RESUMO
Active electroreception-the ability to detect objects and communicate with conspecifics via the detection and generation of electric organ discharges (EODs)-has evolved convergently in several fish lineages. South American electric fishes (Gymnotiformes) are a highly species-rich group, possibly in part due to evolution of an electric organ (EO) that can produce diverse EODs. Neofunctionalization of a voltage-gated sodium channel gene accompanied the evolution of electrogenic tissue from muscle and resulted in a novel gene (scn4aa) uniquely expressed in the EO. Here, we investigate the link between variation in scn4aa and differences in EOD waveform. We combine gymnotiform scn4aa sequences encoding the C-terminus of the Nav1.4a protein, with biogeographic data and EOD recordings to test whether physiological transitions among EOD types accompany differential selection pressures on scn4aa. We found positive selection on scn4aa coincided with shifts in EOD types. Species that evolved in the absence of predators, which likely selected for reduced EOD complexity, exhibited increased scn4aa evolutionary rates. We model mutations in the protein that may underlie changes in protein function and discuss our findings in the context of gymnotiform signalling ecology. Together, this work sheds light on the selective forces underpinning major evolutionary transitions in electric signal production.
Assuntos
Peixe Elétrico , Animais , Peixe Elétrico/genética , Órgão Elétrico/fisiologia , Filogenia , Canais de Sódio/genética , América do SulRESUMO
Secretoneurin (SN) in the preoptic area and pituitary of mammals and fish has a conserved close association with the vasopressin and oxytocin systems, members of a peptide family that are key in the modulation of sexual and social behaviors. Here we show the presence of SN-immunoreactive cells and projections in the brain of the electric fish, Brachyhypopomus gauderio. Secretoneurin colocalized with vasotocin (AVT) and isotocin in cells and fibers of the preoptic area. In the rostral pars distalis of the pituitary, many cells were both SN and prolactin-positive. In the hindbrain, at the level of the command nucleus of the electric behavior (pacemaker nucleus; PN), some of SN-positive fibers colocalized with AVT. We also explored the potential neuromodulatory role of SN on electric behavior, specifically on the rate of the electric organ discharge (EOD) that signals arousal, dominance and subordinate status. Each EOD is triggered by the command discharge of the PN, ultimately responsible for the basal EOD rate. SN modulated diurnal basal EOD rate in freely swimming fish in a context-dependent manner; determined by the initial value of EOD rate. In brainstem slices, SN partially mimicked the in vivo behavioral effects acting on PN firing rate. Taken together, our results suggest that SN may regulate electric behavior, and that its effect on EOD rate may be explained by direct action of SN at the PN level through either neuroendocrine and/or endocrine mechanisms.
Assuntos
Peixe Elétrico/genética , Neuropeptídeos/metabolismo , Secretogranina II/metabolismo , Vasotocina/metabolismo , AnimaisRESUMO
One of the most remarkable examples of convergent evolution among vertebrates is illustrated by the independent origins of an active electric sense in South American and African weakly electric fishes, the Gymnotiformes and Mormyroidea, respectively. These groups independently evolved similar complex systems for object localization and communication via the generation and reception of weak electric fields. While good estimates of divergence times are critical to understanding the temporal context for the evolution and diversification of these two groups, their respective ages have been difficult to estimate due to the absence of an informative fossil record, use of strict molecular clock models in previous studies, and/or incomplete taxonomic sampling. Here, we examine the timing of the origins of the Gymnotiformes and the Mormyroidea using complete mitogenome sequences and a parametric bayesian method for divergence time reconstruction. Under two different fossil-based calibration methods, we estimated similar ages for the independent origins of the Mormyroidea and Gymnotiformes. Our absolute estimates for the origins of these groups either slightly postdate, or just predate, the final separation of Africa and South America by continental drift. The most recent common ancestor of the Mormyroidea and Gymnotiformes was found to be a non-electrogenic basal teleost living more than 85 millions years earlier. For both electric fish lineages, we also estimated similar intervals (16-19 or 22-26 million years, depending on calibration method) between the appearance of electroreception and the origin of myogenic electric organs, providing rough upper estimates for the time periods during which these complex electric organs evolved de novo from skeletal muscle precursors. The fact that the Gymnotiformes and Mormyroidea are of similar age enhances the comparative value of the weakly electric fish system for investigating pathways to evolutionary novelty, as well as the influences of key innovations in communication on the process of species radiation.
Assuntos
Peixe Elétrico/classificação , Peixe Elétrico/genética , Gimnotiformes/classificação , Gimnotiformes/genética , África , Animais , Teorema de Bayes , DNA Mitocondrial/genética , Peixe Elétrico/anatomia & histologia , Peixe Elétrico/fisiologia , Órgão Elétrico/fisiologia , Evolução Molecular , Fósseis , Duplicação Gênica , Genoma Mitocondrial , Gimnotiformes/anatomia & histologia , Gimnotiformes/fisiologia , Funções Verossimilhança , Músculo Esquelético/fisiologia , Filogenia , América do Sul , Fatores de TempoRESUMO
Chromosomes of a species of Eigenmannia presenting a X1X1X2X2:X1X2Y sex chromosome system, resulting from a Y-autosome Robertsonian translocation, were analyzed using the C-banding technique, chromomycin A3 (CMA3) and mithramycin (MM) staining and in situ digestion by the restriction endonuclease AluI. A comparison of the metacentric Y chromosome of males with the corresponding acrocentrics in females indicated that a C-band-positive, CMA3/MM-fluorescent and AluI digestion-resistant region had been lost during the process of translocation, resulting in a diminution of heterochromatin in the males. It is hypothesized that the presence of a smaller amount of G + C-rich heterochromatin in the sex chromosomes of the heteromorphic sex when compared with the homomorphic sex may be associated with the sex determination mechanism in this species and may be a more widely occurring phenomenon in fish with differentiated sex chromosomes than was initially thought.
Assuntos
Evolução Biológica , Peixe Elétrico/genética , Cromossomos Sexuais/genética , Animais , Cromomicina A3/química , Feminino , Heterocromatina , Cariotipagem , Masculino , Plicamicina/química , Mapeamento por Restrição , Diferenciação Sexual , Coloração pela Prata/métodos , Translocação GenéticaRESUMO
An investigation was conducted on six populations of Gymnotus carapo from the Upper Parana river system in Brazil. A wide variability of the NOR-bearing chromosomes was found involving paracentric inversions in the heterochromatic regions associated with NORs, resulting in 5 NOR chromosome phenotypes. The distribution of the distinct NOR phenotypes varied both inter- and intrapopulationally. Results obtained using an exact test revealed that the six populations are in Hardy-Weinberg equilibrium. Although NOR size polymorphism is quite a common occurrence in fish karyotypes, this is the first description of a balanced polymorphism involving 3 different NOR chromosomes in 5 combinations.
Assuntos
Peixe Elétrico/genética , Região Organizadora do Nucléolo/genética , Polimorfismo Genético , Animais , Feminino , Variação Genética , Masculino , Fenótipo , FilogeniaRESUMO
In this report we generate a partial phylogeny of the mormyriform fishes using mitochondrial DNA sequences from twelve species of mormyriforms belonging to five genera. Electric organs and electric organ discharges are also examined. We have sequenced and aligned 373 bases from the mitochondrial 12S rRNA and 559 bases from the 16s rRNA from fourteen species of the superorder Osteoglossomorpha. Two non-mormyriform genera were used as outgroups. Three phylogenetic methods generated concordant partial phylogenies for these fish. Our analysis focuses on the genus Brienomyrus, which is a heterogeneous clade with at least eleven nominal species. Six morphs from Gabon had distinctive EODs but were morphologically 'cryptic' in that they all had the brachyistius-like body morphology. DNA analysis fully supports the EOD data that the six morphs represent distinct clades. The group from Gabon is monophyletic, while B. brachyistius from West Africa is a separate lineage. B. niger, a second distinct lineage, is a sister group to the six species from Gabon. Petrocephalus is the sister group of all the genera of the subfamily Mormyrinae so far analyzed, thereby confirming previous osteological results. Gymnarchus niloticus is the sister group of the family Mormyridae, also confirming an earlier phylogenetic hypothesis based on morphology. The molecular data adds polarity to electric organ characteristics. Stalkless electrocytes appear to be primitive. Petrocephalus, with non-penetrating stalked electrocytes innervated on the posterior side, represents an ancestral state for the Mormyridae, while Marcusenius. Brienomyrus and Gnathonemus with penetrating-stalked electrocytes, represent the apomorphic condition. Two species with doubly-penetrating electrocytes innervated on the posterior side may represent a transitional stage. At least two species of Brienomyrus appear to have reverted to non-penetrating stalked electrocytes, possibly through paedomorphosis.
Assuntos
Evolução Biológica , Peixe Elétrico/classificação , Órgão Elétrico , Animais , Sequência de Bases , DNA , DNA Mitocondrial , Peixe Elétrico/anatomia & histologia , Peixe Elétrico/genética , Órgão Elétrico/anatomia & histologia , Feminino , Masculino , Dados de Sequência Molecular , Filogenia , RNA Ribossômico/genética , RNA Ribossômico 16S/genética , Análise de Sequência de DNARESUMO
Fish cytogenetics has incorporated during the last years new methodologies that employ molecular techniques, such as in situ hybridization with DNA probes for localization of chromosomal segments, chromosome banding using in situ digestion with restriction enzymes, in vivo incorporation of DNA base analogues, base-specific fluorochrome staining and, more recently, immunolabelling of chromosomes with antinucleoside antibodies. These techniques, associated with results obtained by using classical cytogenetic markers such as C-bands and nucleolus organizer regions, have allowed a more comprehensive understanding of the molecular structure of chromosomes and enlarged the area of cytogenetic evolutive studies. In neotropical fish the use of these modern techniques resulted in the localization of rDNA segments and the analysis of their activity; the localization of telomeric DNA segments; the identification of C-band modified patterns in species analyzed by in situ digestion of chromosomes with restriction endonucleases; the identification of R-handing patterns after incorporation of 5-bromodeoxyuridine; and, using the antibody antimethylcytosine, the identification of the methylated state of the heterochromatin in diploids and triploids.
Assuntos
Animais , Masculino , Feminino , Cromossomos , Sondas de DNA , Peixes/genética , Hibridização In Situ , Brasil , Bandeamento Cromossômico , Peixes/imunologia , Água Doce , Estrutura Molecular , Peixe Elétrico/genéticaRESUMO
Nucleolus organizer regions (NORs) were analysed in two related and geographically close populations of Eigenmannia sp.1 (Pisces, Gymnotoidei, Sternopygidae) using silver staining and fluorescence in situ hybridization (FISH). The two populations differed in their Ag-NOR phenotypes, displaying fixed differences in the NOR-bearing chromosome pairs. FISH with rDNA probes showed that these differences were due to the location of rDNA cistrons. This finding, showing fixed NOR differences between two populations belonging to the same species in a connected river system, is highly significant in terms of evolutionary change, possibly indicating an initial step of genetic differentiation. This result also has important implications from the cytosystematic point of view, as NORs usually have a very constant karyotypic location in fish species and have been used as species-specific chromosome markers.
Assuntos
Sondas de DNA , DNA Ribossômico , Peixe Elétrico/genética , Hibridização in Situ Fluorescente/métodos , Região Organizadora do Nucléolo/genética , Animais , Brasil , Bandeamento Cromossômico , Feminino , Cariotipagem , Masculino , FenótipoRESUMO
The order Gymnotiformes (South American electric fishes) is a fascinating assemblage of freshwater fishes that share the unusual ability to produce and sense electric fields used for electrolocation and social communication. In the last few decades, the electrogenic and electrosensory systems (EES) of these fish have served as an excellent model to study motor and sensory physiology in vertebrates. In an attempt to the evolution of characters associated with the EES in the group, we applied maximum-parsimony (MP), minimum-evolution (ME), and maximum-likelihood (ML) methods to analyze 302 aligned bases of the mitochondrial 12S rRNA and 416 bases of the mitochondrial 16S rRNA of 19 gymnotiform genera representing all six recognized families. Six catfish genera (order Siluriformes) were also sequenced and used as outgroups. The phylogenetic hypothesis resultant from molecular data analysis differs in some respects from previous hypotheses based on morphological studies. Our results were most informative within the family level, as we were unable to elucidate the relationships among deeper branches in this order with sufficient confidence by using molecular data alone. The phylogenetic information of both mitochondrial DNA segments appears to be affected by functional constraints, and the resultant topologies were sensitive to different weighting schemes and the algorithm used. Nonetheless, we found unanimous support for the following phylogenetic relationships: (1) the family Sternopygidae is an unnatural group, and Sternopygus is the sole representative of a unique lineage within the order; (2) the family Hypopomidae is not monophyletic; and (3) the order Gymnotiformes is composed of at least six natural clades: Sternopygus, family Apteronotidae, a new clade consisting of the remaining sternopygids, families Hypopomidae + Rhamphicthyidae, family Electrophoridae, and family Gymnotidae. By combining molecular, morphological, and physiological information, we propose a new hypothesis for the phylogeny of this group and suggest a new family Eigenmanniidae n. (order Gymnotiformes).