Evolution of the feeding mechanism in primitive actionopterygian fishes: A functional anatomical analysis of Polypterus, Lepisosteus, and Amia.
01 Mar 1980-Journal of Morphology (Wiley Subscription Services, Inc., A Wiley Company)-Vol. 163, Iss: 3, pp 283-317
TL;DR: The comparative functional anatomy of feeding in Polypterus senegalus, Lepisosteus oculatus, and Amia calva, three primitive actinopterygian fishes, was studied by high‐speed cinematography synchronized with electromyographic recordings of cranial muscle activity.
Abstract: The comparative functional anatomy of feeding in Polypterus senegalus, Lepisosteus oculatus, and Amia calva, three primitive actinopterygian fishes, was studied by high-speed cinematography (200 frames per second) synchronized with electromyographic recordings of cranial muscle activity. Several characters of the feeding mechanism have been identified as primitive for actinopterygian fishes: (1) Mandibular depression is mediated by the sternohyoideus muscle via the hyoid apparatus and mandibulohyoid ligament. (2) The obliquus inferioris and sternohyoideus muscles exhibit synchronous activity at the onset of the expansive phase of jaw movement. (3) Activity in the adductor operculi occurs in a double burst pattern—an initial burst at the onset of the expansive phase, followed by a burst after the jaws have closed. (4) A median septum divides the sternohyoideus muscle into right and left halves which are asymmetrically active during chewing and manipulation of prey. (5) Peak hyoid depression occurs only after peak gape has been reached and the hyoid apparatus remains depressed after the jaws have closed. (6) The neurocranium is elevated by the epaxial muscles during the expansive phase. (7) The adductor mandibulae complex is divided into three major sections—an anterior (suborbital) division, a medial division, and a posterolateral division.
In Polypterus, the initial strike lasts from 60 to 125 msec, and no temporal overlap in muscle activity occurs between muscles active at the onset of the expansive phase (sternohyoideus, obliquus superioris, epaxial muscles) and the jaw adductors of the compressive phase. In Lepisosteus, the strike is extremely rapid, often occuring in as little as 20 msec. All cranial muscles become active within 10 msec of each other, and there is extensive overlap in muscle activity periods.
Two biomechanically independent mechanisms mediate mandibular depression in Amia, and this duality in mouth-opening couplings is a shared feature of the halecostome fishes. Mandibular depression by hyoid retraction, and intermandibular musculature, consisting of an intermandibularis posterior and interhyoideus, are hypothesized to be primitive for the Teleostomi.
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TL;DR: A multiscale experimental and computational approach is presented that reveals the materials design principles present within individual ganoid scales from the 'living fossil' Polypterus senegalus, which belongs to the ancient family Polypteridae.
Abstract: Knowledge of the structure–property–function relationships of dermal scales of armoured fish could enable pathways to improved bioinspired human body armour, and may provide clues to the evolutionary origins of mineralized tissues. Here, we present a multiscale experimental and computational approach that reveals the materials design principles present within individual ganoid scales from the ‘living fossil’ Polypterus senegalus. This fish belongs to the ancient family Polypteridae, which first appeared 96 million years ago during the Cretaceous period and still retains many of their characteristics. The mechanistic origins of penetration resistance (approximating a biting attack) were investigated and found to include the juxtaposition of multiple distinct reinforcing composite layers that each undergo their own unique deformation mechanisms, a unique spatial functional form of mechanical properties with regions of differing levels of gradation within and between material layers, and layers with an undetectable gradation, load-dependent effective material properties, circumferential surface cracking, orthogonal microcracking in laminated sublayers and geometrically corrugated junctions between layers. The scales of a fish are its first level of defence. Now, the multilayered structure of fish scales has been analysed according to its mechanical properties and penetration resistance. This study of the four different layers provides a mechanistic understanding of evolutionary design as well as inspiring new materials for armour protection.
401 citations
TL;DR: Five features fundamental to the biology of acipenseriforms that benefit from the availability of the new phylogenetic hypothesis are discussed, and a cladogram summarizing osteological characters for those four groups is provided.
Abstract: Acipenseriformes occupy a special place in the history of ideas concerning fish evolution, but in many respects, phylogenetic studies of the group remain in their infancy Even such basic questions as the monophyly of Acipenser (the largest genus) are unanswered We define relationships based on comparative osteology, which allows us to incorporate well-preserved fossils into analyses Acipenseriformes has existed at least since the Lower Jurassic (approximately 200 MYBP), and all fossil and recent taxa are from the Holarctic Phylogenetic relationships among Paleozoic and Early Mesozoic actinopterygians are problematic, but most workers agree that Acipenseriformes is monophyletic and derived from some component of ‘paleonisciform’ fishes (‘Paleonisciformes’ is a grade of primitive non-neopterygian actinopterygians, sensu Gardiner 1993) Taxa discussed in comparison here are: †Cheirolepis, Polypterus, †Mimia †Moythomasia, †Birgeria, †Saurichthys, Lepisosteus and Amia We review generic diversity within the four nominal families of fossil and recent Acipenseriformes (†Chondrosteidae, †Peipiaosteidae, Polyodontidae, and Acipenseridae), and provide a cladogram summarizing osteological characters for those four groups Monophyly of the two extant families is well-supported, but there are no comprehensive studies of all of the known species and specimens of †Chondrosteidae and †Peipiaosteidae As a result, sister-group relationships among †Chondrosteidae, †Peipiaosteidae, and Acipenseroidei (= Polyodontidae + Acipenseridae)are unresolved We discuss five features fundamental to the biology of acipenseriforms that benefit from the availability of our new phylogenetic hypothesis: (1) specializations of jaws and operculum relevant to jaw protrusion, feeding, and ram ventilation; (2) anadromy or potamodromy and demersal spawning; (3) paedomorphosis and evolution of the group; (4) the biogeography of Asian and North American polyodontids and scaphirhynchines; and (5) the great abundance of electroreceptive organs in the rostral and opercular regions Finally, we summarize our nomenclatural recommendations
332 citations
01 Jan 1982
TL;DR: The starting point of comparative evolutionary studies of the dermal skeleton of vertebrates is Hertwig’s series of papers (1874, 1876/1879/1882), which directly stimulated many dozens of papers, most of them in German and some of them long forgotten.
Abstract: The starting point of comparative evolutionary studies of the dermal skeleton of vertebrates is Hertwig’s series of papers (1874, 1876/1879/1882), which directly stimulated many dozens of papers, most of them in German and some of them long forgotten. The literature on comparative histology and histogenesis of the dermal skeleton and on regulatory and morphogenetic processes of the vertebrate integument is so voluminous that it can hardly be summarized. Ever since Hertwig, attempts have been made not only to contribute descriptive and experimental data, but also to arrive at a synthesis. Most of the synthetic papers, however, address only a small section of the theoretical problems, and it seems that some important questions have never been asked.
260 citations
TL;DR: This study examines the diversity of mechanical design of the oral jaws in 35 species of ray-finned fishes to analyze lower jaw lever models in a broad phylogenetic range of taxa and identify the origin and evolutionary patterns of change in the linkage systems that power maxillary rotation and upper jaw protrusion.
Abstract: SYNOPSIS. The evolution of feeding mechanisms in the ray-finned fishes (Actinopterygii) is a compelling example of transformation in a musculoskeletal complex involving multiple skeletal elements and numerous muscles that power skull motion. Biomechanical models of jaw force and skull kinetics aid our understanding of these complex systems and enable broad comparison of feeding mechanics across taxa. Mechanical models characterize how muscles move skeletal elements by pulling bones around points of rotation in lever mechanisms, or by transmitting force through skeletal elements connected in a linkage. Previous work has focused on the feeding biomechanics of several lineages of fishes, but a broader survey of skull function in the context of quantitative models has not been attempted. This study begins such a survey by examining the diversity of mechanical design of the oral jaws in 35 species of ray-finned fishes with three main objectives: (1) analyze lower jaw lever models in a broad phylogenetic range of taxa, (2) identify the origin and evolutionary patterns of change in the linkage systems that power maxillary rotation and upper jaw protrusion, and (3) analyze patterns of change in feeding design in the context of actinopterygian phylogeny. The mandibular lever is present in virtually all actinopterygians, and the diversity in lower jaw closing force transmission capacity, with mechanical advantage ranging from 0.04 to 0.68, has important functional consequences. A four-bar linkage for maxillary rotation arose in the Amiiformes and persists in various forms in many teleost species. Novel mechanisms for upper jaw protrusion based on this linkage for maxillary rotation have evolved independently at least five times in teleosts. The widespread anterior jaws linkage for jaw protrusion in percomorph fishes arose initially in Zeiformes and subsequently radiated into a wide range of premaxillary protrusion capabilities.
229 citations
Cites background from "Evolution of the feeding mechanism ..."
...The maxilla has a dorsal rotational joint with the neurocranium, which allows it to swing anteriorly (Lauder, 1980)....
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...Lauder (1980) investigated the feeding mechanisms of these three genera and showed that they feed primarily by rotating the skull dorsally, dropping the lower jaw, and employing hyoid depression to generate suction....
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...Lower jaw rotation is generated in all three taxa by retracting the hyoid and exerting a posterior force on the opening inlever of the mandible via the mandibulohyoid ligament (Lauder, 1980)....
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...…morphology of skull mechanisms in fishes has a long history due to broad interest in the high level of kineticism in fish skulls (Alexander, 1967; Elshoud-Oldenhave, 1979; Lauder, 1980, 1982; Liem, 1978, 1980; Osse, 1969; Waltzek and Wainwright, 2003; Westneat, 1991; Westneat and Wainwright, 1989)....
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...The homologies of the adductor mandibulae complex are detailed in Lauder (1980), and their mechanical advantage for jaw closing force ranges across an order of magnitude from Lepisosteus osseus (0.05) to Polypterus senegalus (0.42)....
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TL;DR: It is concluded that Cladistia are the sistergroup of Recent actinopterygians (Actinopteri), the two groups together comprising the Actinoperygii, and Recent chondrosteans are more closely related to higher act inopts than to cladistians.
Abstract: SYNOPSIS. The concept of the Actinopterygii as a natural group of fishes was not generally accepted until early in this century. Ever since, the characterization of the group has been blurred by the problem of cladistian (polypterid) relationships. From a review of the structure of polypterids and actinopts, it is concluded that Cladistia are the sistergroup of Recent actinopterygians (Actinopteri), the two groups together comprising the Actinopterygii. Recent chondrosteans are more closely related to higher actinopts (Neopterygii) than to cladistians. The extinct Palaeonisciformes appear to be a paraphyletic group, comprising stem-group actinopterygians ( e.g., Cheirolepts ), stem-group actinopterans ( e.g., Moythomasia ) and relatives of higher actinopterans ( e.g., Pteroniscus )
226 citations
References
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TL;DR: The conversion of the preexisting elements into a new and significantly improved cichlid adaptive complex of high selective value may have evolved by rapid steps under influence of strong selection pressure acting on the minor reconstruction of the -genotype which is involved in evolutionary changes of the pertinent ontogenetic mechanisms.
Abstract: Liem, Karel F. (Museum of Comparative Zoology, Harvard University, Cambridge, Mass. 02138) 1974. Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws. Syst. Zool. 22:425-441.-The percoid fish family Cichlidae possesses a phenomenal ability to colonize lakes and to diversify to an extent unmatched by any other vertebrate family in the presence of predator pressure and strong competition. The invading cichlids successfully occupy contiguous and occasionally overlapping adaptive zones and specialize progressively into diversified subzones, ramifying prodigiously and covering a breadth of total adaptation that would have been entirely unpredictable if we were aware only of the rudiments of the evolutionary process. This evolutionary avalanche can be attributed to the cooccurrence of a wide range of prospective adaptive zones in the lacustrine environment, and the presence of a unique morphological key innovation of maximum versatility. The new adaptive complex has been revealed in this study by electromyographic analysis synchronized with cineradiography of the cichlid pharyngeal jaw apparatus. The morphological novelty characterizing the family Cichlidae involves the development of: a synarthrosis between the lower pharyngeal jaws, a strategic shift of insertion of the two fourth levator externi muscles, and synovial joints between upper pharyngeal jaws and basicranium. This specialized, highly integrated key innovation enables the cichlids not only to transport (deglutination) but also to prepare food, freeing the premaxillary and mandibular jaws to evolve numerous specializations dealing with the collection of dramatically diverse foods. The functional integration of the innovation is so basic and its potential adaptive versatility so rich that it is maintained throughout the adaptive radiation even though numerous nondisruptive evolutionary changes do take place, providing prodigious opportunities for explosive evolution during the exploitation of rich resources of food in the lacustrine environment. The conversion of the preexisting elements into a new and significantly improved cichlid adaptive complex of high selective value may have evolved by rapid steps under influence of strong selection pressure acting on the minor reconstruction of the -genotype which is involved in evolutionary changes of the pertinent ontogenetic mechanisms. Such relatively simple evolutionary processes are probably the cause for the general phenomenon that only slight reconstructions of existing structures are necessary for successful and rapid adaptation to drastic shifts of adaptive zones.
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519 citations
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01 Jan 1974
509 citations
"Evolution of the feeding mechanism ..." refers background in this paper
...Winterbottom, R. (1974) A descriptive synonymy of the striated muscles of the Teleostei....
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506 citations