Functional coupling in the evolution of suction feeding and gill ventilation of sculpins (Perciformes: Cottoidei).

Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems.

Benthic walking, bounding, and maneuvering in flatfishes (Pleuronectiformes: Pleuronectidae): New vertebrate gaits.

Video-based observations of voluntary movements reveal that six species of pleuronectid flatfishes use sequential portions of long-based dorsal and anal fins as "feet" (hereafter, fin-feet) to move on the substrate. All six species used a gait that we term "walking," which produced constant forward movement, and several of these species also used a second gait that we call "bounding" for intermittent movements over the substrate. We selected Pacific Sand Sole, Psettichthys melanostictus, and English Sole, Parophrys vetulus, for kinematic analyses of these two gaits. Psettichthys melanostictus consistently used walking for benthic locomotion; Parophrys vetulus primarily used a bounding gait. During forward walking, a fin ray swings up off the substrate, protracts and converges with neighboring fin rays to contribute to a fin-foot. The fin-foot pushes down on the substrate and rotates posteriorly by sequential recruitment of fin rays, a pattern known as a metachronal wave. As one fin-foot passes off the posterior end of the fin, a new fin-foot forms anteriorly. During bounding, undulations of the body and tail assist one or two waves of fin-feet, producing rapid but intermittent forward acceleration of the body. Flatfishes also use fin-feet to maneuver on the substrate. The Starry Flounder, Platichthys stellatus, performs near zero displacement rotation by running waves of fin-feet in opposing directions along the dorsal and anal fins. Although other teleosts use specialized pectoral fin rays for bottom walking (e.g., Sea Robins: Triglidae), the duplication of structures and patterns of movement in the median fins of flatfishes more closely resembles metachronal motions of millipede feet or the parapodia of polychaete worms. Sequential use of median fin rays in flatfishes resembles that of other teleosts that swim with elongate median fins, including Amiiformes, Gymnotiformes, and some Tetraodontiformes, but flatfishes offer a novel form of substrate locomotion based on dorsal and anal fins.

Localization and partial characterization of melatonin receptors in amphioxus, hagfish, lamprey, and skate.

Through its secretion of melatonin, the pineal complex of vertebrates exerts a range of physiological effects including regulation of circadian rhythms, seasonal reproduction, metamorphosis, and body color change. Little is known about phylogenetic differences in the distribution and characteristics of melatonin binding sites in fishes. We used in vitro autoradiography to examine binding of [2-125I]iodomelatonin (IMEL) in 20-micron frozen sections of amphioxus (Branchiostoma lanceolatum), Atlantic hagfish (Myxine glutinosa), larval and adult lamprey (Petromyzon marinus), little skate (Raja erinacea), and rainbow trout (Oncorhynchus mykiss). Tissue was incubated with IMEL in the presence or absence of unlabeled melatonin (1 muM, in order to assess nonspecific binding). A concentration of 32 pM IMEL was used for single point assays and competition studies. No specific binding was found in hagfish or amphioxus, which lack a pineal complex. In the optic tecta of lamprey, skate, and trout, IMEL binding is highly specific (melatonin >> N-acetylserotonin > 5- methoxytryptophol >> serotonin). Scatchard analysis revealed that the tectal binding sites are of high affinity (Kd = 36, 38, and 50 pM) and low capacity (Bmax = 8.1, 19.8, and 21.8 fmol/mg protein) in lamprey, skate, and trout, respectively. In adult lampreys, intense specific IMEL binding is found in the optic tectum (layer I > II > III) and preoptic nucleus (pars parvocellularis > magnocellularis). Binding was less intense and consistent in the same areas of ammocoete brain. In skates and trout, intense specific binding is found in optic tectum, lateral geniculate body, diencephalic preoptic and suprachiasmatic nuclei, basal hypothalamus, and the medial pallium. These results indicate that specific melatonin binding sites are present in all craniate taxa examined except in hagfish. Although we cannot rule out the possibility that melatonin receptors are secondarily lost in hagfish, their absence in amphioxus makes this unlikely. We speculate that melatonin actions in early vertebrates may have included regulation of visual and endocrine responses to light.

Cranial nerves of the coelacanth, Latimeria chalumnae [Osteichthyes: Sarcopterygii: Actinistia], and comparisons with other craniata.

We reconstructed the cranial nerves of a serially sectioned prenatal coelacanth, Latimeria chalumnae. This allowed us to correct several mistakes in the literature and to make broad phylogenetic comparisons with other craniates. The genera surveyed in our phylogenetic analysis were Eptatretus, Myxine, Petromyzon, Lampetra, Chimaera, Hydrolagus, Squalus, Mustelus, Polypterus, Acipenser, Lepisosteus, Amia, Neoceratodus, Protopterus, Lepidosiren, Latimeria and Ambystoma. Cladistic analysis of our data shows that Latimeria shares with Ambystoma two characters of the cranial nerves. Our chief findings are: 1) Latimeria possesses an external nasal papilla and pedunculated olfactory bulbs but lacks a discrete terminal nerve. In other respects its olfactory system resembles the plesiomorphic pattern for craniates. 2) The optic nerve is plicated, a character found in many but not all gnathostomes. Latimeria retains an interdigitated partial decussation of the optic nerves, a character found in all craniates surveyed. 3) The oculomotor nerve supplies the same extrinsic eye muscles as in lampreys and gnathostomes. As in gnathostomes generally, Latimeria has a ciliary ganglion but its cells are located intracranially in the root of the oculomotor nerve, and their processes reach the eye via oculomotor and profundal rami. 4) The trochlear nerve supplies the superior oblique muscle as in all craniates that have not secondarily reduced the eye and its extrinsic musculature. 5) The profundal ganglion and ramus are entirely separate from the trigeminal system, with no exchange of fibers. This character has an interesting phylogenetic distribution: in hagfishes, lampreys, lungfishes and tetrapods, the profundal and trigeminal ganglia are fused, whereas in other taxa surveyed the ganglia are separate. The principal tissues innervated by the profundal nerve are the membranous walls of the tubes of the rostral organ. 6) As in lampreys and gnathostomes, the trigeminal nerve has maxillary and mandibular rami. Unlike all other gnathostomes surveyed, the trigeminal nerve of Latimeria lacks a sizable superficial ophthalmic ramus. Thus, Latimeria lacks the well-developed superficial ophthalmic complex reported in most other fishes. As in gnathostomes generally, the maxillary ramus of the trigeminal nerve fuses with the buccal ramus of the anterodorsal lateral line nerve to form the buccal+maxillary complex. We reject the term 'Gasserian ganglion', which is often applied to the fused profundal and trigeminal ganglion of tetrapods. 7) The abducent nerve innervates not only the lateral rectus muscle (a character common to myopterygians) but also the basicranial muscle. As we previously reported, it is probable that the basicranial muscle of Latimeria is homologous to the ocular retracter muscle of amphibians.(ABSTRACT TRUNCATED AT 400 WORDS)

Structure and function of the external gill filaments of embryonic skates (Raja erinacea).

We have investigated structure and function of the external gill filaments, which occur transiently in the embryonic little skate, Raja erinacea. Approximately 25-30 days after spawning (body mass 0.03-0.05 g) external gill filaments appear as an outgrowth from the caudal side of the gill arches. These filaments are thread-like, each containing one afferent and one efferent blood vessel, and by day 70-75 (body mass 0.4-0.5 g) they reach their maximum size at a length of about 1 cm and a blood vessel diameter of 70-80 microns. Subsequent resorption of the filaments is characterized by a decrease in both length and diameter of the blood vessel. By day 90-95 (body mass 0.9-1.0 g) the external gill filaments are completely resorbed and replaced by internal gills. Blood velocity, measured in these external filaments, increased with development from 0.1 mm.sec-1 to about 0.7 min.sec-1, and decreased again during resorption. Blood flow, calculated therefrom with blood vessel diameter, showed a similar maximum curve. A model analysis supports the hypothesis that in a full grown filament respiratory gas exchange is mainly perfusion-limited and can contribute significantly to the total oxygen uptake of the embryo. Analysis of the results indicates, however, that the gill filaments are not adequate as a gas exchange organ for later developmental stages.

Early development of the actinopterygian head. I. External development and staging of the paddlefish Polyodon spathula.

A large sample of embryological material of the North American paddlefish Polyodon spathula (Acipenseriformes: Polyodontidae) confirms that early development in Polyodon is very similar to that reported for the sister group of Polyodontidae, the sturgeons (Acipenseridae). Polyodon illustrates many basic aspects of acipenseriform (and actinopterygian) head development that have not been adequately described. In this paper, we provide an overview of external features of cranial development using scanning electron microscopy. The observations are correlated with staging schemes previously proposed for paddlefishes and other acipenseriforms. Events that occur after the start of neurulation (stage 19) to the start of feeding (stage 46) are emphasized. New information on the structure and folding of the mandibular and hyoid segments permits an understanding of the early development of the pharyngeal region. In addition, we offer new descriptions of the hatching gland, the olfactory organ, the sensory barbel, and the initiation of paddle outgrowth. We also comment on the mode of origin of the hypophysis, and refute the notion that it is derived from the lips of the anterior neuropore as suggested in older literature. This information sets the stage for future comparative and experimental studies of the embryology of basal actinopterygians. © 1992 Wiley-Liss, Inc.

Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi).

The feeding mechanism of the South American lungfish, Lepidosiren paradoxa retains many primitive teleostome characteristics. In particular, the process of initial prey capture shares four salient functional features with other primitive vertebrates: 1) prey capture by suction feeding, 2) cranial elevation at the cranio-vertebral joint during the mouth opening phase of the strike, 3) the hyoid apparatus plays a major role in mediating expansion of the oral cavity and is one biomechanical pathway involved in depressing the mandible, and 4) peak hyoid excursion occurs after maximum gape is achieved. Lepidosiren also possesses four key morphological and functional specializations of the feeding mechanism: 1) tooth plates, 2) an enlarged cranial rib serving as a site for the origin of muscles depressing the hyoid apparatus, 3) a depressor mandibulae muscle, apparently not homologous to that of amphibians, and 4) a complex sequence of manipulation and chewing of prey in the oral cavity prior to swallowing. The depressor mandibulae is always active during mouth opening, in contrast to some previous suggestions. Chewing cycles include alternating adduction and transport phases. Between each adduction, food may be transported in or out of the buccal cavity to position it between the tooth plates. The depressor mandibulae muscle is active in a double-burst pattern during chewing, with the larger second burst serving to open the mouth during prey transport. Swallowing is characterized by prolonged activity in the hyoid constrictor musculature and the geniothoracicus. Lepidosiren uses hydraulic transport achieved by movements of the hyoid apparatus to position prey within the oral cavity. This function is analogous to that of the tongue in many tetrapods.