial muscles are known to act as motors, powering rapid mouth ...expansion by shortening to elevate the neurocranium and retract the pectoral girdle, respectively. However, some species, like catfishes, use little cranial elevation. Are these fishes instead using the epaxial muscles to forcefully anchor the head, and if so, are they limited to lower-power strikes? We used X-ray imaging to measure epaxial and hypaxial length dynamics (fluoromicrometry) and associated skeletal motions (XROMM) during 24 suction feeding strikes from three channel catfish (
). We also estimated the power required for suction feeding from oral pressure and dynamic endocast volume measurements. Cranial elevation relative to the body was small (<5 deg) and the epaxial muscles did not shorten during peak expansion power. In contrast, the hypaxial muscles consistently shortened by 4-8% to rotate the pectoral girdle 6-11 deg relative to the body. Despite only the hypaxial muscles generating power, catfish strikes were similar in power to those of other species, such as largemouth bass (
), that use epaxial and hypaxial muscles to power mouth expansion. These results show that the epaxial muscles are not used as motors in catfish, but suggest they position and stabilize the cranium while the hypaxial muscles power mouth expansion ventrally. Thus, axial muscles can serve fundamentally different mechanical roles in generating and controlling cranial motion during suction feeding in fishes.
When animals move they must coordinate motion among multiple parts of the musculoskeletal system. Different behaviours exhibit different patterns of coordination, however, it remains unclear what ...general principles determine the coordination pattern for a particular behaviour. One hypothesis is that speed determines coordination patterns as a result of differences in voluntary versus involuntary control. An alternative hypothesis is that the nature of the behavioural task determines patterns of coordination. Suction-feeding fishes have highly kinetic skulls and must coordinate the motions of over a dozen skeletal elements to draw fluid and prey into the mouth. We used a dataset of intracranial motions at five cranial joints in channel catfish ( Ictalurus punctatus), collected using X-ray reconstruction of moving morphology, to test whether speed or task best explained patterns of coordination. We found that motions were significantly more coordinated (by 20-29%) during prey capture than during prey transport, supporting the hypothesis that the nature of the task determines coordination patterns. We found no significant difference in coordination between low- and high-speed motions. We speculate that capture is more coordinated to create a single fluid flow into the mouth while transport is less coordinated so that the cranial elements can independently generate multiple flows to reposition prey. Our results demonstrate the benefits of both higher and lower coordination in animal behaviours and the potential of motion analysis to elucidate motor tasks.
The Ontology for Biomedical Investigations (OBI) is an ontology that provides terms with precisely defined meanings to describe all aspects of how investigations in the biological and medical domains ...are conducted. OBI re-uses ontologies that provide a representation of biomedical knowledge from the Open Biological and Biomedical Ontologies (OBO) project and adds the ability to describe how this knowledge was derived. We here describe the state of OBI and several applications that are using it, such as adding semantic expressivity to existing databases, building data entry forms, and enabling interoperability between knowledge resources. OBI covers all phases of the investigation process, such as planning, execution and reporting. It represents information and material entities that participate in these processes, as well as roles and functions. Prior to OBI, it was not possible to use a single internally consistent resource that could be applied to multiple types of experiments for these applications. OBI has made this possible by creating terms for entities involved in biological and medical investigations and by importing parts of other biomedical ontologies such as GO, Chemical Entities of Biological Interest (ChEBI) and Phenotype Attribute and Trait Ontology (PATO) without altering their meaning. OBI is being used in a wide range of projects covering genomics, multi-omics, immunology, and catalogs of services. OBI has also spawned other ontologies (Information Artifact Ontology) and methods for importing parts of ontologies (Minimum information to reference an external ontology term (MIREOT)). The OBI project is an open cross-disciplinary collaborative effort, encompassing multiple research communities from around the globe. To date, OBI has created 2366 classes and 40 relations along with textual and formal definitions. The OBI Consortium maintains a web resource (http://obi-ontology.org) providing details on the people, policies, and issues being addressed in association with OBI. The current release of OBI is available at http://purl.obolibrary.org/obo/obi.owl.
Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated ...phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This ‘ecomechanical approach’ integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.
All organisms must comply with physical laws, which place rigid or hard constraints on survival and reproduction. Ecomechanics is the expression of that interplay, and assumes a central role when considering organismal development, ecology, and evolution.How organisms will respond to changes in the environment, such as human-mediated climate change, will depend strongly on ecomechanics.Functional traits are commonly used to investigate the consequences of ecological variation. Ecomechanical models that incorporate functional traits and environmental variables are key to deciphering the rules of life and expand upon functional trait studies.The use of the ecomechanical framework is illustrated using multiple examples (e.g., wind-induced bending mechanics in trees and gecko adhesion in the real world). We emphasize safety factors as a key metric when assessing the evolution of form and performance. Biologists can apply our framework to many other systems.We offer suggestions for constructing and tailoring the data pipeline for future ecomechanical models to enhance their availability and utility for various disciplines.
Tooth replacement in piranhas is unusual: all teeth on one side of the head are lost as a unit, then replaced simultaneously. We used histology and microCT to examine tooth‐replacement modes across ...carnivorous piranhas and their herbivorous pacu cousins (Serrasalmidae) and then mapped replacement patterns onto a molecular phylogeny. Pacu teeth develop and are replaced in a manner like piranhas. For serrasalmids, unilateral tooth replacement is not an “all or nothing” phenomenon; we demonstrate that both sides of the jaws have developing tooth rows within them, albeit with one side more mineralized than the other. All serrasalmids (except one) share unilateral tooth replacement, so this is not an adaptation for carnivory. All serrasalmids have interlocking teeth; piranhas interdigitate lateral tooth cusps with adjacent teeth, forming a singular saw‐like blade, whereas lateral cusps in pacus clasp together. For serrasalmids to have an interlocking dentition, their teeth need to develop and erupt at the same time. We propose that interlocking mechanisms prevent tooth loss and ensure continued functionality of the feeding apparatus. Serrasalmid dentitions are ubiquitously heterodont, having incisiform and molariform dentitions reminiscent of mammals. Finally, we propose that simultaneous tooth replacement be considered as a synapomorphy for the family.
Tooth replacement in piranhas and pacus (Serrasalmidae) is unusual: All teeth on one side of the head are lost as a unit, then replaced simultaneously. We used histology and microCT to examine tooth‐replacement modes across carnivorous piranhas and their herbivorous pacu cousins. Unilateral tooth replacement arose in herbivorous pacu‐like ancestors, suggesting this tooth‐replacement mode is an exaptation for carnivory in piranha lineages. All serrasalmids have interlocking teeth; piranhas interdigitate lateral tooth cusps with adjacent teeth, forming a singular saw‐like blade, whereas lateral cusps in pacus clasp together. For serrasalmids to have an interlocking dentition, their teeth need to develop and erupt at the same time.
RESEARCH HIGHLIGHTS
Piranhas and pacus lose all teeth on one side of their head at once. Teeth are also heterodont and lock together, therefore, needing to be replaced simultaneously. As this phenomenon arose in herbivorous pacus, it is exapted for carnivory in piranhas.
Remoras are fishes that piggyback onto larger marine fauna via an adhesive disc to increase locomotor efficiency, likelihood of finding mates and access to prey. Attaching rapidly to a large, ...fast-moving host is no easy task, and while research to date has focused on how the disc supports adhesion, no attention has been paid to how or if remoras are able to sense attachment. We identified push-rod-like mechanoreceptor complexes embedded in the soft lip of the remora adhesive disc that are known in other organisms to respond to touch and shear forces. This is, to our knowledge, the first time such mechanoreceptor complexes are described in fishes as they were only known previously in monotremes. The presence of push-rod-like mechanoreceptor complexes suggests not only that fishes may be able to sense their environment in ways not heretofore described but that specialized tactile mechanoreceptor complexes may be a more basal vertebrate feature than previously thought.
Bottom Feeding and Beyond Hernandez, L. Patricia; Staab, Katie Lynn
Integrative and comparative biology,
07/2015, Letnik:
55, Številka:
1
Journal Article
Recenzirano
Odprti dostop
While much of the functional work on suction feeding has involved members of Acanthopterygii, an earlier cypriniform radiation led to over 3200 species filling nearly every freshwater trophic niche. ...Within the great majority of acanthomorph clades that have been investigated suction feeding and the underlying morphology responsible for the generation of rapid suction have been largely conserved. This conserved feeding-apparatus is often associated with increasing the force experienced by the prey item, thus making a strike on elusive prey more effective. Cypriniforms’ trophic anatomy is comprised of a number of novelties used for benthic feeding, which characterized early members of this clade. The modified cypriniform structure of the oral jaws represents a situation in which a particular type of suction feeding allowed for probing the benthos with a more functionally maneuverable anatomy. Requisite evolutionary modifications included origin and elongation of a median kinethmoid, duplications of certain divisions of the muscles of the adductor mandibulae, and origin of a dorsal, intra-buccal muscular palatal organ used in winnowing detritus. The elongated kinethmoid (coupled with modified adductor muscles) allowed for a type of premaxillary protrusion that decoupled the upper and lower jaws, enabled premaxillary protrusions with a closed mouth, and facilitated benthic feeding by increasing functional flexibility. The resultant flow of fluid generated by cypriniforms is also quite flexible, with multiple instances of peak flow in a single feeding event. This greatly modified morphology allowed for a degree of kinematic maneuverability not seen within most acanthomorphs. Later cypriniform radiations into piscivorous, insectivorous, or planktivorous feeding guilds were associated with shortening of the kinethmoid and with simplified morphology of the adductor, likely involving an emphasis on ram feeding. Although this suite of morphological novelties seemingly originated within the context of benthic feeding, with minimal modifications these anatomical features were later coopted during radiations into different functional niches.
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