Evidence that mechanisms of fin development evolved in the midline of early vertebrates

Department of Zoology, University of Florida, PO Box 118525, Gainesville, Florida 32611, USA.
Nature (Impact Factor: 41.46). 09/2006; 442(7106):1033-7. DOI: 10.1038/nature04984
Source: PubMed

ABSTRACT 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.

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Available from: Renata Freitas, Jul 25, 2014
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    • "Goodrich (1930)] and corresponding to the vertebral arches of gnathostomes. These presumably originate from sclerotome cells, as indicated by recent studies showing the expression patterns of genes proposed as sclerotome markers (see Table 1), such as FoxC2, Tbx18 and the orthologue of the ancestor of scleraxis (Freitas et al., 2006), and "
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    ABSTRACT: The segmented vertebral column comprises a repeat series of vertebrae, each consisting of two key components: the vertebral body (or centrum) and the vertebral arches. Despite being a defining feature of the vertebrates, much remains to be understood about vertebral development and evolution. Particular controversy surrounds whether vertebral component structures are homologous across vertebrates, how somite and vertebral patterning are connected, and the developmental origin of vertebral bone-mineralizing cells. Here, we assemble evidence fromichthyologists, palaeontologists and developmental biologists to consider these issues. Vertebral arch elementswere present in early stemvertebrates, whereas centra arose later.We argue that centra are homologous among jawed vertebrates, and review evidence in teleosts that the notochord plays an instructive role in segmental patterning, alongside the somites, and contributes to mineralization. By clarifying the evolutionary relationship between centra and arches, and their varying modes of skeletal mineralization, we can better appreciate the detailed mechanisms that regulate and diversify vertebral patterning.
    Development 05/2015; 142(10):1733-1744. DOI:10.1242/dev.118950 · 6.46 Impact Factor
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    • "Fgf8 and Dlx proteins are also detected in the MFF apical tissue of sharks suggesting that ancestral molecular mechanisms implicated in unpaired fin development might have been established during early vertebrate evolution [22]. It is now well accepted that paired appendages evolved after unpaired appendages [22], [64], [65]. Despite their different embryonic origins [66], [67], it has been suggested that paired and unpaired fins use a common suite of developmental mechanisms, a hypothesis mainly based on expression analyses [17], [22], [68], [69]. "
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    ABSTRACT: The Dlx5 and Dlx6 genes encode homeodomain transcription factors essential for the proper development of limbs in mammalian species. However, the role of their teleost counterparts in fin development has received little attention. Here, we show that dlx5a is an early marker of apical ectodermal cells of the pectoral fin buds and of the median fin fold, but also of cleithrum precursor cells during pectoral girdle development. We propose that early median fin fold establishment results from the medial convergence of dlx5a-expressing cells at the lateral edges of the neural keel. Expression analysis also shows involvement of dlx5a during appendage skeletogenesis. Using morpholino-mediated knock down, we demonstrate that disrupted dlx5a/6a function results in pectoral fin agenesis associated with misexpression of bmp4, fgf8a, and1 and msx genes. In contrast, the median fin fold presents defects in mesenchymal cell migration and actinotrichia formation, whereas the initial specification seems to occur normally. Our results demonstrate that the dlx5a/6a genes are essential for the induction of pectoral fin outgrowth, but are not required during median fin fold specification. The dlx5a/6a knock down also causes a failure of cleithrum formation associated with a drastic loss of runx2b and col10a1 expression. The data indicate distinct requirements for dlx5a/6a during median and pectoral fin development suggesting that initiation of unpaired and paired fin formation are not directed through the same molecular mechanisms. Our results refocus arguments on the mechanistic basis of paired appendage genesis during vertebrate evolution.
    PLoS ONE 05/2014; 9(5):e98505. DOI:10.1371/journal.pone.0098505 · 3.23 Impact Factor
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    • "As such, it provides a unique window into early vertebrate history, enabling inference of the ancestral states and evolutionary origins of vertebrate characters. For example, investigations into lamprey genetics and embryogenesis have shed light on the evolution of the jaw [2], [3], paired fins [4], neural crest [5], [6], pharynx [7], immune system [8], sympathetic nervous system [9], forebrain [10], [11], and hindbrain [12]. Whilst the restricted summer breeding season presents some practical difficulties for studying lamprey embryology, the availability of copious embryos during this period has enabled the establishment of a suite of developmental biology techniques for lamprey, including in-situ hybridisation, morpholino-mediated gene knockdown and cell labelling [5], [7], [13] [14]. "
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    ABSTRACT: The sea lamprey is an important model organism for investigating the evolutionary origins of vertebrates. As more vertebrate genome sequences are obtained, evolutionary developmental biologists are becoming increasingly able to identify putative gene regulatory elements across the breadth of the vertebrate taxa. The identification of these regions makes it possible to address how changes at the genomic level have led to changes in developmental gene regulatory networks and ultimately to the evolution of morphological diversity. Comparative genomics approaches using sea lamprey have already predicted a number of such regulatory elements in the lamprey genome. Functional characterisation of these sequences and other similar elements requires efficient reporter assays in lamprey. In this report, we describe the development of a transient transgenesis method for lamprey embryos. Focusing on conserved non-coding elements (CNEs), we use this method to investigate their functional conservation across the vertebrate subphylum. We find instances of both functional conservation and lineage-specific functional evolution of CNEs across vertebrates, emphasising the utility of functionally testing homologous CNEs in their host species.
    PLoS ONE 01/2014; 9(1):e85492. DOI:10.1371/journal.pone.0085492 · 3.23 Impact Factor
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