Zoological Science

The Zoological Society of Japan is one of the longest-standing scientific societies in Japan, and it has been publishing a unique prestigious international journal in zoology, Zoological Science, for a long period of time since its foundation in 1984 as the continuation of Zoological Magazine (1888–1983) and Annotationes Zoologicae Japonenses (1897–1983). One of the most salient features of the Society and the Journal may be the variety of species of animals used in the studies by the members of the society and the authors of the journal. Among various animal species, fish may have contributed to almost all disciplines of presentations and publications, including behavioral biology, biochemistry, cell biology, developmental biology, diversity and evolution, ecology, endocrinology, genetics, immunology, morphology, neurobiology, phylogeny, reproductive biology, and taxonomy. Owing to the recent advancement of modern molecular genetic methods in biology, not a few fish species have contributed to various research disciplines in zoological science as model animals. The present Special Issue includes various kinds of such studies in zoological science by taking advantage of a variety of fish species, which are contributed by authors of various generations ranging from junior to senior zoologists.

Herpesviruses are a large family of DNA viruses infecting vertebrates and invertebrates, and are important pathogens in the field of aquaculture. In general, herpesviruses do not have the ability to integrate into the host genomes since they do not have a chromosomal integration step in their life cycles. Recently, we identified a novel group of herpesviruses, “Teratorn” and its related elements, in the genomes of various teleost fish species. At least some of the Teratorn-like herpesviruses are fused with a piggyBac-like DNA transposon, suggesting that they have acquired the transposon-like intragenomic lifestyle by hijacking the transposon system. In this review, we describe the sequence characteristics of Teratorn-like herpesviruses and phylogenetic relationships with other herpesviruses. Then we discuss the process of transposon-herpesvirus fusion, their life cycle, and the generality of transposon-virus fusion. Teratorn-like herpesviruses provide a piece of concrete evidence that even non-retroviral elements can become intragenomic parasites retaining replication capacity, by acquiring transposition machinery from other sources.

For adaptation to a high salinity marine environment, cartilaginous fishes have evolved a ureosmotic strategy. They have a highly elaborate “four-loop nephron” in the kidney, which is considered to be important for reabsorption of urea from the glomerular filtrate to maintain a high concentration of urea in the body. However, the function and regulation, generally, of the “four-loop nephron” are still largely unknown due to the complicated configuration of the nephron and its many subdivided segments. Laser microdissection (LMD) followed by RNA-sequencing (RNA-seq) analysis is a powerful technique to obtain segment-dependent gene expression profiles. In the present study, using the kidney of cloudy catshark, Scyliorhinus torazame, we tested several formaldehyde-free and formaldehyde-based fixatives to optimize the fixation methods. Fixation by 1% neutral buffered formalin for 15 min resulted in sufficient RNA and structural integrities, which allowed LMD clipping of specific nephron segments and subsequent RNA-seq analysis. RNA-seq from the LMD samples of the second-loop, the fourth-loop, and the five tubular segments in the bundle zone revealed a number of specific membrane transporter genes that can characterize each segment. Among them, we examined expressions of the Na ⁺ -coupled cotransporters abundantly expressed in the second loop samples. Although the proximal II segment of the second loop is known for the elimination of excess solutes, the present results imply that the PII segment is also crucial for reabsorption of valuable solutes. Looking ahead to future studies, the segment-dependent gene expression profiling will be a powerful technique for unraveling the renal mechanisms and regulation in euryhaline elasmobranchs.

Visual pathways to the telencephalon in teleost fishes have been studied in detail only in a few species, and their evolutionary history remained unclear. On the basis of our recent studies we propose that there were two visual pathways in the common ancestor of teleosts, while one of them became lost in acanthopterygian fishes that emerged relatively recently. Our in-depth analyses on the connections of visual centers also revealed that there are connections shared with those of mammals, and retinotopic organization of the ascending connections is maintained at least to the level of the diencephalon in the yellowfin goby. The major visual telencephalic center, or the lateral part of the dorsal telencephalon (Dl), shows considerable species differences in the number of regions and cytoarchitecture. In particular, four highly specialized compartments are noted in the Dl of gobies, and we analyzed about 100 species of teleosts to investigate the evolution of the compartments in the Dl, which indicated that four compartments emerged only in Gobiiformes, while there are fewer specialized compartments in some other percomorph lineages. We also discuss the connections of forebrain visual centers with the cerebellum and other lower brain centers and infer possible functions of the circuitries.

Weakly electric fish possess electrosensory neural systems that are dedicated to detect microsecond time differences between sensory signals. Many features of this timing system, such as electroreceptor encoding, time-locked responses, and time-comparator neural circuit, are shared by closely related as well as distantly related electric fishes. The appearance and location of the time-comparator neural structures, however, are different among species. The timing systems of different electric fish species are compared.

Many vertebrate species show breeding periods and exhibit series of characteristic species-specific sexual behaviors only during the breeding period. Here, secretion of gonadal sex hormones from the mature gonads has been considered to facilitate sexual behaviors. Thus, the sexual behavior has long been considered to be regulated by neural and hormonal mechanisms. In this review, we discuss recent progress in the study of neural control mechanisms of sexual behavior with a focus on studies using fish, which have often been the favorite animals used by many researchers who study instinctive animal behaviors. We first discuss control mechanisms of sexual behaviors by sex steroids in relation to the anatomical studies of sex steroid-concentrating neurons in various vertebrate brains, which are abundantly distributed in evolutionarily conserved areas such as preoptic area (POA) and anterior hypothalamus. We then focus on another brain area called the ventral telencephalic area, which has also been suggested to contain sex steroid-concentrating neurons and has been implicated in the control of sexual behaviors, especially in teleosts. We also discuss control of sex-specific behaviors and sexual preference influenced by estrogenic signals or by olfactory/pheromonal signals. Finally, we briefly summarize research on the modulatory control of motivation for sexual behaviors by a group of peptidergic neurons called terminal nerve gonadotropin-releasing hormone (TN-GnRH) neurons, which are known to be especially developed in fishes among various vertebrate species.

The cerebellum receives inputs via the climbing fibers originating from the inferior olivary nucleus in the ventral medulla. In mammals, the climbing fibers entwine and terminate onto both major and peripheral branches of dendrites of the Purkinje cells. In this study, the inferior olivary nucleus and climbing fiber in the goldfish were investigated with several histological techniques. By neural tracer application to the hemisphere of the cerebellum, labeled inferior olivary neurons were found in the ventral edge of the contralateral medulla. Kainate stimulated Co ^{+ +} uptake and gephyrin immunoreactivities were found in inferior olivary neurons, indicating, respectively, that they receive both excitatory (glutamatergic) and inhibitory (GABAergic or glycinergic) inputs. Inferior olivary neurons express vglut2.1 transcripts, suggesting they are glutamatergic. Around 85% of inferior olivary neurons were labeled with anti-calretinin antiserum. Calretinin immunoreactive (ir) climbing fiber terminal-like structures were distributed near the Purkinje cells and in the molecular layer. Double labeling immunofluorescence with anti-calretinin and zebrin II antisera revealed that the calretinin-ir climbing fibers run along and made synaptic-like contacts on the major dendrites of the zebrin II-ir Purkinje cells. In teleost fish, cerebellar efferent neurons, eurydendroid cells, also lie near the Purkinje cells and extend dendrites outward to intermingle with dendrites of the Purkinje cells within the molecular layer. Here we found no contacts between the climbing fiber terminals and the eurydendroid cell dendrites. These results support the idea that Purkinje cells, but not eurydendroid cells, receive strong inputs via the climbing fibers, similar to the mammalian situation.

Vertebrates generally possess hypophysiotropic and non-hypophysiotropic gonadotropin releasing hormone (GnRH) neurons. The terminal nerve (TN) GnRH neurons are known to belong to the non-hypophysiotropic neurons and have been suggested to modulate sexual behaviors. These neurons show spontaneous pacemaker firing activity and release neuropeptides GnRH and neuropeptide FF. Since the spontaneous firing activities of peptidergic neurons, including GnRH neurons, are believed to play important roles in the release of neuropeptides, understanding the regulatory mechanisms of these spontaneous firing activities is important. Here, we analyzed firing activities of the TN-GnRH neurons in medaka during application of acetylcholine (ACh), which is one of the essential neuromodulators in the brain. Whole cell patch clamp recording of TN-GnRH neurons demonstrated that ACh induces hyperpolarization and inhibits their pacemaker firing. Electrophysiological analysis using an antagonist for acetylcholine receptors and in situ hybridization analysis showed that firing of TN-GnRH neurons is inhibited via M2-type muscarinic acetylcholine receptor. These findings, taken together with literature from several other fish species (including teleosts and elasmobranchs), indicate that ACh may generally play an inhibitory role in modulating spontaneous activities of TN-GnRH neurons and thereby sexual behaviors in fish.

Lateral preference in behaviors has been widely documented in many vertebrates and invertebrates. Such preferences are strange, puzzling, and on the surface, not adaptive. However, behavioral laterality may increase an individual's fitness as well as foraging accuracy and speed. There is little experimental evidence regarding the developmental process of laterality, and unsolved questions have perplexed researchers for several decades. Related to these issues, here, I review that the scale-eating cichlid Perissodus microlepis found in Lake Tanganyika is a valuable model to address the developmental mechanism of animal laterality. The scale-eating cichlid has pronounced behavioral laterality and uses its asymmetric mouth during feeding events. Recent studies have shown that behavioral laterality in this fish depends on both genetic factors and past experience. The attack-side preference of scale eaters is an acquired trait in an early developmental stage. Juvenile fish empirically learn which side of the prey is more effective for tearing scales and gradually select the dominant side for attacking. However, the superior kinetics of body flexion during the dominant side attack has innate characteristics. Additionally, left–right differences in scale-eater mandibles also develop during ontogeny. Further progress toward understanding the comprehensive mechanisms of laterality should address the following persistent barriers: (1) the effects of phylogenetic constraints and ecological factors on the level of laterality; and (2) the neuronal and molecular mechanisms that produce left–right behavioral differences.

Individual recognition is a necessary cognitive ability for the maintenance of stable social relationships. Recent studies have shown that like primates, some fish species can distinguish familiar fish from unfamiliar strangers via face-recognition. However, the taxa of the studied fish species are restricted (within Perciformes) and the visual signal used for the recognition of fish remains unclear. Here, we investigated the visual signal for individual-recognition in males of a sexually dichromatic guppy (Poecilia reticulata, Cyprinodontiformes). Using guppy males, we examined the hypothesis that fish distinguish between familiar individuals and unknown strangers by their faces rather than by body coloration. We randomly presented focal fish with four types of composite photo-models: familiar (familiar-face and familiar-body = F/F), stranger (stranger-face and stranger-body = S/S), familiar face combined with stranger body (F/S) and stranger face combined with familiar body (S/F). Focal males infrequently attacked familiar-face models but frequently attacked stranger-face models, regardless of body types. These behavioral reactions indicate that guppy males discriminate between familiar and stranger males by their face, not body coloration with wide variation. Importantly, male faces contain clear individual-variation in white/metallic colored patches on the operculum visible for humans. Considering the photo-model, our results suggest that these patches might be an important visual stimulus for face-recognition in guppy males, like some cichlids. Comparative examination among males of different guppy variants, including wild type phenotype, suggests that the face color-patch is stable regardless of variation in body color, with a different genetic mechanism potentially underlying face and body colors.