RESUMEN
The production of communication signals can be modulated by hormones acting on the brain regions that regulate these signals. However, less is known about how signal perception is regulated by hormones. The electrocommunication signals of weakly electric fishes are sexually dimorphic, sensitive to hormones, and vary across species. The neural circuits that regulate the production and perception of these signals are also well-characterized, and electric fishes are thus an excellent model to examine the neuroendocrine regulation of sensorimotor mechanisms of communication. We investigated (1) whether steroid-related genes are expressed in sensory brain regions that process communication signals; and (2) whether this expression differs across sexes and species that have different patterns of sexual dimorphism in their signals. Apteronotus leptorhynchus and Apteronotus albifrons produce continuous electric organ discharges (EODs) that are used for communication. Two brain regions, the electrosensory lateral line lobe (ELL) and the dorsal torus semicircularis (TSd), process inputs from electroreceptors to allow fish to detect and discriminate electrocommunication signals. We used qPCR to quantify the expression of genes for two androgen receptors (ar1, ar2), two estrogen receptors (esr1, esr2b), and aromatase (cyp19a1b). Four out of five steroid-related genes were expressed in both sensory brain regions, and their expression often varied between sexes and species. These results suggest that expression of steroid-related genes in the brain may differentially influence how EOD signals are encoded across species and sexes, and that gonadal steroids may coordinately regulate central circuits that control both the production and perception of EODs.
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Encéfalo , Pez Eléctrico , Órgano Eléctrico , Caracteres Sexuales , Animales , Femenino , Pez Eléctrico/genética , Pez Eléctrico/metabolismo , Masculino , Encéfalo/metabolismo , Órgano Eléctrico/metabolismo , Órgano Eléctrico/fisiologíaRESUMEN
Nutrient absorption is essential for animal survival and development. Our previous study on zebrafish reported that nutrient absorption in lysosome-rich enterocytes (LREs) is promoted by the voltage-sensing phosphatase (VSP), which regulates phosphoinositide (PIP) homeostasis via electrical signaling in biological membranes. However, it remains unknown whether this VSP function is shared by different absorptive tissues in other species. Here, we focused on the function of VSP in a viviparous teleost Xenotoca eiseni, whose intraovarian embryos absorb nutrients from the maternal ovarian fluid through a specialized hindgut-derived pseudoplacental structure called trophotaenia. Xenotoca eiseni VSP (Xe-VSP) is expressed in trophotaenia epithelium, an absorptive tissue functionally similar to zebrafish LREs. Notably, the apical distribution of Xe-VSP in trophotaenia epithelial cells closely resembles zebrafish VSP (Dr-VSP) distribution in zebrafish LREs, suggesting a shared role for VSP in absorptive tissues between the two species. Electrophysiological analysis using a heterologous expression system revealed that Xe-VSP preserves functional voltage sensors and phosphatase activity with the leftward shifted voltage sensitivity compared with zebrafish VSP (Dr-VSP). We also identified a single amino acid variation in the S4 helix of Xe-VSP as one of the factors contributing to the leftward shifted voltage sensitivity. This study highlights the biological variation and significance of VSP in various animal species, as well as hinting at the potential role of VSP in nutrient absorption in X. eiseni trophotaenia.NEW & NOTEWORTHY We investigate the voltage-sensing phosphatase (VSP) in Xenotoca eiseni, a viviparous fish whose intraovarian embryos utilize trophotaenia for nutrient absorption. Although X. eiseni VSP (Xe-VSP) shares key features with known VSPs, its distinct voltage sensitivity arises from species-specific amino acid variation. Xe-VSP in trophotaenia epithelium suggests its involvement in nutrient absorption, similar to VSP in zebrafish enterocytes and potentially in species with similar absorptive cells. Our findings highlight the potential role of VSP across species.
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Monoéster Fosfórico Hidrolasas , Viviparidad de Animales no Mamíferos , Animales , Femenino , Monoéster Fosfórico Hidrolasas/metabolismo , Monoéster Fosfórico Hidrolasas/genética , Proteínas de Peces/metabolismo , Proteínas de Peces/genética , Enterocitos/metabolismo , Enterocitos/enzimología , Pez Eléctrico/fisiología , Pez Eléctrico/metabolismo , Pez Cebra , Potenciales de la MembranaRESUMEN
Hypoxia is a significant source of metabolic stress that activates many cellular pathways involved in cellular differentiation, proliferation, and cell death. Hypoxia is also a major component in many human diseases and a known driver of many cancers. Despite the challenges posed by hypoxia, there are animals that display impressive capacity to withstand lethal levels of hypoxia for prolonged periods of time and thus offer a gateway to a more comprehensive understanding of the hypoxic response in vertebrates. The weakly electric fish genus Brachyhypopomus inhabits some of the most challenging aquatic ecosystems in the world, with some species experiencing seasonal anoxia, thus providing a unique system to study the cellular and molecular mechanisms of hypoxia tolerance. In this study, we use closely related species of Brachyhypopomus that display a range of hypoxia tolerances to probe for the underlying molecular mechanisms via hypoxia inducible factors (HIFs)-transcription factors known to coordinate the cellular response to hypoxia in vertebrates. We find that HIF1⺠from hypoxia tolerant Brachyhypopomus species displays higher transactivation in response to hypoxia than that of intolerant species, when overexpressed in live cells. Moreover, we identified two SUMO-interacting motifs near the oxygen-dependent degradation and transactivation domains of the HIF1⺠protein that appear to boost transactivation of HIF1, regardless of the genetic background. Together with computational analyses of selection, this shows that evolution of HIF1⺠are likely to underlie adaptations to hypoxia tolerance in Brachyhypopomus electric fishes, with changes in two SUMO-interacting motifs facilitating the mechanism of this tolerance.
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Pez Eléctrico , Subunidad alfa del Factor 1 Inducible por Hipoxia , Oxígeno , Animales , Ecosistema , Pez Eléctrico/genética , Pez Eléctrico/metabolismo , Subunidad alfa del Factor 1 Inducible por Hipoxia/genética , Subunidad alfa del Factor 1 Inducible por Hipoxia/metabolismo , Anaerobiosis , Oxígeno/metabolismoRESUMEN
Hormones and receptors coevolve to generate species diversity in hormone action. We compared the structure and function of androgen receptors (ARs) across fishes, with a focus on ARs in ghost knifefishes (Apteronotidae). Apteronotids, like many other teleosts, have two ARs (ARα and ARß). ARß is largely conserved, whereas ARα sequences vary considerably across species. The ARα ligand binding domain (LBD) has evolved under positive selection, and differences in the LBD across apteronotid species are associated with diversity in androgenic regulation of behavior. The Apteronotus leptorhynchus ARα LBD differs substantially from that of the Apteronotus albifrons ARα or the ancestral AR. Structural modeling and transactivation assays demonstrated that A. leptorhynchus ARα cannot bind androgens. We propose a model whereby relative expression of ARα versus ARß in the brain, coupled with loss of androgen binding by ARα in A. leptorhynchus might explain reversals in androgenic regulation and sex differences in electrocommunication behavior.
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Andrógenos , Pez Eléctrico , Animales , Femenino , Masculino , Andrógenos/farmacología , Andrógenos/metabolismo , Pez Eléctrico/metabolismo , Receptores Androgénicos/metabolismo , Peces/genética , Peces/metabolismo , ComunicaciónRESUMEN
The ability to generate and detect electric fields has evolved in several groups of fishes as a means of communication, navigation and, occasionally, predation. The energetic burden required can account for up to 20% of electric fishes' daily energy expenditure. Despite this, molecular adaptations that enable electric fishes to meet the metabolic demands of bioelectrogenesis remain unknown. Here, we investigate the molecular evolution of the mitochondrial oxidative phosphorylation (OXPHOS) complexes in the two most diverse clades of weakly electric fishes-South American Gymnotiformes and African Mormyroidea, using codon-based likelihood approaches. Our analyses reveal that although mitochondrial OXPHOS genes are generally subject to strong purifying selection, this constraint is significantly reduced in electric compared to non-electric fishes, particularly for complexes IV and V. Moreover, analyses of concatenated mitochondrial genes show strong evidence for positive selection in complex I genes on the two branches associated with the independent evolutionary origins of electrogenesis. These results suggest that adaptive evolution of proton translocation in the OXPHOS cellular machinery may be associated with the evolution of bioelectrogenesis. Overall, we find striking evidence for remarkably similar effects of electrogenesis on the molecular evolution of mitochondrial OXPHOS genes in two independently derived clades of electrogenic fishes. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.
Asunto(s)
Pez Eléctrico/genética , Evolución Molecular , Proteínas de Peces/genética , Mitocondrias/metabolismo , Familia de Multigenes , Fosforilación Oxidativa , Animales , Pez Eléctrico/metabolismo , Proteínas de Peces/metabolismo , Genoma Mitocondrial , Selección GenéticaRESUMEN
Environmental hypoxia has effected numerous and well-documented anatomical, physiological and behavioural adaptations in fishes. Comparatively little is known about hypoxia's impacts on sensing because it is difficult to quantify sensory acquisition in vivo. Weakly electric fishes, however, rely heavily on an easily-measurable sensory modality-active electric sensing-whereby individuals emit and detect electric organ discharges (EODs). In this study, hypoxia tolerance of a mormyrid weakly electric fish, Marcusenius victoriae, was assessed by examining both its metabolic and EOD rates using a critical threshold (pcrit ) paradigm. The routine metabolic rate was 1.42 mg O2 h-1 , and the associated critical oxygen tension was 14.34 mmHg. Routine EOD rate was 5.68 Hz with an associated critical tension of 15.14 mmHg. These metabolic indicators of hypoxia tolerance measured in this study were consistent with those in previous studies on M. victoriae and other weakly electric fishes. Furthermore, our results suggest that some aerobic processes may be reduced in favour of maintaining the EOD rate under extreme hypoxia. These findings underscore the importance of the active electrosensory modality to these hypoxia-tolerant fish.
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Pez Eléctrico/fisiología , Órgano Eléctrico/fisiología , Hipoxia/fisiopatología , Aerobiosis , Animales , Pez Eléctrico/metabolismo , Femenino , Hipoxia/metabolismo , Lagos , Masculino , Oxígeno/metabolismo , Uganda , HumedalesRESUMEN
The evolution of increased encephalization comes with an energetic cost. Across species, this cost may be paid for by an increase in metabolic rate or by energetic trade-offs between the brain and other energy-expensive tissues. However, it remains unclear whether these solutions to deal with the energetic requirements of an enlarged brain are related to direct physiological constraints or other evolved co-adaptations. We studied the highly encephalized mormyrid fishes, which have extensive species diversity in relative brain size. We previously found a correlation between resting metabolic rate and relative brain size across species; however, it is unknown how this interspecific relationship evolved. To address this issue, we measured intraspecific variation in relative brain size, the sizes of other organs, metabolic rate, and hypoxia tolerance to determine if intraspecific relationships between brain size and organismal energetics are similar to interspecific relationships. We found that 3 species of mormyrids with varying degrees of encephalization had no intraspecific relationships between relative brain size and relative metabolic rate or relative sizes of other organs, and only 1 species had a relationship between relative brain size and hypoxia tolerance. These species-specific differences suggest that the interspecific relationship between metabolic rate and relative brain size is not the result of direct physiological constraints or strong stabilizing selection, but is instead due to other species level co-adaptations. We conclude that variation within species must be considered when determining the energetic costs and trade-offs underlying the evolution of extreme encephalization.
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Evolución Biológica , Encéfalo/anatomía & histología , Encéfalo/metabolismo , Pez Eléctrico/anatomía & histología , Pez Eléctrico/metabolismo , Animales , Metabolismo Energético , Hipoxia/metabolismo , Tamaño de los Órganos , Consumo de Oxígeno , Especificidad de la EspecieRESUMEN
Heterogeneity of neural properties within a given neural class is ubiquitous in the nervous system and permits different sub-classes of neurons to specialize for specific purposes. This principle has been thoroughly investigated in the hindbrain of the weakly electric fish A. leptorhynchus in the primary electrosensory area, the Electrosensory Lateral Line lobe (ELL). The pyramidal cells (PCs) that receive inputs from tuberous electroreceptors are organized in three maps in distinct segments of the ELL. The properties of these cells vary greatly across maps due to differences in connectivity, receptor expression, and ion channel composition. These cells are a seminal example of bursting neurons and their bursting dynamic relies on the presence of voltage-gated Na+ channels in the extensive apical dendrites of the superficial PCs. Other ion channels can affect burst generation and their expression varies across ELL neurons and segments. For example, SK channels cause hyperpolarizing after-potentials decreasing the likelihood of bursting, yet bursting propensity is similar across segments. We question whether the depolarizing mechanism that generates the bursts presents quantitative differences across segments that could counterbalance other differences having the opposite effect. Although their presence and role are established, the distribution and density of the apical dendrites' Na+ channels have not been quantified and compared across ELL maps. Therefore, we test the hypothesis that Na+ channel density varies across segment by quantifying their distribution in the apical dendrites of immunolabeled ELL sections. We found the Na+ channels to be two-fold denser in the lateral segment (LS) than in the centro-medial segment (CMS), the centro-lateral segment (CLS) being intermediate. Our results imply that this differential expression of voltage-gated Na+ channels could counterbalance or interact with other aspects of neuronal physiology that vary across segments (e.g., SK channels). We argue that burst coding of sensory signals, and the way the network regulates bursting, should be influenced by these variations in Na+ channel density.
Asunto(s)
Dendritas/metabolismo , Pez Eléctrico/metabolismo , Células Piramidales/metabolismo , Rombencéfalo/metabolismo , Canales de Sodio/metabolismo , Animales , Sistema de la Línea Lateral/metabolismoRESUMEN
Sexually dimorphic behaviors are often regulated by androgens and estrogens. Steroid receptors and metabolism are control points for evolutionary changes in sexual dimorphism. Electric communication signals of South American knifefishes are a model for understanding the evolution and physiology of sexually dimorphic behavior. These signals are regulated by gonadal steroids and controlled by a simple neural circuit. Sexual dimorphism of the signals varies across species. We used transcriptomics to examine mechanisms for sex differences in electric organ discharges (EODs) of two closely related species, Apteronotus leptorhynchus and Apteronotus albifrons, with reversed sexual dimorphism in their EODs. The pacemaker nucleus (Pn), which controls EOD frequency (EODf), expressed transcripts for steroid receptors and metabolizing enzymes, including androgen receptors, estrogen receptors, aromatase, and 5α-reductase. The Pn expressed mRNA for ion channels likely to regulate the high-frequency activity of Pn neurons and for neuromodulator and neurotransmitter receptors that may regulate EOD modulations used in aggression and courtship. Expression of several ion channel genes, including those for Kir3.1 inward-rectifying potassium channels and sodium channel ß1 subunits, was sex-biased or correlated with EODf in ways consistent with EODf sex differences. Our findings provide a basis for future studies to characterize neurogenomic mechanisms by which sex differences evolve.
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Comunicación Animal , Pez Eléctrico/genética , Caracteres Sexuales , Agresión/fisiología , Animales , Biodiversidad , Biología Computacional , Cortejo , Pez Eléctrico/metabolismo , Órgano Eléctrico/fisiología , Femenino , Expresión Génica , Canales Iónicos/genética , Canales Iónicos/metabolismo , Masculino , ARN Mensajero/metabolismo , Receptores de Esteroides/genética , Receptores de Esteroides/metabolismo , Conducta Sexual Animal/fisiología , Especificidad de la Especie , TranscriptomaRESUMEN
Aromatase is a steroidogenic enzyme involved in the conversion of testosterone into estradiol. Teleosts are unique among vertebrates in possessing two distinct aromatase genes that show different expression patterns within the body. Since the brain is the essential organ underlying the control of behavior, an understanding of the expression pattern of aromatase in the brain can help to identify neural circuits and behaviors that are most likely to be affected by aromatase activity. In addition, identifying species differences in aromatase expression in the brain can further our understanding of divergence in behaviors regulated by local estradiol production and estrogen signaling. Apteronotus leptorhynchus is a species of weakly electric fish in which little is known about sex steroid expression within the brain and its role in electric signaling behavior. The goal of this study was to identify the mRNA expression pattern of aromatase in the brain of A. leptorhynchus. Aromatase mRNA was detected in several parts of the forebrain and in the pituitary gland; however, no aromatase expression was detected in the midbrain or hindbrain. These findings in A. leptorhynchus support a role for aromatase activity in reproduction, but no direct role in electric signaling behavior in non-breeding fish. The findings of this study help to broaden the basis for making phylogenetic comparisons of aromatase expression across teleost lineages as well as different signaling systems, and provide information on behaviors and neural circuits that are potentially affected by local estradiol production in A. leptorhynchus.
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Aromatasa/biosíntesis , Encéfalo/enzimología , Pez Eléctrico/metabolismo , Animales , Aromatasa/análisis , ARN Mensajero/análisisRESUMEN
Hypothalamic nonapeptides (arginin vasotocin-vasopressin, oxytocin-isotocin) are known to modulate social behaviors across vertebrates. The neuroanatomical conservation of nonapeptide systems enables the use of novel vertebrate model species to identify general strategies of their functional mechanisms. We present a detailed immunohistochemical description of vasotocin (AVT) cell populations and their projections in two species of weakly electric fish with different social structure, Gymnotus omarorum and Brachyhypopomus gauderio. Strong behavioral, pharmacological, and electrophysiological evidence support that AVT modulation of electric behavior differs between the gregarious B. gauderio and the solitary G. omarorum. This functional diversity does not necessarily depend on anatomical differences of AVT neurons. To test this, we focus on interspecific comparisons of the AVT system in basal non-breeding males along the brain. G. omarorum and B. gauderio showed similar AVT somata sizes and comparable distributions of AVT somata and fibers. Interestingly, AVT fibers project to areas related to the control of social behavior and electromotor displays in both species. We found that no gross anatomical differences in the organization of the AVT system account for functional differences between species, which rather shall depend on the pattern of activation of neurons embedded in the same basic anatomical organization of the AVT system.
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Pez Eléctrico/metabolismo , Hipotálamo/metabolismo , Neuronas/metabolismo , Vasotocina/metabolismo , Animales , Conducta Animal/fisiología , Pez Eléctrico/anatomía & histología , Pez Eléctrico/crecimiento & desarrollo , Jerarquia Social , Hipotálamo/anatomía & histología , Hipotálamo/crecimiento & desarrollo , MasculinoRESUMEN
In mormyrid weakly electric fish, the electric organ discharge (EOD) is used for species recognition, orientation and prey localization. Produced in the muscle-derived adult electric organ, the EOD exhibits a wide diversity across species in both waveform and duration. While certain defining EOD characteristics can be linked to anatomical features of the electric organ, many factors underlying EOD differentiation are yet unknown. Here, we report the differential expression of 13 Kv1 voltage-gated potassium channel genes, two inwardly rectifying potassium channel genes, two previously studied sodium channel genes and an ATPase pump in two sympatric species of the genus Campylomormyrus in both the adult electric organ and skeletal muscle. Campylomormyrus compressirostris displays a basal EOD, largely unchanged during development, while C. tshokwe has an elongated, putatively derived discharge. We report an upregulation in all Kv1 genes in the electric organ of Campylomormyrus tshokwe when compared to both skeletal muscle and C. compressirostris electric organ. This pattern of upregulation in a species with a derived EOD form suggests that voltage-gated potassium channels are potentially involved in the diversification of the EOD signal among mormyrid weakly electric fish.
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Pez Eléctrico/genética , Pez Eléctrico/metabolismo , Órgano Eléctrico/fisiología , Canales de Potasio con Entrada de Voltaje/biosíntesis , Canales de Potasio con Entrada de Voltaje/genética , Animales , Femenino , Expresión GénicaRESUMEN
Teleost fish are capable of complex behaviors, including social and spatial learning; lesion studies show that these abilities require dorsal telencephalon (pallium). The teleost telencephalon has subpallial and pallial components. The subpallium is well described and highly conserved. In contrast, the teleost pallium is not well understood and its relation to that of other vertebrates remains controversial. Here we analyze the connectivity of the subdivisions of dorsal pallium (DD) of an electric gymnotiform fish, Apteronotus leptorhynchus: superficial (DDs), intermediate (DDi) and magnocellular (DDmg) components. The major pathways are recursive: the dorsolateral pallium (DL) projects strongly to DDi, with lesser inputs to DDs and DDmg. DDi in turn projects strongly to DDmg, which then feeds back diffusely to DL. Our quantitative analysis of DDi connectivity demonstrates that it is a global recurrent network. In addition, we show that the DD subnuclei have complex reciprocal connections with subpallial regions. Specifically, both DDi and DDmg are reciprocally connected to pallial interneurons within the misnamed rostral entopeduncular nucleus (Er). Based on DD connectivity, we illustrate the close similarity, and possible homology, between hippocampal and DD/DL circuitry. We hypothesize that DD/DL circuitry can implement the same pattern separation and completion computations ascribed to the hippocampal dentate gyrus and CA3 fields. We further contend that the DL to DDi to DDmg to DL feedback loop makes the pattern separation/completion operations recursive. We discuss our results with respect to recent studies on fear avoidance conditioning in zebrafish and attention and spatial learning in a pulse gymnotiform fish. J. Comp. Neurol. 525:8-46, 2017. © 2016 Wiley Periodicals, Inc.
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Cerebro/anatomía & histología , Pez Eléctrico/anatomía & histología , Animales , Cerebro/metabolismo , Conexinas/genética , Conexinas/metabolismo , Pez Eléctrico/genética , Pez Eléctrico/metabolismo , Retroalimentación Fisiológica , Proteínas de Peces/genética , Proteínas de Peces/metabolismo , Inmunohistoquímica , Hibridación in Situ , Modelos Neurológicos , Vías Nerviosas/anatomía & histología , Vías Nerviosas/metabolismo , Técnicas de Trazados de Vías Neuroanatómicas , Alineación de Secuencia , Homología de Secuencia de Aminoácido , Ácido gamma-Aminobutírico/metabolismoRESUMEN
Timing is crucial for social interactions. Animal behavior is synchronized with biotic and abiotic environment variables ensuring that the activity phase of conspecifics occurs during the same period of the day. As biological rhythms are embedded in the complex integrative control of the brain, it is fundamental to explore its interaction with environmental and social factors. This approach will unravel the link between external stimuli carrying information on environmental cycles and the neural commands for behavior, including social behavior, associated with precise phases of those cycles. Arousal in the solitary Gymnotus omarorum and in the gregarious Brachyhypopomus gauderio is characterized by a nocturnal increase in the basal discharge rate of electric behavior, which is mild and transient in G. omarorum and large and persistent in B. gauderio. In this study, we show that the major integrator of social behavior, AVT (arginine vasotocin), is not involved in the nocturnal increase of electric behavior basal rate in isolated animals of either species. On the other hand, endogenous melatonin, the major modulator of the circadian system, is responsible for the nocturnal increase in electric behavior in isolated individuals of both species.
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Nivel de Alerta/fisiología , Conducta Animal/fisiología , Ritmo Circadiano/fisiología , Pez Eléctrico/fisiología , Melatonina/fisiología , Conducta Social , Vasotocina/fisiología , Animales , Pez Eléctrico/metabolismo , Gymnotiformes/metabolismo , Gymnotiformes/fisiología , Uruguay , Vasotocina/metabolismoRESUMEN
Most vertebrates, including cartilaginous fishes, maintain their plasma SO4 (2-) concentration ([SO4 (2-)]) within a narrow range of 0.2-1 mM. As seawater has a [SO4 (2-)] about 40 times higher than that of the plasma, SO4 (2-) excretion is the major role of kidneys in marine teleost fishes. It has been suggested that cartilaginous fishes also excrete excess SO4 (2-) via the kidney. However, little is known about the underlying mechanisms for SO4 (2-) transport in cartilaginous fish, largely due to the extraordinarily elaborate four-loop configuration of the nephron, which consists of at least 10 morphologically distinguishable segments. In the present study, we determined cDNA sequences from the kidney of holocephalan elephant fish (Callorhinchus milii) that encoded solute carrier family 26 member 1 (Slc26a1) and member 6 (Slc26a6), which are SO4 (2-) transporters that are expressed in mammalian and teleost kidneys. Elephant fish Slc26a1 (cmSlc26a1) and cmSlc26a6 mRNAs were coexpressed in the proximal II (PII) segment of the nephron, which comprises the second loop in the sinus zone. Functional analyses using Xenopus oocytes and the results of immunohistochemistry revealed that cmSlc26a1 is a basolaterally located electroneutral SO4 (2-) transporter, while cmSlc26a6 is an apically located, electrogenic Cl(-)/SO4 (2-) exchanger. In addition, we found that both cmSlc26a1 and cmSlc26a6 were abundantly expressed in the kidney of embryos; SO4 (2-) was concentrated in a bladder-like structure of elephant fish embryos. Our results demonstrated that the PII segment of the nephron contributes to the secretion of excess SO4 (2-) by the kidney of elephant fish. Possible mechanisms for SO4 (2-) secretion in the PII segment are discussed.
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Pez Eléctrico/metabolismo , Túbulos Renales Proximales/metabolismo , Riñón/metabolismo , Proteínas de Transporte de Membrana/metabolismo , Sulfatos/metabolismo , Secuencia de Aminoácidos , Animales , ADN Complementario/genética , Embrión no Mamífero/metabolismo , Proteínas de Peces/metabolismo , Nefronas/metabolismo , Oocitos/metabolismo , Distribución Tisular , XenopusRESUMEN
The conventional prolactin (PRL), also known as PRL1, is an adenohypophysial hormone that critically regulates various physiological events in reproduction, metabolism, growth, osmoregulation, among others. PRL1 shares its evolutionary origin with PRL2, growth hormone (GH), somatolactin and placental lactogen, which together form the GH/PRL hormone family. Previously, several bioassays implied the existence of PRL1 in elasmobranch pituitaries. However, to date, all attempts to isolate PRL1 from chondrichthyans have been unsuccessful. Here, we cloned PRL1 from the pituitary of the holocephalan elephant fish, Callorhinchus milii, as the first report of chondrichthyan PRL1. The putative mature protein of elephant fish PRL1 (cmPRL1) consists of 198 amino acids, containing two conserved disulfide bonds. The orthologous relationship of cmPRL1 to known vertebrate PRL1s was confirmed by the analyses of molecular phylogeny and gene synteny. The cmPRL1 gene was similar to teleost PRL1 genes in gene synteny, but was distinct from amniote PRL1 genes, which most likely arose in an early amphibian by duplication of the ancestral PRL1 gene. The mRNA of cmPRL1 was predominantly expressed in the pituitary, but was considerably less abundant than has been previously reported for bony fish and tetrapod PRL1s; the copy number of cmPRL1 mRNA in the pituitary was less than 1% and 0.1% of that of GH and pro-opiomelanocortin mRNAs, respectively. The cells expressing cmPRL1 mRNA were sparsely distributed in the rostral pars distalis. Our findings provide a new insight into the studies on molecular and functional evolution of PRL1 in vertebrates.
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Evolución Biológica , Pez Eléctrico/metabolismo , Evolución Molecular , Filogenia , Hipófisis/metabolismo , Prolactina/metabolismo , Secuencia de Aminoácidos , Animales , Clonación Molecular , Pez Eléctrico/crecimiento & desarrollo , Hibridación in Situ , Datos de Secuencia Molecular , Hipófisis/citología , Homología de Secuencia de Aminoácido , Distribución TisularRESUMEN
In marine cartilaginous fish, reabsorption of filtered urea by the kidney is essential for retaining a large amount of urea in their body. However, the mechanism for urea reabsorption is poorly understood due to the complexity of the kidney. To address this problem, we focused on elephant fish (Callorhinchus milii) for which a genome database is available, and conducted molecular mapping of membrane transporters along the different segments of the nephron. Basically, the nephron architecture of elephant fish was similar to that described for elasmobranch nephrons, but some unique features were observed. The late distal tubule (LDT), which corresponded to the fourth loop of the nephron, ran straight near the renal corpuscle, while it was convoluted around the tip of the loop. The ascending and descending limbs of the straight portion were closely apposed to each other and were arranged in a countercurrent fashion. The convoluted portion of LDT was tightly packed and enveloped by the larger convolution of the second loop that originated from the same renal corpuscle. In situ hybridization analysis demonstrated that co-localization of Na(+),K(+),2Cl(-) cotransporter 2 and Na(+)/K(+)-ATPase α1 subunit was observed in the early distal tubule and the posterior part of LDT, indicating the existence of two separate diluting segments. The diluting segments most likely facilitate NaCl absorption and thereby water reabsorption to elevate urea concentration in the filtrate, and subsequently contribute to efficient urea reabsorption in the final segment of the nephron, the collecting tubule, where urea transporter-1 was intensely localized.
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Pez Eléctrico/anatomía & histología , Pez Eléctrico/metabolismo , Túbulos Renales Colectores/anatomía & histología , Túbulos Renales Colectores/metabolismo , Animales , Clonación Molecular , Proteínas de Peces/genética , Proteínas de Peces/metabolismo , Inmunohistoquímica , Hibridación in Situ , Modelos Biológicos , Filogenia , Subunidades de Proteína/genética , Subunidades de Proteína/metabolismo , ARN Mensajero/genética , ARN Mensajero/metabolismoRESUMEN
In animal communication, the social context that elicits particular dynamic changes in the signal can provide indirect clues to signal function. Female presence should increase the expression of male signal traits relevant for mate-choice, while male presence should promote the enhancement of traits involved in male-male competition. The electric fish Brachyhypopomus gauderio produces a biphasic electric pulse for electrolocation and communication. Pulse amplitude predicts the signaler's body size while pulse duration predicts circulating androgen levels. Males enhance pulse amplitude and duration when the numbers of males and females increase simultaneously. Here we tested the relative effects of female presence and male presence on male signal enhancement, and whether the size of the male competitor affected this enhancement. We found that male presence drives the enhancement of both pulse amplitude and second phase duration, independently of the size of the male competitor. Female presence induces the enhancement of pulse duration, but not pulse amplitude. These data suggest that males probably attend to information about a competitor's body size coded by pulse amplitude and attend to aggressiveness coded by a competitor's pulse duration, both potential predictors of fight outcome. Females may be primarily concerned about information on reproductive condition coded by pulse duration.
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Comunicación Animal , Señales (Psicología) , Pez Eléctrico/fisiología , Órgano Eléctrico/fisiología , Plasticidad Neuronal , Conducta Social , Andrógenos/metabolismo , Animales , Conducta Competitiva , Pez Eléctrico/metabolismo , Órgano Eléctrico/efectos de los fármacos , Órgano Eléctrico/metabolismo , Femenino , Antagonistas de Hormonas/farmacología , Masculino , Preferencia en el Apareamiento Animal , Melanocortinas/metabolismo , Potenciales de la Membrana , Plasticidad Neuronal/efectos de los fármacos , Receptores de Melanocortina/antagonistas & inhibidores , Receptores de Melanocortina/metabolismo , Factores Sexuales , Detección de Señal Psicológica , Factores de TiempoRESUMEN
The ability to regenerate tissues is shared across many metazoan taxa, yet the type and extent to which multiple cellular mechanisms come into play can differ across species. For example, urodele amphibians can completely regenerate all lost tissues, including skeletal muscles after limb amputation. This remarkable ability of urodeles to restore entire limbs has been largely linked to a dedifferentiation-dependent mechanism of regeneration. However, whether cell dedifferentiation is the fundamental factor that triggers a robust regeneration capacity, and whether the loss or inhibition of this process explains the limited regeneration potential in other vertebrates is not known. Here, we studied the cellular mechanisms underlying the repetitive regeneration of myogenic tissues in the electric fish S. macrurus. Our in vivo microinjection studies of high molecular weight cell lineage tracers into single identified adult myogenic cells (muscle or noncontractile muscle-derived electrocytes) revealed no fragmentation or cellularization proximal to the amputation plane. In contrast, ultrastructural and immunolabeling studies verified the presence of myogenic stem cells that express the satellite cell marker Pax7 in mature muscle fibers and electrocytes of S. macrurus. These data provide the first example of Pax-7 positive muscle stem cells localized within a non-contractile electrogenic tissue. Moreover, upon amputation, Pax-7 positive cells underwent a robust replication and were detected exclusively in regions that give rise to myogenic cells and dorsal spinal cord components revealing a regeneration process in S. macrurus that is dependent on the activation of myogenic stem cells for the renewal of both skeletal muscle and the muscle-derived electric organ. These data are consistent with the emergent concept in vertebrate regeneration that different tissues provide a distinct progenitor cell population to the regeneration blastema, and these progenitor cells subsequently restore the original tissue.
Asunto(s)
Pez Eléctrico/metabolismo , Fibras Musculares Esqueléticas/metabolismo , Factor de Transcripción PAX7/metabolismo , Secuencia de Aminoácidos , Animales , Órgano Eléctrico/citología , Órgano Eléctrico/metabolismo , Datos de Secuencia Molecular , Contracción Muscular/fisiología , Fibras Musculares Esqueléticas/citología , Factor de Transcripción PAX7/genética , Homología de Secuencia de AminoácidoRESUMEN
Gymnotiform weakly electric fishes generate electric organ discharges (EODs) and sense perturbations of the resulting electric field for purposes of orientation, prey detection and communication. Some species produce oscillatory ('wave-type') EODs at very high frequencies (up to 2 kHz) that have been proposed to be energetically expensive. If high-frequency EODs are expensive, then fish may modulate their EOD frequency and/or amplitude in response to low-oxygen (hypoxic) stress and/or compensate for costs of signalling through other adaptations that maximize oxygen uptake efficiency. To test for evidence of an energetic cost of signalling, we recorded EOD in conjunction with metabolic rates, critical oxygen tension and aquatic surface respiration (ASR(90)) thresholds in Apteronotus leptorhynchus, a species found in high-oxygen habitats, and Eigenmannia virescens, a species more typically found in low-oxygen waters. Eigenmannia virescens had a lower mean ASR(90) threshold and critical oxygen tension compared with A. leptorhynchus, consistent with field distributions. Within each species, there was no evidence for a relationship between metabolic rate and either EOD frequency or amplitude under normoxia, suggesting that there is no significant direct metabolic cost associated with producing a higher frequency EOD. However, when exposed to progressive hypoxia, fish generally responded by reducing EOD amplitude, which may reduce energetic costs. The threshold at which fish reduced EOD amplitude tended to be lower in E. virescens, a pattern consistent with higher tolerance to hypoxic stress. The results of this study suggest that wave-type fish reduce their EOD amplitude to reduce direct energetic costs without reducing metabolic rate under hypoxia.