The Neuroecology of the Elasmobranch Electrosensory World: Why Peripheral Morphology Shapes Behavior

The adaptations of elasmobranch sensory systems can be studied by linking the morphological structure with the natural behavior and ecology of the organism. This paper presents the first step in a neuroecological approach to interpret the spatial arrangement of the electrosensory ampullary organs in elasmobranch fishes. A brief review of the structure and function of the ampullae of Lorenzini is provided for interpretation of the organ system morphology in relation to the detection of dipole and uniform electric fields. The spatial projections of canals from discrete ampullary clusters were determined for the barndoor skate, Raja laevis, based upon a published figure in Raschi (1986), and measured directly from the head of the white shark, Carcharodon carcharias. The dorsoventrally flattened body of the skate restricts the projections of long canals to the horizontal plane. There is a distinct difference between dorsal and ventral projection patterns in all groups. Notable within-cluster features include a relatively long canal subgroup in the dorsal superficial ophthalmic (SOd) and dorsal hyoid (HYOd) clusters that are oriented parallel (bidirectionally) to the longitudinal axis of the body. It is postulated that this subgroup of canals may be important for detection and orientation to weak uniform fields. Ventral canal projections in the skate are primarily lateral, with the exception of the hyoid (HYOv) that also projects medially. This wide dispersion may function for the detection of prey located below the body and pectoral fins of the skate, and may also be used for orientation behavior. The mandibular canals located near the margin of the lower jaw (of both study species) are ideally positioned for use during prey manipulation or capture, and possibly for interspecific courtship or biting. The head of the white shark, which lacks the hyoid clusters, is ovoid in cross section and thus ampullary canals can project into three-dimensional space. The SOd and superficial ophthalmic ventral (SOv) clusters show strong rostral, dorsal and lateral projection components, whereas the SOv also detects rostral fields under the snout. In the sagittal plane, the SOv and SOd have robust dorsal projections as well as ventral in the SOv. Most notable are canal projections in the white shark buccal (BUC) ampullary cluster, which has a radial turnstile configuration on the ventrolateral side of the snout. The turnstile design and tilt between orthogonal planes indicates the white shark BUC may function in detection of uniform fields, including magnetically induced electric fields that may be used in orientation behaviors. These data can be used in future neuroecology behavioral performance experiments to (1) test for possible specializations of cluster groups to different natural electric stimuli, (2) the possibility of specialized canal subgroups within a cluster, and (3) test several models of navigation that argue for the use of geomagnetically induced electric cues.     

Using a Comparative Species Approach to Investigate the Neurobiology of Paternal Responses

A goal of behavioral neuroscience is to identify underlying neurobiological factors that regulate specific behaviors. Using animal models to accomplish this goal, many methodological strategies require invasive techniques to manipulate the intensity of the behavior of interest (e.g., lesion methods, pharmacological manipulations, microdialysis techniques, genetically-engineered animal models). The utilization of a comparative species approach allows researchers to take advantage of naturally occurring differences in response strategies existing in closely related species. In our lab, we use two species of the Peromyscus genus that differ in paternal responses. The male California deer mouse (Peromyscus californicus) exhibits the same parental responses as the female whereas its cousin, the common deer mouse (Peromyscus maniculatus) exhibits virtually no nurturing/parental responses in the presence of pups. Of specific interest in this article is an exploration of the neurobiological factors associated with the affiliative social responses exhibited by the paternal California deer mouse. Because the behavioral neuroscience approach is multifaceted, the following key components of the study will be briefly addressed: the identification of appropriate species for this type of research; data collection for behavioral analysis; preparation and sectioning of the brains; basic steps involved in immunocytochemistry for the quantification of vasopressin-immunoreactivity; the use of neuroimaging software to quantify the brain tissue; the use of a microsequencing video analysis to score behavior and, finally, the appropriate statistical analyses to provide the most informed interpretations of the research findings.     

Sex Allocation in Lythrypnus (Gobiidae): Variations on a Hermaphroditic Theme

The gonadal sexual patterns of three Atlantic/Caribbean Lythrypnus (L. nesiotes, L. phorellus, L. spilus) are described, based on histological examination, and compared with previously described sexual patterns of L. dalli and L. zebra, from the eastern Pacific. Overall, there was striking similarity in the sexual patterns of all the species; each exhibited simultaneous hermaphroditism with a high degree of variability in allocation to male tissue among individuals. Among the five species whose sexual patterns are described, at least three distinct sexual patterns were identified. Lythrypnus dalli has an allocation pattern distinct from the other species, with populations consisting of primarily pure females, strongly female-biased hermaphrodites and pure males. Lythrypnus nesiotes was also found to be distinct from the other species, consisting primarily of pure females and strongly female-biased hermaphrodites and male-biased individuals (mean allocation to male tissue = 75%). In contrast to L. dalli, L. nesiotes had no pure males. Indeed, no other species examined included pure males. L. phorellus, L. spilus and L. zebra had much more intermediate allocation patterns than either L. dalli or L. nesiotes. Most individuals were female biased (<10% male tissue), and there were significant numbers of individuals with intermediate allocation (10–90% male). L. zebra differed somewhat from L. phorellus and L. spilus in that more strongly male-biased individuals were common in the sample (i.e., ranging in allocation from 90 to 98% male); this difference was not statistically compelling. This marked variation in allocation among closely related species suggests Lythrypnus is a useful model system to explore factors affecting allocation. For example, models developed for simultaneous hermaphrodites and appropriate for Lythrypnus predict that pure sexed individuals will be more common at higher density (e.g., because mating success is more certain). The observed interspecific variation supports this prediction – both L. dalli and L. nesiotes occur at high density and have the most extreme allocation patterns, whereas L. phorellus, L. spilus, and L. zebra occur at lower density and have more intermediate allocation patterns.     

Structures and Mechanisms of Viral Membrane Fusion Proteins: Multiple Variations on a Common Theme

Recent work has identified three distinct classes of viral membrane fusion proteins based on structural criteria. In addition, there are at least four distinct mechanisms by which viral fusion proteins can be triggered to undergo fusion-inducing conformational changes. Viral fusion proteins also contain different types of fusion peptides and vary in their reliance on accessory proteins. These differing features combine to yield a rich diversity of fusion proteins. Yet despite this staggering diversity, all characterized viral fusion proteins convert from a fusion-competent state (dimers or trimers, depending on the class) to a membrane-embedded homotrimeric prehairpin, and then to a trimer-of-hairpins that brings the fusion peptide, attached to the target membrane, and the transmembrane domain, attached to the viral membrane, into close proximity thereby facilitating the union of viral and target membranes. During these conformational conversions, the fusion proteins induce membranes to progress through stages of close apposition, hemifusion, and then the formation of small, and finally large, fusion pores. Clearly, highly divergent proteins have converged on the same overall strategy to mediate fusion, an essential step in the life cycle of every enveloped virus.     

Phylogenetic dating and characterization of gene duplications in vertebrates: the cartilaginous fish reference

Vertebrates originated in the lower Cambrian. Their diversification and morphological innovations have been attributed to large-scale gene or genome duplications at the origin of the group. These duplications are predicted to have occurred in two rounds, the "2R" hypothesis, or they may have occurred in one genome duplication plus many segmental duplications, although these hypotheses are disputed. Under such models, most genes that are duplicated in all vertebrates should have originated during the same period. Previous work has shown that indeed duplications started after the speciation between vertebrates and the closest invertebrate, amphioxus, but have not set a clear ending. Consideration of chordate phylogeny immediately shows the key position of cartilaginous vertebrates (Chondrichthyes) to answer this question. Did gene duplications occur as frequently during the 45 Myr between the cartilaginous/bony vertebrate split and the fish/tetrapode split as in the previous approximately 100 Myr? Although the time interval is relatively short, it is crucial to understanding the events at the origin of vertebrates. By a systematic appraisal of gene phylogenies, we show that significantly more duplications occurred before than after the cartilaginous/bony vertebrate split. Our results support rounds of gene or genome duplications during a limited period of early vertebrate evolution and allow a better characterization of these events.     

Crystal Structures of Influenza A Virus Matrix Protein M1: Variations on a Theme

Matrix protein 1 (M1) of the influenza A virus plays multiple roles in virion assembly and infection. Interest in the pH dependence of M1''s multiple functions led us to study the effect of subtle pH changes on M1 structure, resulting in the elucidation of a unique low-pH crystal structure of the N^1-165-domain of A/WSN/33 (H1N1) M1 that has never been reported. Although the 2.2 Å crystal structure of M1 N-terminus shows a dimer with the two monomers interacting in a face-to-face fashion at low pH as observed earlier, a 44° rotation of the second monomer has led to a significantly different dimer interface that possibly affects dimer stability. More importantly, while one of the monomers is fully defined, the N-terminal half of the second monomer shows considerable disorder that appears inherent in the protein and is potentially physiologically relevant. Such disorder has not been observed in any other previously reported structure at either low or high pH conditions, despite similar crystallization pH conditions. By comparing our novel N^1-165-domain structure with other low-pH or neutral-pH M1 structures, it appears that M1 can energetically access different monomer and dimer conformations, as well as oligomeric states, with varying degree of similarities. The study reported here provides further insights into M1 oligomerization that may be essential for viral propagation and infectivity.     

番荔枝科植物叶的比较解剖学

利用扫描电镜、叶表皮离析法和石蜡切片法研究了番荔枝科93种2变种植物叶片的形态结构.结果表明番荔枝科植物叶片形态结构具有较大相似性,如叶表面均具有表皮毛,表皮细胞具有晶体,气孔器为平列型,具2～6个副卫细胞,仅分布在远轴面,普遍具有败育气孔器,叶肉组织中普遍含有油细胞等,但表皮毛的类型,表皮细胞的形状,表皮细胞内晶体的类型和形态,叶肉组织的结构具有明显的属间和种间差异.     

Comparative anatomy of the young stem,node, and leaf of Bonnetiaceae,including observations on a foliar endodermis

A comprehensive study of the nodal and leaf anatomy of Bonnetiaceae was completed in order to provide evidence for evaluation in relation to systematics. Nodal anatomy is trilacunar, three-trace or unilacunar, one-trace. Basic leaf anatomical features of the family include: complete or incomplete medullated vascular cylinder in petiole; paracytic mature stomata with encircling ridges; large mucilaginous cells in the adaxial surface of mesophyll; periclinal divisions in upper surface layers; and discrete patches of phloem within the vascular bundles. Especially noteworthy is the presence in some genera of foliar vascular bundles enveloped by a sheath composed of two concentric regions, i.e., an inner region consisting of multiple layers of fibers and an outer specialized endodermis composed of thin-walled cells with Casparian strips. Leaves are variable with respect to lamina and cuticle thickness, relative amount and number of palisade and spongy layers, venation of lamina, and the presence or absence of sclereids and crystals in the mesophyll. A major feature in the evolution of Bonnetiaceae is development of a highly divergent, essentially parallel, leaf venation that is superficially similar to that of some monocotyledons and apparently unique among dicotyledons. Foliar anatomy provides important characters for the recognition of subgroups within Bonnetiaceae and is consistent with the segregation of Bonnetiaceae from Theaceae.     

番荔枝科蚁花属和澄广花属叶的比较解剖学研究

利用扫描电镜技术,叶片离析方法和石蜡切片法对蚁花属1种和澄广花属9种植物叶的形态结构进行比较研究。结果表明,两属植物有许多相似之处,但又有以下一些显著不同;蚁花属植物叶表皮细胞均具一晶族,叶肉组织中具1-2层栅栏组织细胞,油细胞均匀分布在栅栏组织和海绵组织中,栅栏组织在主脉处不连续,而澄广花属植物叶的表皮细胞内具一单斜晶,叶肉组织中具1层栅栏组织细胞,油细胞仅分布在海绵组织中,栅栏组织在主脉处连续,结果为蚁花属和澄广花属的分类学处理提供了新证据。     

Observations on the Oman Shark,Iago omanensis (Triakidae), with emphasis on the morphological and cytological changes of the oviduct and yolk sac during gestation

The shark Iago omanensis (Triakidae, Selachia) is encountered in large populations in the Gulf of Aqaba, Red Sea, at depths of 150–1,500 m. It is a placental viviparous species, reproductive all year round and giving birth to four (occasionally five) young of 170- to 180-mm total length (TL). Its distribution and morphometrics, as well as histological and cytological changes in the oviducts, were studied. The ratio of weight of the female genital organs to body weight changes from 0.7% in nongravid females to 19.8% in the final stages of pregnancy. The ripe, liberated eggs, which are 11–12 mm long and 5 mm wide, pass through the nidamental gland and settle in the uterus. The embryo attains 9- to 11-mm TL and settles on a protruding ridge of the submucosa, covered with a microvillar endometrium. At this site of attachment, a placenta is formed and the participating uterine endometrium and wall of the yolk sac undergo profound histocytological changes, forming two parts of this organ. Three forms of food provisioning occur in the growing embryos: (1) lecithotrophic, based on yolk transported from the egg to the embryonic gut via the umbilical cord; (2) mixed food provision, during which, in addition to nourishment provided via the umbilicus, food is transported across the placenta through transfer from the female blood vascular system to the embryonic yolk sac via the trophic villi of the yolk sac; and (3) histotrophic, when all yolk reserves have been used and nutrition is provided from the so-called “milk” within the yolk sac, metabolized by the trophic structures of the sac and transported by blood vessels. Despite the gradual utilization of yolk, the yolk sac mass initially increases from 0.5–1.0 cc to 2.0–2.2 cc with the addition of primary and secondary trophic villi until, during the final stages of embryogenesis, it decreases again to 1.4–1.6 cc. Neonate juveniles are 35–40 times heavier than the original eggs. J. Morphol. 236:151–165, 1998. © 1998 Wiley-Liss, Inc.     

Comparative anatomy of the cheek muscles of Korean cobitid fishes (Ostariophysi: Cypriniformes), with the comments on their phylogenetic relationships

Cheek muscles of 16 species of all Korean cobitid species belong to six genera were examined and described in detail, with comments on their phylogenetic relationships made on the basis of characteristics of cheek muscles. Korean cobitids were divided into two groups, the Cobitis and Misgurnus groups, by five characters related to three cheek muscles (adductor mandibulae, preorbitalis, and retractor arcus palatine). The former group, comprising Cobitis, Iksookimia, Kichulchoia, Koreocobitis, and Niwaella, is defined by four apomorphies, and the latter, including Misgurnus, by a single apomorphy.     

Variations on a theme: the many modes of cytokinesis

Animal cell division is believed to be mediated primarily by the 'purse-string' mechanism, which entails furrowing of the equatorial region, driven by the interaction of actin and myosin II filaments within contractile rings. However, myosin II-null Dictyostelium cells on substrates divide efficiently in a cell cycle-coupled manner. This process, termed cytokinesis B, appears to be driven by polar traction forces. Data in the literature can be interpreted as suggesting that adherent higher animal cells also use a cytokinesis B-like mechanism for cytokinesis. An additional chemotaxis-based cytokinesis that involves a 'midwife' cell has also been reported. Collectively, these findings demonstrate an unexpected diversity of mechanisms by which animal cells carry out cytokinesis.     

Morphology of the Mechanosensory Lateral Line System in Elasmobranch Fishes: Ecological and Behavioral Considerations

The relationship between morphology of the mechanosensory lateral line system and behavior is essentially unknown in elasmobranch fishes. Gross anatomy and spatial distribution of different peripheral lateral line components were examined in several batoids (Raja eglanteria, Narcine brasiliensis, Gymnura micrura, and Dasyatis sabina) and a bonnethead shark, Sphyrna tiburo, and are interpreted to infer possible behavioral functions for superficial neuromasts, canals, and vesicles of Savi in these species. Narcine brasiliensis has canals on the dorsal surface with 1 pore per tubule branch, lacks a ventral canal system, and has 8–10 vesicles of Savi in bilateral rows on the dorsal rostrum and numerous vesicles ( = 65 ± 6 SD per side) on the ventral rostrum. Raja eglanteria has superficial neuromasts in bilateral rows along the dorsal body midline and tail, a pair anterior to each endolymphatic pore, and a row of 5–6 between the infraorbital canal and eye. Raja eglanteria also has dorsal canals with 1 pore per tubule branch, pored and non-pored canals on the ventral surface, and lacks a ventral subpleural loop. Gymnura micrura has a pored dorsal canal system with extensive branch patterns, a pored ventral hyomandibular canal, and non-pored canal sections around the mouth. Dasyatis sabina has more canal pores on the dorsal body surface, but more canal neuromasts and greater diameter canals on the ventral surface. Sphyrna tiburo has primarily pored canals on both the dorsal and ventral surfaces of the head, as well as the posterior lateral line canal along the lateral body surface. Based upon these morphological data, pored canals on the dorsal body and tail of elasmobranchs are best positioned to detect water movements across the body surface generated by currents, predators, conspecifics, or distortions in the animal's flow field while swimming. In addition, pored canals on the ventral surface likely also detect water movements generated by prey. Superficial neuromasts are protected from stimulation caused by forward swimming motion by their position at the base of papillar grooves, and may detect water flow produced by currents, prey, predators, or conspecifics. Ventral non-pored canals and vesicles of Savi, which are found in benthic batoids, likely function as tactile or vibration receptors that encode displacements of the skin surface caused by prey, the substrate, or conspecifics. This mechanotactile mechanism is supported by the presence of compliant canal walls, neuromasts that are enclosed in wide diameter canals, and the presence of hair cells in neuromasts that are polarized both parallel to and nearly perpendicular to the canal axis in D. sabina. The mechanotactile, schooling, and mechanosensory parallel processing hypotheses are proposed as future directions to address the relationships between morphology and physiology of the mechanosensory lateral line system and behavior in elasmobranch fishes.     

Comparative internal morphology of deep-sea eels, with particular emphasis on gonads and gut structure

Anatomic and cytological studies of some 110 species of deep-sea eels of among others the families Congridae, Colocongridae, Heterenchelyidae, Synaphobranchidae, Nettastomatidae, Nemichthyidae, Serrivomeridae, revealed a very high diversity in the visceral organs, especially gonads, guts and kidneys and their relation to the anal opening.
The ovaries of various species were either monocyclic, producing eggs periodically, or polycyclic with frequent egg production. Some testes showed synchronous and others asynchronous sperm production. In some of the families, such as Heterenchelyidae, all the gonads are situated post-anally, in the tail, whereas in Congridae the extent of penetration varies in the different genera, indicating that this family is an artificial one. As some gonads of a few species were found to harbour gametes of the two sexes, the possible occurrence of hermaphroditism is discussed. Melanization of gut was observed in numerous species produced by the penetration of pigmented tissue between the muscle layers of the gut wall or between these and the gut epithelium, this differing between various taxa and in young and adult specimens. The melanization of gut or parts of gut prevent slight (emitted by the swallowed bioluminescent prey) from being seen outside, and in this way protects the eel from predation. Pigmentation also occurs in the kidneys and other explanations for melanization are therefore discussed. In numerous species the gut, kidney and gas chamber partially penetrate into the tail, and as with the gonads, these characters can also be used on eel taxonomy.