RESUMO
Oxygen is a key regulator of both development and homeostasis and a promising candidate to bridge the influence of the environment and the evolution of new traits. To clarify the various ways in which oxygen may modulate embryogenesis, its effects are reviewed at distinct organizational levels. First, the role of pathways that sense dioxygen levels and reactive oxygen species are reviewed. Then, the effects of microenvironmental oxygen on metabolism, stemness, and differentiation throughout embryogenesis are discussed. Last, the interplay between ecology and development are reexamined with a focus on the evolution of tetrapods, including during the emergence of a novel mechanism that shapes amniote limbs-interdigital cell death. Both genetic and environmental components work together during the formation of organisms, highlighting the importance of a multidisciplinary approach for understanding the evolution of new traits.
Assuntos
Ecologia , Oxigênio , Evolução Biológica , Extremidades , Fenótipo , Espécies Reativas de OxigênioRESUMO
Interdigital cell death is an important mechanism employed by amniotes to shape their limbs; inhibiting this process leads to the formation of webbed fingers, as seen in bats and ducks. The Chinese softshell turtle Pelodiscus sinensis (Reptilia: Testudines: Trionychidae) has a distinctive limb morphology: the anterior side of the limbs has partially webbed fingers with claw-like protrusions, while the posterior fingers are completely enclosed in webbings. Here, P. sinensis embryos were investigated to gain insights on the evolution of limb-shaping mechanisms in amniotes. We found cell death and cell senescence in their interdigital webbings. Spatial or temporal modulation of these processes were correlated with the appearance of indentations in the webbings, but not a complete regression of this tissue. No differences in interdigital cell proliferation were found. In subsequent stages, differential growth of the finger cartilages led to a major difference in limb shape. While no asymmetry in bone morphogenetic protein signaling was evident during interdigital cell death stages, some components of this pathway were expressed exclusively in the clawed digit tips, which also had earlier ossification. In addition, a delay and/or truncation in the chondrogenesis of the posterior digits was found in comparison with the anterior digits of P. sinensis, and also when compared with the previously published pattern of digit skeletogenesis of turtles without posterior webbings. In conclusion, modulation of cell death, as well as a heterochrony in digit chondrogenesis, may contribute to the formation of the unique limbs of the Chinese softshell turtles.
Assuntos
Embrião não Mamífero/embriologia , Desenvolvimento Embrionário , Extremidades/embriologia , Tartarugas/embriologia , AnimaisRESUMO
In amniotes, limb muscle precursors de-epithelialize from the ventral dermomyotome and individually migrate into limb buds. In catsharks, Scyliorhinus, fin muscle precursors are also derived from the ventral dermomyotome, but shortly after de-epithelialization, they reaggregate within the pectoral fin bud and differentiate into fin muscles. Delamination of muscle precursors has been suggested to be controlled by hepatocyte growth factor (HGF) and its tyrosine kinase receptor (MET) in amniotes. Here, we explore the possibility that HGF/MET signaling regulates the delamination of appendicular muscle precursors in embryos of the catshark Scyliorhinus canicula. Our analysis reveals that Hgf is expressed in pectoral fin buds, whereas c-Met expression in fin muscle precursors is rapidly downregulated. We propose that alteration of the duration of c-Met expression in appendicular muscle precursors might underlie the evolution of individually migrating muscle precursors, which leads to the emergence of complex appendicular muscular systems in amniotes.
Assuntos
Fator de Crescimento de Hepatócito/metabolismo , Músculo Esquelético/embriologia , Músculo Esquelético/metabolismo , Receptores Proteína Tirosina Quinases/metabolismo , Tubarões/embriologia , Tubarões/metabolismo , Transdução de Sinais , Animais , Desenvolvimento Muscular , Músculo Esquelético/citologia , Músculo Esquelético/enzimologiaRESUMO
In zebrafish, pelvic fin buds appear at 3 weeks post fertilization (wpf) during the larval to juvenile transition (metamorphosis), but their fate is already determined during embryogenesis. Thus, presumptive pelvic fin cells appear to memorize their positional information for three weeks, but no factors expressed in the pelvic fin field from the embryonic to the metamorphic stages have been identified. In mice, Islet1 is proposed to promote nuclear accumulation of ß-catenin in the hindlimb field, which leads to the initiation of hindlimb bud outgrowth through activation of the Wnt/ßcatenin pathway. Here, we examined the distribution of ß-catenin and islet proteins in the pelvic fin field of zebrafish from the embryonic to the metamorphic stages. We found that transcripts of islet2a, but not islet1, are detected in the posterior lateral plate mesoderm, including the presumptive pelvic fin field, at the embryonic stage as well as in the pelvic fin bud at the metamorphic stage. Immunolocalization revealed that ß-catenin and islet proteins, which are synthesized during the embryonic stage, remain in the cytoplasm of the presumptive pelvic fin cells during the larval stage, and are then translocated into the nuclei of the pelvic fin bud at the metamorphic stage. We propose that cytoplasmic localization of these proteins in the presumptive pelvic fin cells that remained during the larval stage may underlie the mechanism by which pelvic fin cells memorize their positional information from the embryonic stage to the metamorphic stage.
Assuntos
Nadadeiras de Animais/embriologia , Proteínas com Homeodomínio LIM/metabolismo , Fatores de Transcrição/metabolismo , Proteínas de Peixe-Zebra/metabolismo , Peixe-Zebra/embriologia , beta Catenina/metabolismo , Nadadeiras de Animais/crescimento & desenvolvimento , Animais , Proteínas com Homeodomínio LIM/genética , Larva , Mesoderma , Metamorfose Biológica , Transdução de Sinais , Fatores de Transcrição/genética , Peixe-Zebra/crescimento & desenvolvimento , Proteínas de Peixe-Zebra/genética , beta Catenina/genéticaRESUMO
The evolution from fins to limbs was one of the most successful innovations for vertebrates, allowing them to vastly expand their behaviors and habitats. Fossil records suggest that morphological changes occurred not only along the proximal-distal axis included appearance of the autopod, but also occurred along the anterior-posterior axis included reductions in the size and number of basal bones and digits. This review focuses on recent progress in developmental and genetic studies aimed at elucidating the mechanisms underlying alteration of anterior-posterior patterning and its accompanying changes along the proximal-distal axis during the fin-to-limb transition.
Assuntos
Nadadeiras de Animais , Evolução Biológica , Padronização Corporal , Extremidades , Animais , Padronização Corporal/genética , Evolução MolecularRESUMO
Little is known about the biogeographical and evolutionary histories of macaques (Macaca spp.) in East Asia because the phylogenetic positions of fossil species remain unclear. Here we examined the zygomaxillary remains of a fossil macaque (M. cf. robusta) from the Durubong Cave Complex, South Korea, that dates back to the late Middle to Late Pleistocene, to infer its phylogenetic relationship to extant species. We took 195 fixed- and semi-landmarks from the zygomaxillary regions of the fossil specimen and from 147 specimens belonging to 14 extant species. We then conducted a generalized Procrustes analysis followed by a multivariate statistical analysis to evaluate the phenetic affinities of the fossil to the extant species and reconstructed the most parsimonious phylogenetic tree using a phylogenetic morphometric approach. We found that the fossil was most similar to Macaca fuscata (Japanese macaque) in the zygomaxillary morphospace although it was at the limit of the range of variation for this species. The second closest in the morphospace was the continental Macaca mulatta (rhesus macaque). Parsimonious reconstruction confirmed that the fossil was most closely related to M. fuscata, even after controlling for the effects of allometry. These findings suggest that in the late Middle to Late Pleistocene, close relatives of M. fuscata that looked like the extant species were distributed on the Korean Peninsula, where no species of macaques are found today. Thus, some morphological characteristics of M. fuscata may have developed before its ancestor dispersed into the Japanese archipelago.
Assuntos
Fósseis/anatomia & histologia , Macaca mulatta/anatomia & histologia , Macaca mulatta/classificação , Maxila/anatomia & histologia , Filogenia , Animais , República da CoreiaRESUMO
Two major morphological changes occurred during the fin-to-limb transition: the appearance of the autopod, and the reduction of anterior skeletal elements. In the past decades, numerous approaches to the study of genetic developmental systems involved in patterning of fins/limbs among different taxa have provided clues to better understand the mechanism of the fin-to-limb transition. In this article, I discuss recent progress toward elucidating the evolutionary origin of the autopod and the mechanism through which the multiple-basal bones of ancestral fins were reduced into a single bone (humerus/femur). A particular focus of this article is the patterning mechanism of the tetrapod limb and chondrichthyan fin controlled by gene networks involving the 5'Hox genes, Gli3 and Shh. These recent data provide possible scenarios that could have led to the transformation of fins into limbs.
Assuntos
Nadadeiras de Animais/fisiologia , Evolução Biológica , Extremidades/fisiologia , Proteínas Hedgehog/metabolismo , Proteínas de Homeodomínio/metabolismo , Fatores de Transcrição/metabolismo , Proteínas de Peixe-Zebra/metabolismo , Animais , Padronização Corporal , Osso e Ossos , Evolução Molecular , Peixes , Regulação da Expressão Gênica no Desenvolvimento , Redes Reguladoras de Genes , Genes Homeobox , Família Multigênica , Proteína Gli3 com Dedos de ZincoRESUMO
Apoptosis is an important mechanism for sculpting morphology. However, the molecular cascades that control apoptosis in developing limb buds remain largely unclear. Here, we show that MafB was specifically expressed in apoptotic regions of chick limb buds, and MafB/cFos heterodimers repressed apoptosis, whereas MafB/cJun heterodimers promoted apoptosis for sculpting the shape of the limbs. Chromatin immunoprecipitation sequencing in chick limb buds identified potential target genes and regulatory elements controlled by Maf and Jun. Functional analyses revealed that expression of p63 and p73, key components known to arrest the cell cycle, was directly activated by MafB and cJun. Our data suggest that dimeric combinations of MafB, cFos and cJun in developing chick limb buds control the number of apoptotic cells, and that MafB/cJun heterodimers lead to apoptosis via activation of p63 and p73.
Assuntos
Apoptose , Extremidades/embriologia , Fator de Transcrição MafB/metabolismo , Morfogênese , Multimerização Proteica , Proteínas Proto-Oncogênicas c-fos/metabolismo , Proteínas Proto-Oncogênicas c-jun/metabolismo , Animais , Sítios de Ligação , Proteínas Morfogenéticas Ósseas/metabolismo , Sobrevivência Celular , Embrião de Galinha , Galinhas , Regulação para Baixo/genética , Perfilação da Expressão Gênica , Regulação da Expressão Gênica no Desenvolvimento , Botões de Extremidades/citologia , Botões de Extremidades/embriologia , Botões de Extremidades/metabolismo , Macrófagos/metabolismo , Fator de Transcrição MafB/genética , Modelos Biológicos , Morfogênese/genética , Ligação Proteica , Proteínas Proto-Oncogênicas c-fos/genética , Proteínas Proto-Oncogênicas c-jun/genética , Transdução de Sinais/genética , Fator de Transcrição AP-1/metabolismo , Tretinoína/metabolismoRESUMO
Paired limbs were acquired in the ancestor of tetrapods and their morphology has been highly diversified in amniotes in relation to the adaptive radiation to the terrestrial environment. These morphological changes may have been induced by modification of the developmental program of the skeletal or muscular system. To complete limb modification, it is also important to change the neuronal framework, because the functions of the limbs rely on neural circuits that involve coordinated movement. Previous studies have shown that class 3 semaphorins (Sema3 semaphorins), which act as repulsive axonal guidance cues, play a crucial role in the formation of the peripheral nerves in mice. Here, we studied the expression pattern of Sema3A orthologues in embryos of developing amniotes, including mouse, chick, soft-shelled turtle, and ocelot gecko. Sema3A transcripts were expressed in restricted mesenchymal parts of the developing limb primordium in all animals studied, and developing spinal nerves appeared to extend through Sema3A-negative regions. These results suggest that a Sema3A-dependent guidance system plays a key role in neuronal circuit formation in amniote limbs. We also found that Sema3A partially overlapped with the distribution of cartilage precursor cells. Based on these results, we propose a model in which axon guidance and skeletogenesis are linked by Sema3A; such mechanisms may underlie functional neuron rearrangement during limb diversification.
Assuntos
Extremidades/embriologia , Extremidades/inervação , Regulação da Expressão Gênica no Desenvolvimento , Semaforina-3A/genética , Animais , Embrião de Galinha , Lagartos , Camundongos , Neurogênese/genética , Neurogênese/fisiologia , Semaforina-3A/metabolismo , TartarugasRESUMO
In vertebrates, paired appendages (limbs and fins) are derived from the somatic mesoderm subsequent to the separation of the lateral plate mesoderm into somatic and splanchnic layers. This is less clear for teleosts, however, because the developmental processes of separation into two layers and of extension over the yolk have rarely been studied. During teleost evolution, the position of pelvic fins has generally shifted rostrally (Rosen; Nelson, 1982, 1994), although at the early embryonic stage the presumptive pelvic fin cells are initially located near the future anus region - the anterior border of hoxc10a expression in the spinal cord - regardless of their final destination. Our previous studies in zebrafish (abdominal pelvic fins) and Nile tilapia (thoracic pelvic fins) showed that the presumptive pelvic fin cells shift their position with respect to the body trunk after its protrusion from the yolk surface. Furthermore, in Nile tilapia, presumptive pelvic fin cells migrate anteriorly on the yolk surface. Here, we examined the embryonic development of the lateral plate mesoderm at histological levels in the pufferfish Takifugu niphobles, which belongs to the highly derived teleost order Tetraodontiformes, and lacks pelvic fins. Our results show that, in T. niphobles, the lateral plate mesoderm bulges out as two separate layers of cells alongside the body trunk prior to its further extension to cover the yolk sphere. Once the lateral plate mesoderm extends laterally, it rapidly covers the surface of the yolk. Furthermore, cells located near the anterior border of hoxc10a expression in the spinal cord reach the anterior-most region of the yolk surface. In light of our previous and current studies, we propose that anterior migration of presumptive pelvic fin cells might be required for them to reach the thoracic or more anterior positions as is seen in other highly derived teleost groups.
Assuntos
Nadadeiras de Animais/embriologia , Mesoderma/embriologia , Tetraodontiformes/embriologia , Animais , Evolução Biológica , Desenvolvimento Embrionário/fisiologia , Dados de Sequência MolecularRESUMO
The position of the pelvic fins among teleost fishes has tended to shift rostrally during evolution. This positional shift seems to have led to the diversification of feeding behavior and allowed adaptation to new environments. To understand the developmental basis of this shift in pelvic fin position among teleosts, we investigated the embryonic development of the lateral plate mesoderm, which gives rise to the pelvic fins, at histological levels in the medaka Oryzias latipes (abdominal pelvic fins) and Nile tilapia Oreochromis niloticus (thoracic pelvic fins). Our histological analyses revealed that the lateral plate mesodermal cells expand not only ventrally but also rostrally to cover the yolk during embryogenesis of both medaka and Nile tilapia. In medaka, we also found that the lateral plate mesoderm completely covered the yolk prior to the initiation of the pelvic fin buds, whereas in Nile tilapia the pelvic fin buds appeared in the body wall from the lateral plate mesoderm at the thoracic level when the lateral plate mesodermal cells only covered one-third of the yolk. We discuss the relevance of such differences in the rate of the lateral plate mesoderm expansion on the yolk surface and the position of the pelvic fins.
Assuntos
Nadadeiras de Animais/embriologia , Ciclídeos/embriologia , Mesoderma/embriologia , Oryzias/embriologia , Animais , Evolução BiológicaRESUMO
The role of hybridization in morphological diversification is a fundamental topic in evolutionary biology. However, despite the accumulated knowledge on adult hybrid variation, how hybridization affects ontogenetic allometry is less well understood. Here, we investigated the effects of hybridization on postnatal ontogenetic allometry in the skulls of a putative hybrid population of introduced Taiwanese macaques (Macaca cyclopis) and native Japanese macaques (Macaca fuscata). Genomic analyses indicated that the population consisted of individuals with varying degrees of admixture, formed by male migration from Japanese to Taiwanese macaques. For overall skull shape, ontogenetic trajectories were shifted by hybridization in a nearly additive manner, with moderate transgressive variation observed throughout development. In contrast, for the maxillary sinus (hollow space in the face), hybrids grew as fast as Taiwanese macaques, diverging from Japanese macaques, which showed slow growth. Consequently, adult hybrids showed a mosaic pattern, that is, the maxillary sinus is as large as that of Taiwanese macaques, while the overall skull shape is intermediate. Our findings suggest that the transgressive variation can be caused by prenatal shape modification and nonadditive inheritance on regional growth rates, highlighting the complex genetic and ontogenetic bases underlying hybridization-induced morphological diversification.
Assuntos
Macaca fuscata , Crânio , Animais , Masculino , Crânio/anatomia & histologia , Macaca/anatomia & histologia , Macaca/genética , Evolução BiológicaRESUMO
Specification of limb field and initiation of limb development involve multiple steps, each of which is tightly regulated both spatially and temporally. Recent developmental analyses on various vertebrates have provided insights into the molecular mechanisms that specify limb field and have revealed several genetic interactions of signals involved in limb initiation processes. Furthermore, new approaches to the study of the developmental mechanisms of the lateral plate mesoderm of amphioxus and lamprey embryos have given us clues to understand the evolutionary scenarios that led to the acquisition of paired appendages during evolution. This review highlights such recent findings and discusses the mechanisms of limb field specification and limb bud initiation during development and evolution.
Assuntos
Evolução Biológica , Extremidades/embriologia , Regulação da Expressão Gênica no Desenvolvimento , Animais , Padronização Corporal , Embrião de Galinha , Extremidades/fisiologia , Fatores de Crescimento de Fibroblastos/genética , Fatores de Crescimento de Fibroblastos/metabolismo , Botões de Extremidades/embriologia , Botões de Extremidades/metabolismo , Mesoderma/embriologia , Mesoderma/metabolismo , Fatores de Transcrição Box Pareados/genética , Fatores de Transcrição Box Pareados/metabolismo , Proteínas com Domínio T/genética , Proteínas com Domínio T/metabolismo , Asas de Animais/embriologia , Asas de Animais/metabolismo , Via de Sinalização WntRESUMO
Amphibians shape their limbs by differential outgrowth of digits and interdigital regions. In contrast, amniotes employ cell death, an additional developmental system, to determine the final shape of limbs. Previous work has shown that high oxygen availability is correlated with the induction of cell death in developing limbs. Given the diversity of life histories of amphibians, it is conceivable that some amphibians are exposed to a high-oxygen environment during the tadpole phase and exhibit cell death in their limbs. Here, we examined whether air-breathing behavior underlies the cell death in limbs of aquatic tadpoles of the frog species Rana pirica. Our experimental approach revealed that R. pirica tadpoles exhibit cell death in their limbs that is likely to be induced by oxidative stress associated with their frequent air-breathing behavior.
RESUMO
Anterior and posterior paired appendages of vertebrates are notable examples of heterochrony in the relative timing of their development. In teleosts, posterior paired appendages (pelvic fin buds) emerge much later than their anterior paired appendages (pectoral fin buds). Pelvic fin buds of zebrafish (Danio rerio) appear at 3 weeks post-fertilization (wpf) during the larva-to-juvenile transition (metamorphosis), whereas pectoral fin buds arise from the lateral plate mesoderm on the yolk surface at the embryonic stage. Here we explored the mechanism by which presumptive pelvic fin cells maintain their fate, which is determined at the embryonic stage, until the onset of metamorphosis. Expression analysis revealed that transcripts of pitx1, one of the key factors for the development of posterior paired appendages, became briefly detectable in the posterior lateral plate mesoderm at early embryonic stages. Further analysis indicated that the pelvic fin-specific pitx1 enhancer was in the poised state at the larval stage and is activated at the juvenile stage. We discuss the implications of these findings for the heterochronic development of pelvic fin buds.
RESUMO
The evolution and diversification of vertebrate behaviors associated with locomotion depend highly on the functional transformation of paired appendages. Although the evolution of fins into limbs has long been a focus of interest to scientists, the evolution of neural control during this transition has not received much attention. Recent studies have provided significant progress in the understanding of the genetic and developmental bases of the evolution of fin/limb motor circuitry in vertebrates. Here we compare the organization of the motor neurons in the spinal cord of various vertebrates. We also discuss recent advances in our understanding of these events and how they can provide a mechanistic explanation for the evolution of fin/limb motor circuitry in vertebrates.
Assuntos
Nadadeiras de Animais/inervação , Evolução Biológica , Extremidades/inervação , Neurônios Motores , Animais , Medula Espinal , VertebradosRESUMO
Possession of paired appendages is regarded as a novelty that defines crown gnathostomes and allows sophisticated behavioral and locomotive patterns. During embryonic development, initiation of limb buds in the lateral plate mesoderm involves several steps. First, the lateral plate mesoderm is regionalized into the cardiac mesoderm (CM) and the posterior lateral plate mesoderm (PLPM). Second, in the PLPM, Hox genes are expressed in a collinear manner to establish positional values along the anterior-posterior axis. The developing PLPM splits into somatic and splanchnic layers. In the presumptive limb field of the somatic layer, expression of limb initiation genes appears. To gain insight into the evolutionary sequence leading to the emergence of paired appendages in ancestral vertebrates, we examined the embryonic development of the ventral mesoderm in the cephalochordate amphioxus Branchiostoma floridae and of the lateral plate mesoderm in the agnathan lamprey Lethenteron japonicum, and studied the expression patterns of cognates of genes known to be expressed in these mesodermal layers during amniote development. We observed that, although the amphioxus ventral mesoderm posterior to the pharynx was not regionalized into CM and posterior ventral mesoderm, the lateral plate mesoderm of lampreys was regionalized into CM and PLPM, as in gnathostomes. We also found nested expression of two Hox genes (LjHox5i and LjHox6w) in the PLPM of lamprey embryos. However, histological examination showed that the PLPM of lampreys was not separated into somatic and splanchnic layers. These findings provide insight into the sequential evolutionary changes that occurred in the ancestral lateral plate mesoderm leading to the emergence of paired appendages.
Assuntos
Evolução Biológica , Cordados não Vertebrados/embriologia , Lampreias/embriologia , Mesoderma/embriologia , Animais , Sequência de Bases , Primers do DNA , Genes Homeobox , Hibridização In Situ , Reação em Cadeia da Polimerase Via Transcriptase ReversaRESUMO
The origin of paired fins has long been a focus of both paleontologists and developmental biologists. Fossil records indicate that the first pair of fin-like structures emerged in the body wall of early vertebrates. However, extant agnathan lampreys and hagfishes lack paired fins, and thus it has been difficult to determine the developmental processes underlying the ancestral acquisition of paired fins in vertebrates. Fortunately, recent advances in our knowledge of the developmental mechanisms of the lateral plate mesoderm among different taxa have provided clues for understanding the evolutionary origin of vertebrate paired appendages.
Assuntos
Nadadeiras de Animais/anatomia & histologia , Evolução Biológica , Mesoderma/anatomia & histologia , Nadadeiras de Animais/embriologia , Animais , Fósseis , Genes Controladores do Desenvolvimento , Feiticeiras (Peixe)/embriologia , Feiticeiras (Peixe)/genética , Lampreias/embriologia , Lampreias/genética , Mesoderma/embriologiaRESUMO
The pelvic fin position among teleost fishes has shifted rostrally during evolution, resulting in diversification of both behavior and habitat. We explored the developmental basis for the rostral shift in pelvic fin position in teleost fishes using zebrafish (abdominal pelvic fins) and Nile tilapia (thoracic pelvic fins). Cell fate mapping experiments revealed that changes in the distribution of lateral plate mesodermal cells accompany the trunk-tail protrusion. Presumptive pelvic fin cells are originally located at the body wall adjacent to the anterior limit of hoxc10a expression in the spinal cord, and their position shifts rostrally as the trunk grows. We then showed that the differences in pelvic fin position between zebrafish and Nile tilapia were not due to changes in expression or function of gdf11. We also found that hox-independent motoneurons located above the pelvic fins innervate into the pelvic musculature. Our results suggest that there is a common mechanism among teleosts and tetrapods that controls paired appendage positioning via gdf11, but in teleost fishes the position of prospective pelvic fin cells on the yolk surface shifts as the trunk grows. In addition, teleost motoneurons, which lack lateral motor columns, innervate the pelvic fins in a manner independent of the rostral-caudal patterns of hox expression in the spinal cord.