Structure and development of onychophoran eyes: what is the ancestral visual organ in arthropods?

Scarce and controversial information on visual organs and their innervation in Onychophora currently do not allow a thorough comparison with Euarthropoda. Therefore, this study sets out to provide additional data on the architecture and morphogenesis of the onychophoran visual system and to explore similarities and differences between the visual organs of onychophorans and other arthropods. Based on the new data for Epiperipatus biolleyi (Peripatidae) and Metaperipatus blainvillei (Peripatopsidae), it is suggested that the compound eyes represent an autapomorphy of Euarthropoda since similarities with the onychophoran eyes are weak or absent. Instead, the innervation from a central rather than lateral part of the brain, the presence of only one (paired or unpaired) visual center, and a similar ontogenetic origin from an ectodermal groove rather than a proliferation zone suggest homology between the onychophoran eyes and the median ocelli of euarthropods. In conclusion, I suggest that the last common ancestor of arthropods bore only one pair of ocellus-like visual organs that were modified in several arthropod lineages. This hypothesis is supported by recent paleontological data.     

Comparative anatomy of slime glands in onychophora (velvet worms)

Onychophorans use a unique hunting and defense strategy, which involves the ejection of an adhesive slime secretion produced by a pair of specialized glands. So far, a comparative study on the anatomy of these glands has not been carried out among different species. In this article, we compare anatomical features of slime glands in representatives of two major onychophoran subgroups, the Peripatopsidae and the Peripatidae, from different parts of the world. Our data show that the musculature of the reservoir is conserved whereas the composition of the secretory duct displays taxon‐specific variation. Major differences concern the arrangement of glandular endpieces, which are distributed along the duct in Peripatopsidae but condensed in numerous repeated rosettes in Peripatidae. In addition, there are differences in the attachment pattern of slime glands to the inner surface of the body wall and to the outer surface of the gut between the two major onychophoran subgroups. A tube‐like structure with a putative valve‐like function is found at the transition of the secretory duct and the reservoir in the five Peripatopsidae species studied whereas it is absent in the two representatives of Peripatidae. Our findings suggest that the arrangement of musculature in the reservoir of the slime gland has remained unchanged since the divergence of Peripatidae and Peripatopsidae, while the composition of the secretory duct has been altered in one of these groups. However, the direction of evolutionary changes in duct composition cannot be determined unambiguously due to current uncertainty regarding the phylogenetic relationships of Onychophora. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system

The neuroectoderm of the Euperipatoides kanangrensis embryo becomes distinguishable during germ band formation when the antennal segment is evident externally. During later stages of development, the neuroectoderm proliferates extensively and, at the anterior part of the head, newly-formed neuron precursor cells occupy most of the volume. The antenna forms from the dorsolateral side of the anterior somite. The antenna has no neuroectoderm of its own at the onset of its formation, but instead, neurons migrate out to the appendage from the nearby region of the developing brain. When the antennal tract is formed it is positioned horizontally in the brain, in line with the antennal commissure. Only later, and coincidentally with the anterior repositioning of the antenna, is the tract's distal part bent anteriorly and positioned laterally. The eye starts to develop posteriorly to the antenna and the antennal commissure. This suggests that the segment(s) associated with the onychophoran eye and antenna are not serially homologous with segments carrying equivalent structures within the Euarthropoda. Evidence is presented to further support the presence of a terminal mouth in the ground plan of the Onychophora and, hence, an acron may not exist in the arthropod clade.     

Unexplored Character Diversity in Onychophora (Velvet Worms): A Comparative Study of Three Peripatid Species

Low character variation among onychophoran species has been an obstacle for taxonomic and phylogenetic studies in the past, however we have identified a number of new and informative characters using morphological, molecular, and chromosomal techniques. Our analyses involved a detailed examination of Epiperipatus biolleyi from Costa Rica, Eoperipatus sp. from Thailand, and a new onychophoran species and genus from Costa Rica, Principapillatus hitoyensis gen. et sp. nov.. Scanning electron microscopy on embryos and specimens of varying age revealed novel morphological characters and character states, including the distribution of different receptor types along the antennae, the arrangement and form of papillae on the head, body and legs, the presence and shape of interpedal structures and fields of modified scales on the ventral body surface, the arrangement of lips around the mouth, the number, position and structure of crural tubercles and anal gland openings, and the presence and shape of embryonic foot projections. Karyotypic analyses revealed differences in the number and size of chromosomes among the species studied. The results of our phylogenetic analyses using mitochondrial COI and 12S rRNA gene sequences are in line with morphological and karyotype data. However, our data show a large number of unexplored, albeit informative, characters in the Peripatidae. We suggest that analysing these characters in additional species would help unravel species diversity and phylogeny in the Onychophora, and that inconsistencies among most diagnostic features used for the peripatid genera in the literature could be addressed by identifying a suite of characters common to all peripatids.     

A world checklist of Onychophora (velvet worms), with notes on nomenclature and status of names

Currently, the number of valid species of Onychophora is uncertain. To facilitate taxonomic work on this understudied animal group, we present an updated checklist for the two extant onychophoran subgroups, Peripatidae and Peripatopsidae, along with an assessment of the status of each species. According to our study, 82 species of Peripatidae and 115 species of Peripatopsidae have been described thus far. However, among these 197 species, 20 are nomina dubia due to major taxonomic inconsistencies. Apart from nomina dubia, many of the valid species also require revision, in particular representatives of Paraperipatus within the Peripatopsidae, and nearly all species of Peripatidae. In addition to extant representatives, the record of unambiguous fossils includes three species with uncertain relationship to the extant taxa. For all species, we provide a list of synonyms, information on types and type localities, as well as remarks on taxonomic and nomenclatural problems and misspellings. According to recent evidence of high endemism and cryptic speciation among the Peripatidae and Peripatopsidae, previous synonyms are revised. Putative mutations, subspecies and variations are either raised to the species status or synonymised with corresponding taxa. In our revised checklist, we follow the rules and recommendations of the International Code of Zoological Nomenclature to clarify previous inconsistencies.     

Further structures in the jaw apparatus of Limnognathia maerski (Micrognathozoa), with notes on the phylogeny of the Gnathifera

The jaws of Limnognathia maerski, Micrognathozoa, were investigated with light- and scanning electron microscopy. The study yielded several new structures and sclerites, including the ventral part of main jaw, the pharyngeal lamellae, the manus, the dorsal and ventral fibularium teeth, and a reinterpretation of the fibularium compartmentalization. Furthermore, it was shown that several jaw elements are composed of densely packed rods. Comparison with Rotifera and Gnathostomulida suggested that the micrognathozoan main jaw is homologous with the rotifer incus and the gnathostomulid articularium and that the pseudophalangids (the ventral jaws) and their associated sclerites correspond to the rotifer mallei. These results imply that Micrognathozoa is more closely related to Rotifera than to Gnathostomulida.     

Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea)

Protrusion of the jaws during feeding is common in Batoidea (rays, skates, sawfishes, and guitarfishes), members of which possess a highly modified jaw suspension. The lesser electric ray, Narcine brasiliensis, preys primarily on polychaete annelids using a peculiar and highly derived mechanism for jaw protraction. The ray captures its prey by protruding its jaws beneath the substrate and generating subambient buccal pressure to suck worms into its mouth. Initiation of this protrusion is similar to that proposed for other batoids, in that the swing of the distal ends of the hyomandibulae is transmitted to Meckel's cartilage. A "scissor-jack" model of jaw protrusion is proposed for Narcine, in which the coupling of the upper and lower jaws, and extremely flexible symphyses, allow medial compression of the entire jaw complex. This results in a shortening of the distance between the right and left sides of the jaw arch and ventral extension of the jaws. Motion of the skeletal elements involved in this extreme jaw protrusion is convergent with that described for the wobbegong shark, Orectolobus maculatus. Narcine also exhibits asymmetrical protrusion of the jaws from the midline during processing, accomplished by unequal depression of the hyomandibulae. Lower jaw versatility is a functional motif in the batoid feeding mechanism. The pronounced jaw kinesis of N. brasiliensis is partly a function of common batoid characteristics: euhyostylic jaw suspension (decoupling the jaws from the hyoid arch) and complex and subdivided cranial musculature, affording fine motor control. However, this mechanism would not be possible without the loss of the basihyal in narcinid electric rays. The highly protrusible jaw of N. brasiliensis is a versatile and maneuverable feeding apparatus well-suited for the animal's benthic feeding lifestyle.     

Origin and differentiation of nephridia in the Onychophora provide no support for the Articulata

Comparative morphology currently permits no unambiguous decision on the primary homology of the nephridia of Annelida and Arthropoda. In order to obtain additional information on this subject, ultrastructure of morphogenesis and further differentiation of nephridia was studied in the onychophoran Epiperipatus biolleyi (Peripatidae). In this species, the nephridial anlage develops by reorganization of the lateral portion of the embryonic coelomic wall that initially gives rise to a ciliated canal. All other structural components, including the sacculus, merge after the nephridial anlage has been separated from the remaining mesodermal tissue. The nephridial sacculus does not represent a ‘persisting coelomic cavity’, since it arises de novo during embryogenesis. There is no evidence for ‘nephridioblast‘ cells participating in the nephridiogenesis of Onychophora, which is in contrast to the general mode of nephridial formation in Annelida. Available data on nephridiogenesis in euarthropods (Chelicerata, Myriapoda, Crustacea, and Hexapoda) also provide no evidence for nephridia of Annelida and Arthropoda being a synapomorphy of these taxa. These findings accordingly weaken the traditional Articulata hypothesis.     

Claw retraction and protraction in the carnivora: Skeletal microvariation in the phalanges of the Felidae

All carnivorans retract and protract their claws. In felids and some viverrids the claws of digits II through V of both the manus and pes have a larger arc of rotation than those of other carnivorans; the claws retract to the lateral side of the middle phalanx rather than onto its dorsal surface as in most other carnivorans. This condition should be termed hyper-retraction. Morphological features of the middle and distal (ungual) phalanges that have been purported to be necessary for hyper-retraction in felids vary considerably among digits within the manus and pes. These features include the lateral projection of the distal head and the asymmetry of the shaft of the middle phalanx, and the oblique orientation of the articular surface on the distal phalanx. None of these features is necessary in every instance for hyperretraction, and some of the variation in these features is associated instead with protraction. Differences among digits in the orientation of the articular surface on the distal phalanx are associated with differences in the degree to which the claws must move laterally to rotate from the protracted to the retracted position. Differences in the orientation of the distal head on the middle phalanx are associated with the spreading of the claws during protraction. The manual claws are hook-shaped, whereas the pedal claws are more blade-like; this morphological difference is associated with differences in function between the manus and pes. In the manus the medial claws have a larger radius of curvature and a smaller angle of arc as compared to the more lateral claws; in the pes, the claws on digits III and IV have larger radii of curvature and smaller angles of arc. Digit I of the manus lacks the hyper-retraction mechanism; nonetheless, this digit shares many of the attributes that are associated with this mechanism. © 1996 Wiley-Liss, Inc.     

Adaptation in the jaws of flatfish (Pleuronectiformes)

The structure and mechanisms of the jaws of 18 species of flatfish have been investigated. Clear adaptations to different modes of feeding were found. The mechanisms of the jaws of Soleidae, Cynoglossidae, and Rhombosoleinae are highly specialized and the representatives of the two latter groups have some interesting jaw muscles of doubtful homology.     

Anatomy and Ultrastructure of Ventral Pharyngeal Organs and their Phylogenetic Importance in Polychaeta (Annelida). IV. The Pharynx and Jaws of the Dorvilleidae

An anatomical and ultrastructural investigation of the ventral pharyngeal organ, jaws and replacement of jaws was carried out in Ophryotrocha gracilis and Protodorvillea kefersteini (Dorvilleidae). The pharynx exhibits the following features: jaw apparatus present, consisting of paired mandibles and rows of maxillary plates, the latter are fused to form a single piece; cuticular jaws electron-dense, in P. kefersteini with collagen fibres; muscle bulbus solid, composed of muscle cells only; parallel running myofilaments, centrally located mitochondria and nuclei, bulbus epithelium containing the mandibles and gland cells, maxillary plates lying on folds corresponding to a tongue-like organ, connected with mandibles by longitudinal investing muscles; numerous gland cells not united to distinct salivary glands. Development of jaw replacements occurs in epithelial cavities beside the functional maxillae. Shape of maxillary plates is preformed by microvilli carrying cell processes. Maxilloblasts change their shape during the development. Synapomorphic structures occurring in ventral pharyngeal organs of other species outside the Eunicea are not present and even the closely related Dinophilidae exhibit a completely different pharyngeal organ. Therefore, convergent evolution of these organs is the most probable explanation. These findings do not agree with the hypothesis of the homology of the ventral pharyngeal organs in the Polychaeta.     

Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea

The design of minimum-weight structures that retain their integrity under dynamic loading regimes has long challenged engineers. One solution to this problem found in both human and biological design is the optimization of weight and strength by hollowing a structure and replacing its inner core with supportive struts. In animals, this design is observed in sand dollar test, avian beak, and the cancellous bone of tetrapod limbs. Additionally, within the elasmobranch fishes, mineralized trabeculae (struts) have been reported in the jaws of durophagous myliobatid stingrays (Elasmobranchii: Batoidea), but were believed to be absent in basal members of the batoid clade. This study, however, presents an additional case of batoid trabeculation in the lesser electric ray, Narcine brasiliensis (Torpediniformes). The trabeculae in these species likely play different functional roles. Stingrays use their reinforced jaws to crush bivalves, yet N. brasiliensis feeds by ballistically protruding its jaws into the sediment to capture polychaetes. In N. brasiliensis, trabeculae are localized to areas likely to experience the highest load: the quadratomandibular jaw joints, hyomandibular-cranial joint, and the thinnest sections of the jaws immediately lateral to the symphyses. However, the supports perform different functions dependent on location. In regions where the jaws are loaded transversely (as in durophagous rays), "load leading" trabeculae distribute compressive forces from the cortex through the lumen of the jaws. In the parasymphyseal regions of the jaws, "truss" trabeculae form cross-braces perpendicular to the long axes of the jaws. At peak protrusion, the jaw arch is medially compressed and the jaw loaded axially such that these trabeculae are positioned to resist buckling associated with excavation forces. "Truss" trabeculae function to maintain the second moment of area in the thinnest regions of the jaws, illustrating a novel function for batoid trabeculation. Thus, this method of structural support appears to have arisen twice independently in batoids and performs strikingly different ecological functions associated with the distribution of extreme loading environments.     

Ontogeny of the jaw apparatus and suspensorium of the Tetraodontiformes

Konstantinidis, P. and Johnson, G. David 2012. Ontogeny of the jaw apparatus and suspensorium of the Tetraodontiformes. —Acta Zoologica (Stockholm) 93 : 351–366. The jaw apparatus and suspensorium of adult Tetraodontiformes are well adapted to a durophagous feeding habit. Anatomical indicators are the short, stout jaws and a suspensorium in which the quadrate lies in the same vertical plane as the autopalatine. In contrast, the palatoquadrate of larval Tetraodontiformes generally resembles that of larval percomorphs – a more posteriorly positioned quadrate and a slender and long Meckelian cartilage. Among Tetraodontiformes, the Triacanthodidae retain a protrusible upper jaw and a versatile suspensorium. The jaws of the Balistoidei have greater mobility achieved by a reduced autopalatine that has lost its bony contact with the suspensorium. In contrast to the Balistoidei, the beak‐like jaws of the Tetraodontoidei lack individual teeth in the biting part of the jaws. The autopalatine is enlarged, which results in immobilization of the ethmopalatine articulation. The Ostraciidae are exceptional in having the distal part of the autopalatine reduced, while the proximal part remains attached to the suspensorium.     

Mouthparts in Leptotrombidium larvae (Acariformes: Trombiculidae)

Mouthparts of Leptotrombidium larvae (Acariformes: Trombiculidae), potential vectors of tsutsugamushi disease agents, were studied in detail using light microscopy, scanning electron microscopy, and transmission electron microscopy. The mouthparts incorporated within the pseudotagma gnathosoma are composed of the infracapitulum ventrally and the chelicerae dorsally. The ventral wall of the infracapitulum is formed by a wide mentum posteriorly and a narrowed malapophysis anteriorly. The malapophysis firmly envelops the distal cheliceral portions by its lateral walls. The lateral lips of the malapophysis are flexible structures hiding the cheliceral blades in inactive condition and turning back forming a type of temporary sucker closely applied to the host skin during feeding. The roof of the infracapitulum is formed by a weakly sclerotized labrum anteriorly and a cervix with the capitular apodemes extending posteriorly. The labral muscles are lacking. The capitular apodemes serve as origin for pharyngeal dilators running to the dorsal wall of the pharynx fused with the bottom of the infracapitulum. The basal cheliceral segments are separated from each other besides the very posterior portions where they are movably joined by the inner walls. The sigmoid pieces serve for insertion of the cheliceral elevators originating at the posterior portions of the basal segments. The movable digits reveal the solid basal sclerite and the cheliceral blade curved upward with a tricuspid cap on its tip. Dendrites of nerve cells run along the digits to their tips. The ganglia are placed within the basal segments just behind the movable digits. The chelicerae also reveal well developed flexible fixed digits overhanging the basal portions of the blades. The gnathosoma possesses several sets of extrinsic muscles originating at the scutum and at the soft cuticle behind it. Laterally, the gnathosoma bears five‐segmented palps with a trifurcate palpal claw. J. Morphol. 277:424–444, 2016. © 2016 Wiley Periodicals, Inc.     

The hierarchical basis of serial homology and evolutionary novelty

Given the pervasiveness of gene sharing in evolution and the extent of homology across the tree of life, why is everything not homologous with everything else? The continuity and overlapping genetic contributions to diverse traits across lineages seem to imply that no discrete determination of homology is possible. Although some argue that the widespread overlap in parts and processes should be acknowledged as “partial” homology, this threatens a broad base of presumed comparative morphological knowledge accepted by most biologists. Following a long scientific tradition, we advocate a strategy of “theoretical articulation” that introduces further distinctions to existing concepts to produce increased contrastive resolution among the labels used to represent biological phenomena. We pursue this strategy by drawing on successful patterns of reasoning from serial homology at the level of gene sequences to generate an enriched characterization of serial homology as a hierarchical, phylogenetic concept. Specifically, we propose that the concept of serial homology should be applied primarily to repeated but developmentally individualized body parts, such as cell types, differentiated body segments, or epidermal appendages. For these characters, a phylogenetic history can be reconstructed, similar to families of paralogous genes, endowing the notion of serial homology with a hierarchical, phylogenetic interpretation. On this basis, we propose a five-fold theoretical classification that permits a more fine-grained mapping of diverse trait-types. This facilitates answering the question of why everything is not homologous with everything else, as well as how novelty is possible given that any new character possesses evolutionary precursors. We illustrate the fecundity of our account by reference to debates over insect wing serial homologs and vertebrate paired appendages.     

Jaw structures and movements in higher teleostean fishes

All of the diverse jaw structures in higher teleosts appear to be modifications of a single basal type and are treated as such. Only some of the principal variants are discussed. Though the two jaws act as a coordinated unit during feeding, their movements are different. The upper and lower jaws are discussed separately. In the upper jaw the principal concern is with the various types of premaxillary protrusion and with the secondary development in some groups of a rocking premaxilla. For the lower jaw most of the account is devoted to the repeated differentiation of movements in its anterior and posterior sections. The paper concludes with comments on the jaw apparatus as a functional unit and its evolution in higher teleosts.     

How to recognize in situ fossil cephalopods: evidence from experiments with modern Nautilus

Field and flume experiments with modern Nautilus pompilius establish two prerequisites to recognize in situ preservation of fossil cephalopod shells (soft parts were within body chamber in situ at the time of fossilization): occurrence of the upper jaw within the body chamber and the position of jaws within the body chamber. Morphology of shells and jaws in modern and fossil nautiloids is so similar that these prerequisites can be applied for fossil nautiloids and provide implications for ammonoids. The upper jaws of Nautilus start to move at a water velocity of > 0.2 m/s, when the shells are reoriented with the aperture downstream; jaws are therefore unlikely to be secondarily deposited near the shell aperture by bottom currents. The lower jaws, moved at the velocity of > 0.1 m/s, can be deposited around the shell aperture by weak current (0.1–0.2 m/s in velocity), but never enter the inside of body chamber. Neither jaw is likely to be separately and selectively displaced from the inside of the body chamber through scavenging of the soft parts by burrowing infaunal animals. An upper jaw preserved inside the body chamber, together with a lower jaw, is thus a reliable indicator of in situ preservation; a sole lower jaw preserved around the shell aperture is likely to be secondarily deposited. Sedimentary structures inferring rapid burial events and jaw size are useful as additional evidence. Smaller jaws were more likely to be displaced from the body chamber by scavenging by infaunal animals after in situ burial, so that smaller jaws preserved within the body chamber suggest less scavenging. These findings are crucial to interpreting the taphonomic history and palaeo-ecology of fossil cephalopods.     

Musculoskeletal underpinnings to differences in killing behavior between North American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae)

Accipiters (Accipiter spp.) and falcons (Falco spp.) both use their feet to seize prey, but falcons kill primarily with their beaks, whereas accipiters kill with their feet. This study examines the mechanistic basis to differences in their modes of dispatching prey, by focusing on the myology and biomechanics of the jaws, digits, and distal hindlimb. Bite, grip, and distal hindlimb flexion forces were estimated from measurements of physiological cross-sectional area (PCSA) and indices of mechanical advantage (MA) for the major jaw adductors, and digit and tarsometatarsal flexors. Estimated bite force, total jaw adductor PCSA, and jaw MA (averaged over adductors) tended to be relatively and absolutely greater in falcons, reflecting their emphasis on biting for dispatching their prey. Differences between genera in estimated grip force, total digit flexor PCSA, and digit MA (averaged over inter-phalangeal joints and digits) were not as clear-cut; each of these parameters scaled positively allometric in accipiters, which may reflect the scaling of both prey size, and the proportion of mammalian prey consumed by this lineage with increasing body size. Estimated tarsometatarsal force was greater in falcons than in accipiters, due to their greater MA, which may reflect selection for incurring greater forces during prey strikes. Conversely, the comparatively lower tarsometatarsal MA in accipiters reflects their capacity for greater foot speed potentially necessary for grasping elusive prey. Thus, this study elucidates how differences in jaw and hindlimb musculoskeletal morphology of accipiters and falcons are reflected in differences in their killing modes, and through differences in their force-generating capacities.     

Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda)

The great barracuda, Sphyraena barracuda, is a voracious marine predator that captures fish with a swift ram feeding strike. While aspects of its ram feeding kinematics have been examined, an unexamined aspect of their feeding strategy is the bite mechanism used to process prey. Barracuda can attack fish larger than the gape of their jaws, and in order to swallow large prey, can sever their prey into pieces with powerful jaws replete with sharp cutting teeth. Our study examines the functional morphology and biomechanics of 'ram-biting' behavior in great barracuda where the posterior portions of the oral jaws are used to slice through prey. Using fresh fish and preserved museum specimens, we examined the jaw mechanism of an ontogenetic series of barracuda ranging from 20 g to 8.2 kg. Jaw functional morphology was described from dissections of fresh specimens and bite mechanics were determined from jaw morphometrics using the software MandibLever (v3.2). High-speed video of barracuda biting (1500 framess(-1)) revealed that prey are impacted at the corner of the mouth during capture in an orthogonal position where rapid repeated bites and short lateral headshakes result in cutting the prey in two. Predicted dynamic force output of the lower jaw nearly doubles from the tip to the corner of the mouth reaching as high as 58 N in large individuals. A robust palatine bone embedded with large dagger-like teeth opposes the mandible at the rear of the jaws providing for a scissor-like bite capable of shearing through the flesh and bone of its prey.