The origin of paired appendages was a major evolutionary innovation for vertebrates, marking the first step towards fin- (and later limb-) driven locomotion. The earliest vertebrate fossils lack paired fins but have well-developed median fins, suggesting that the mechanisms of fin development were assembled first in the midline. Here we show that shark median fin development involves the same genetic programs that operate in paired appendages. Using molecular markers for different cell types, we show that median fins arise predominantly from somitic (paraxial) mesoderm, whereas paired appendages develop from lateral plate mesoderm. Expression of Hoxd and Tbx18 genes, which specify paired limb positions, also delineates the positions of median fins. Proximodistal development of median fins occurs beneath an apical ectodermal ridge, the structure that controls outgrowth of paired appendages. Each median fin bud then acquires an anteroposteriorly-nested pattern of Hoxd expression similar to that which establishes skeletal polarity in limbs. Thus, despite their different embryonic origins, paired and median fins utilize a common suite of developmental mechanisms. We extended our analysis to lampreys, which diverged from the lineage leading to gnathostomes before the origin of paired appendages, and show that their median fins also develop from somites and express orthologous Hox and Tbx genes. Together these results suggest that the molecular mechanisms for fin development originated in somitic mesoderm of early vertebrates, and that the origin of paired appendages was associated with re-deployment of these mechanisms to lateral plate mesoderm.
The evolutionary transition of fins to limbs involved development of a new suite of distal skeletal structures, the digits. During tetrapod limb development, genes at the 5′ end of the HoxD cluster are expressed in two spatiotemporally distinct phases. In the first phase, Hoxd9-13 are activated sequentially and form nested domains along the anteroposterior axis of the limb. This initial phase patterns the limb from its proximal limit to the middle of the forearm. Later in development, a second wave of transcription results in 5′ HoxD gene expression along the distal end of the limb bud, which regulates formation of digits. Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods. Here we test this hypothesis by investigating Hoxd gene expression during paired fin development in the shark Scyliorhinus canicula, a member of the most basal lineage of jawed vertebrates. We report that at early stages, 5′Hoxd genes are expressed in anteroposteriorly nested patterns, consistent with the initial wave of Hoxd transcription in teleost and tetrapod paired appendages. Unexpectedly, a second phase of expression occurs at later stages of shark fin development, in which Hoxd12 and Hoxd13 are re-expressed along the distal margin of the fin buds. This second phase is similar to that observed in tetrapod limbs. The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans. We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.
Fossil data suggest that limbs evolved from fish fins by sequential elaboration of their distal endoskeleton, giving rise to the autopod close to the tetrapod origin. This elaboration may have occurred by a simultaneous reduction of the distal ectodermal fold of fish fins. Modulation of 5'Hoxd gene transcription, through tetrapod-specific digit enhancers, has been suggested as a possible evolutionary mechanism involved in these morphological transformations. Here, we overexpress hoxd13a in zebrafish to investigate the impact of increasing 5'Hoxd expression during fin development. This overexpression causes increased proliferation, distal expansion of chondrogenic tissue and finfold reduction. In addition, we also show that the tetrapod-specific 5'Hoxd enhancer CsC promotes similar expression in zebrafish fins and mouse limbs. Our results support the idea that modulation of 5'Hoxd gene expression, by acquisition of novel enhancer elements, offered the substrate for the evolution of fins and the origin of tetrapod limbs.
The roles of bioelectric signaling in developmental patterning remain largely unknown, although recent work has implicated bioelectric signals in cellular processes such as proliferation and migration. Here, we report a mutation in the inwardly rectifying potassium channel (kir) gene, kcnj13/kir7.1, that causes elongation of the fins in the zebrafish insertional mutant Dhi2059. A viral DNA insertion into the noncoding region of kcnj13 results in transient activation and ectopic expression of kcnj13 in the dermomyotome, from which the fin ray progenitors originate. We made an allele-specific loss-of-function kcnj13 CRISPR mutant and showed that it could reverse the long-finned phenotype, but only when located on the same chromosome as the Dhi2059 viral insertion. Also, we showed that ectopic expression of kcnj13 in the dermomyotome of transgenic zebrafish produces phenocopies of the Dhi2059 mutant in a gene dosage-sensitive manner. Finally, to determine whether this developmental function is specific to kcnj13, we ectopically expressed three additional potassium channel genes, kcnj1b, kcnj10a, and kcnk9. We found that all induce the long-finned phenotype, indicating that this function is conserved among potassium channel genes. Taken together, our results suggest that dermomyotome bioelectricity is a new fin patterning mechanism, and we propose a two-stage bioelectricity model for zebrafish fin patterning. This ion-channel-regulated bioelectric developmental patterning mechanism may provide us new insight into vertebrate morphological evolution and human congenital malformations.
Vertebrates have evolved electrosensory receptors that detect electrical stimuli on the surface of the skin and transmit them somatotopically to the brain. In chondrichthyans, the electrosensory system is composed of a cephalic network of ampullary organs, known as the ampullae of Lorenzini, that can detect extremely weak electric fields during hunting and navigation. Each ampullary organ consists of a gel-filled epidermal pit containing sensory hair cells, and synaptic connections with primary afferent neurons at the base of the pit that facilitate detection of voltage gradients over large regions of the body. The developmental origin of electroreceptors and the mechanisms that determine their spatial arrangement in the vertebrate head are not well understood. We have analyzed electroreceptor development in the lesser spotted catshark (Scyliorhinus canicula) and show that Sox8 and HNK1, two markers of the neural crest lineage, selectively mark sensory cells in ampullary organs. This represents the first evidence that the neural crest gives rise to electrosensory cells. We also show that pathfinding by cephalic mechanosensory and electrosensory axons follows the expression pattern of EphA4, a well-known guidance cue for axons and neural crest cells in osteichthyans. Expression of EphrinB2, which encodes a ligand for EphA4, marks the positions at which ampullary placodes are initiated in the epidermis, and EphA4 is expressed in surrounding mesenchyme. These results suggest that Eph-Ephrin signaling may establish an early molecular map for neural crest migration, axon guidance and placodal morphogenesis during development of the shark electrosensory system.
BackgroundThe origin of jawed vertebrates was marked by profound reconfigurations of the skeleton and muscles of the head and by the acquisition of two sets of paired appendages. Extant cartilaginous fish retained numerous plesiomorphic characters of jawed vertebrates, which include several aspects of their musculature. Therefore, myogenic studies on sharks are essential in yielding clues on the developmental processes involved in the origin of the muscular anatomy.ResultsHere we provide a detailed description of the development of specific muscular units integrating the cephalic and appendicular musculature of the shark model, Scyliorhinus canicula. In addition, we analyze the muscle development across gnathostomes by comparing the developmental onset of muscle groups in distinct taxa. Our data reveal that appendicular myogenesis occurs earlier in the pectoral than in the pelvic appendages. Additionally, the pectoral musculature includes muscles that have their primordial developmental origin in the head. This culminates in a tight muscular connection between the pectoral girdle and the cranium, which founds no parallel in the pelvic fins. Moreover, we identified a lateral to ventral pattern of formation of the cephalic muscles, that has been equally documented in osteichthyans but, in contrast with these gnathostomes, the hyoid muscles develop earlier than mandibular muscle in S. canicula.ConclusionOur analyses reveal considerable differences in the formation of the pectoral and pelvic musculatures in S. canicula, reinforcing the idea that head tissues have contributed to the formation of the pectoral appendages in the common ancestor of extant gnathostomes. In addition, temporal differences in the formation of some cranial muscles between chondrichthyans and osteichthyans might support the hypothesis that the similarity between the musculature of the mandibular arch and of the other pharyngeal arches represents a derived feature of jawed vertebrates.
The locomotory appendages of vertebrates have undergone significant changes during evolution, which likely promoted a wide range of adaptive strategies. These appendages first evolved as unpaired finfolds in the dorsal midline of early chordates, more than 500 million years ago. Later on, during vertebrates' radiation, two sets of locomotory appendages emerged, developing from both sides of the latero-ventral body wall. The morphology of these paired fins in fishes at different phylogenetic positions suggests an evolutionary tendency for increasing elaboration of the endoskeleton and concomitant reduction of the distal dermoskeleton. This evolutionary process culminated with the origin of limbs in the lineages leading to tetrapods. The developmental programs responsible for the evolution of vertebrate appendages have been a major topic for evolutionary developmental biology recently. Gene expression comparisons performed in chordates explored how these mechanisms were transferred from a midline to latero-ventral position. On another front, gene function assays have begun to test classical hypotheses concerning the transition from fish fins to tetrapod limbs. In this review, we highlight these recent findings on the evolution of vertebrate fin development. First, we discuss new perspectives on the transition from midline to paired appendages focus on (i) origin and molecular regionalization of the lateral plate mesoderm and (ii) novel ectodermic competency zones for fin induction. Next, we review recent work exploring how tetrapod limbs evolved from fish fins, considering (i) molecular and structural changes in the distal ectoderm of fins and (ii) modulation of 5'HoxD transcription during fin endoskeleton development.
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