RESUMEN
While the chemical signals guiding neuronal migration and axon elongation have been extensively studied, the influence of mechanical cues on these processes remains poorly studied in vivo. Here, we investigate how mechanical forces exerted by surrounding tissues steer neuronal movements and axon extension during the morphogenesis of the olfactory placode in zebrafish. We mainly focus on the mechanical contribution of the adjacent eye tissue, which develops underneath the placode through extensive evagination and invagination movements. Using quantitative analysis of cell movements and biomechanical manipulations, we show that the developing eye exerts lateral traction forces on the olfactory placode through extracellular matrix, mediating proper morphogenetic movements and axon extension within the placode. Our data shed new light on the key participation of intertissue mechanical interactions in the sculpting of neuronal circuits.
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Vías Olfatorias , Pez Cebra , Animales , Axones/fisiología , Ectodermo , Morfogénesis , Neurogénesis , Vías Olfatorias/anatomía & histología , Vías Olfatorias/fisiología , Pez Cebra/anatomía & histología , Pez Cebra/fisiologíaRESUMEN
Lake Malawi cichlid fishes exhibit extensive divergence in form and function built from a relatively small number of genetic changes. We compared the genomes of rock- and sand-dwelling species and asked which genetic variants differed among the groups. We found that 96% of differentiated variants reside in non-coding sequence but these non-coding diverged variants are evolutionarily conserved. Genome regions near differentiated variants are enriched for craniofacial, neural and behavioral categories. Following leads from genome sequence, we used rock- vs. sand-species and their hybrids to (i) delineate the push-pull roles of BMP signaling and irx1b in the specification of forebrain territories during gastrulation and (ii) reveal striking context-dependent brain gene expression during adult social behavior. Our results demonstrate how divergent genome sequences can predict differences in key evolutionary traits. We highlight the promise of evolutionary reverse genetics-the inference of phenotypic divergence from unbiased genome sequencing and then empirical validation in natural populations.
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Conducta Animal , Evolución Biológica , Encéfalo/fisiología , Genoma , Genómica , Animales , Cíclidos/clasificación , Cíclidos/fisiología , Genómica/métodos , Filogenia , TranscriptomaRESUMEN
BACKGROUND: Metamorphosis in marine species is characterized by profound changes at the ecophysiological, morphological, and cellular levels. The cnidarian Clytia hemisphaerica exhibits a triphasic life cycle that includes a planula larva, a colonial polyp, and a sexually reproductive medusa. Most studies so far have focused on the embryogenesis of this species, whereas its metamorphosis has been only partially studied. RESULTS: We investigated the main morphological changes of the planula larva of Clytia during the metamorphosis, and the associated cell proliferation and apoptosis. Based on our observations of planulae at successive times following artificial metamorphosis induction using GLWamide, we subdivided the Clytia's metamorphosis into a series of eight morphological stages occurring during a pre-settlement phase (from metamorphosis induction to planula ready for settlement) and the post-settlement phase (from planula settlement to primary polyp). Drastic morphological changes prior to definitive adhesion to the substrate were accompanied by specific patterns of stem-cell proliferation as well as apoptosis in both ectoderm and endoderm. Further waves of apoptosis occurring once the larva has settled were associated with morphogenesis of the primary polyp. CONCLUSION: Clytia larval metamorphosis is characterized by distinct patterns of apoptosis and cell proliferation during the pre-settlement phase and the settled planula-to-polyp transformation.
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Hidrozoos/crecimiento & desarrollo , Metamorfosis Biológica/fisiología , Animales , Apoptosis/fisiología , Polaridad Celular , Proliferación Celular/fisiología , Larva , Estadios del Ciclo de Vida/fisiología , Células Madre/fisiologíaRESUMEN
Jellyfish (medusae) are a distinctive life-cycle stage of medusozoan cnidarians. They are major marine predators, with integrated neurosensory, muscular and organ systems. The genetic foundations of this complex form are largely unknown. We report the draft genome of the hydrozoan jellyfish Clytia hemisphaerica and use multiple transcriptomes to determine gene use across life-cycle stages. Medusa, planula larva and polyp are each characterized by distinct transcriptome signatures reflecting abrupt life-cycle transitions and all deploy a mixture of phylogenetically old and new genes. Medusa-specific transcription factors, including many with bilaterian orthologues, associate with diverse neurosensory structures. Compared to Clytia, the polyp-only hydrozoan Hydra has lost many of the medusa-expressed transcription factors, despite similar overall rates of gene content evolution and sequence evolution. Absence of expression and gene loss among Clytia orthologues of genes patterning the anthozoan aboral pole, secondary axis and endomesoderm support simplification of planulae and polyps in Hydrozoa, including loss of bilateral symmetry. Consequently, although the polyp and planula are generally considered the ancestral cnidarian forms, in Clytia the medusa maximally deploys the ancestral cnidarian-bilaterian transcription factor gene complement.
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Hidrozoos , Animales , Evolución Molecular , GenomaRESUMEN
Every model species requires its own developmental table. Astyanax mexicanus, a teleost fish comprising both sighted river and blind cave populations, is becoming more and more important in the field of developmental and evolutionary biology. As such, a developmental staging table is increasingly necessary, particularly since comparative analysis of early developmental events is widely employed by researchers. We collected freshly spawned embryos from surface fish and Pachón cavefish populations. Embryos were imaged every 10-12 min during the first day of development, and less frequently in the following days. The results provide an illustrated comparison of selected developmental stages from one cell to hatching of these two populations. The two morphs show an essentially synchronous development regarding major events such as epiboly, neurulation, somitogenesis, heart beating, or hatching. We also present data on particular morphological characters appearing during larval development, such as eye size, yolk regression, swim bladder, and fin development. Some details about the development of F1 Pachón cave×surface hybrids are also given. Comparisons are made with Danio rerio (zebrafish) development.
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Characidae/embriología , Modelos Animales , Morfogénesis , Animales , Characidae/crecimiento & desarrollo , Femenino , Hibridación Genética , Larva/crecimiento & desarrollo , Masculino , Valores de Referencia , Pez Cebra/embriología , Pez Cebra/crecimiento & desarrolloRESUMEN
Brains develop under the influence of signaling centers that link major dorsal/ventral (DV) and anterior/posterior (AP) axes. Over ontogeny, these 'developmental neuraxes' progress from near global signaling gradients into more localized gene expression domains separated by molecular boundaries. Therefore, developmental changes along a neuraxis can have major consequences across the brain, or more precise effects on a specific structure, depending upon the time during ontogeny in which change occurs. It is well known from mammalian systems how evolution has acted later in development, via differential neurogenesis, to reshape the cortex. Recent studies in fishes show how early changes in DV and AP patterning result in divergence of integrated brain regions that ultimately define visual versus olfactory ecotypes. We explore the generality of this trend and suggest that such early developmental differences integrating brain diversification along the neuraxes may be a common theme in vertebrates. Early differences in brain patterning among species imply that adult variation in sensory function and behavior manifests in the embryo.
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Encéfalo/embriología , Neurogénesis , Vertebrados/embriología , Animales , Evolución Biológica , Tipificación del Cuerpo , Linaje de la Célula , Inducción Embrionaria , Peces/embriología , Regulación del Desarrollo de la Expresión Génica , Modelos Biológicos , Morfogénesis , Proteínas del Tejido Nervioso/fisiología , Tamaño de los Órganos , Olfato/fisiología , Especificidad de la Especie , Factores de Transcripción/fisiología , Vertebrados/genética , Visión Ocular/fisiología , Proteínas Wnt/fisiologíaRESUMEN
The cavefish morph of the Mexican tetra (Astyanax mexicanus) is blind at adult stage, although an eye that includes a retina and a lens develops during embryogenesis. There are, however, two major defects in cavefish eye development. One is lens apoptosis, a phenomenon that is indirectly linked to the expansion of ventral midline sonic hedgehog (Shh) expression during gastrulation and that induces eye degeneration. The other is the lack of the ventral quadrant of the retina. Here, we show that such ventralisation is not extended to the entire forebrain because fibroblast growth factor 8 (Fgf8), which is expressed in the forebrain rostral signalling centre, is activated 2 hours earlier in cavefish embryos than in their surface fish counterparts, in response to stronger Shh signalling in cavefish. We also show that neural plate patterning and morphogenesis are modified in cavefish, as assessed by Lhx2 and Lhx9 expression. Inhibition of Fgf receptor signalling in cavefish with SU5402 during gastrulation/early neurulation mimics the typical surface fish phenotype for both Shh and Lhx2/9 gene expression. Fate-mapping experiments show that posterior medial cells of the anterior neural plate, which lack Lhx2 expression in cavefish, contribute to the ventral quadrant of the retina in surface fish, whereas they contribute to the hypothalamus in cavefish. Furthermore, when Lhx2 expression is rescued in cavefish after SU5402 treatment, the ventral quadrant of the retina is also rescued. We propose that increased Shh signalling in cavefish causes earlier Fgf8 expression, a crucial heterochrony that is responsible for Lhx2 expression and retina morphogenesis defect.
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Ojo/patología , Factor 8 de Crecimiento de Fibroblastos/metabolismo , Peces/embriología , Peces/metabolismo , Proteínas Hedgehog/metabolismo , Prosencéfalo/metabolismo , Animales , Peces/anatomía & histología , Morfogénesis , Proteínas del Tejido Nervioso , Tamaño de los Órganos , RetinaRESUMEN
The larvae of the fish Astyanax mexicanus transiently develop a flat and adhesive structure on the top of their heads that we have called "the casquette" (cas, meaning "hat"). We hypothesized that the cas may be a teleostean homolog of the well-studied Xenopus cement gland, despite their different positions and structures. Here we show that the cas has an ectodermal origin, secretes mucus, expresses bone morphogenic protein 4 (Bmp4) and pituitary homeobox 1/2 (Pitx1/2), is innervated by the trigeminal ganglion and serotonergic raphe neurons, and has a role in the control and the development of the larval swimming behavior. These developmental, connectivity, and behavioral functional data support a level of deep homology between the frog cement gland and the Astyanax cas and suggest that attachment organs can develop in varied positions on the head ectoderm by recruitment of a Bmp4-dependent developmental module. We also show that the attachment organs of the cichlid Tilapia mariae larvae display some of these features. We discuss the possibility that these highly diversified attachment glands may be ancestral to chordates and have been lost repetitively in many vertebrate classes.
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Glándulas Exocrinas , Peces/anatomía & histología , Peces/embriología , Peces/crecimiento & desarrollo , Cabeza/anatomía & histología , Animales , Conducta Animal/fisiología , Proteína Morfogenética Ósea 4/genética , Proteína Morfogenética Ósea 4/metabolismo , Glándulas Exocrinas/anatomía & histología , Glándulas Exocrinas/fisiología , Peces/genética , Proteínas de Homeodominio/genética , Proteínas de Homeodominio/metabolismo , Datos de Secuencia Molecular , Moco/metabolismo , Factores de Transcripción Paired Box/genética , Factores de Transcripción Paired Box/metabolismo , Natación/fisiología , Factores de Transcripción/genética , Factores de Transcripción/metabolismo , Ganglio del Trigémino/anatomía & histología , Proteína del Homeodomínio PITX2RESUMEN
One of the goals of evolutionary developmental biology is to link specific adaptations to changes in developmental pathways. The dentition of cypriniform fishes, which in contrast to many other teleost fish species possess pharyngeal teeth but lack oral teeth, provides a suitable model to study the development of feeding adaptations. Here, we have examined the involvement of retinoic acid (RA) in tooth development and show that RA is specifically required to induce the pharyngeal tooth developmental program in zebrafish. Perturbation of RA signaling at this stage abolished tooth induction without affecting the development of tooth-associated ceratobranchial bones. We show that this inductive event is dependent on RA synthesis from aldh1a2 in the ventral posterior pharynx. Fibroblast growth factor (FGF) signaling has been shown to be critical for tooth induction in zebrafish, and its loss has been associated with oral tooth loss in cypriniform fishes. Pharmacological treatments targeting the RA and FGF pathways revealed that both pathways act independently during tooth induction. In contrast, we find that in Mexican tetra and medaka, species that also possess oral teeth, both oral and pharyngeal teeth are induced independently of RA. Our analyses suggest an evolutionary scenario in which the gene network controlling tooth development obtained RA dependency in the lineage leading to the cypriniforms. The loss of pharyngeal teeth in this group was cancelled out through a shift in aldh1a2 expression, while oral teeth might have been lost ultimately due to deficient RA signaling in the oral cavity.
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Dentición , Peces/embriología , Peces/metabolismo , Oryzias/embriología , Oryzias/metabolismo , Tretinoina/metabolismo , Pez Cebra/embriología , Pez Cebra/metabolismo , Aldehído Deshidrogenasa/genética , Aldehído Deshidrogenasa/metabolismo , Animales , Factores de Crecimiento de Fibroblastos/genética , Factores de Crecimiento de Fibroblastos/fisiología , Proteínas de Peces/genética , Proteínas de Peces/metabolismo , Regulación del Desarrollo de la Expresión Génica/efectos de los fármacos , Regulación del Desarrollo de la Expresión Génica/genética , Hibridación in Situ , Datos de Secuencia Molecular , Faringe/embriología , Faringe/metabolismo , Receptores de Ácido Retinoico/agonistas , Receptores de Ácido Retinoico/antagonistas & inhibidores , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Transducción de Señal/efectos de los fármacos , Transducción de Señal/genéticaRESUMEN
The blind cavefish and its surface counterpart of the teleost species Astyanax mexicanus constitute an excellent model to study the evolution of morphological features. During adaptation to their lives in perpetual darkness, the cave population has lost eyes (and pigmentation), but has gained several constructive traits. Recently, the demonstration that an increase in Shh (Sonic Hedgehog) midline signalling was indirectly responsible for the loss of eyes in cavefish led to new ways to search for possible modifications in the forebrain of these cavefish, as this anterior-most region of the vertebrate central nervous system develops under close control of the powerful Shh morphogen. In this review, we summarize the recent progress in the understanding of forebrain and eye modifications in cavefish. These include major changes in cell death, cell proliferation and cell migration in various parts of the forebrain when compared with their surface counterparts with eyes. The outcome of these modifications, in terms of neuronal circuitry, morphological and behavioral adaptations are discussed.