All of the major pterygote groups appear by the Carboniferous — Myr and are assumed to have arisen earlier. Fundamentally, discussion on the origin of wings has focused on whether they are novelties or whether they are modified versions of ancestral structures. If wings were derived from existing structures, what were their anatomical origins and initial functions?
According to this model, proximal limb elements were modified to flap-like structures and adapted to spiracular or movable gill covers to facilitate respiration. These sack-like pro-wings were found on all thoracic and abdominal segments and became stronger as ancestral pterygote nymphs similar to Recent mayfly larvae used them presumably for propulsion. As insect lifestyles became more amphibiotic, some insects might have used a rudimentary proto-wing for surface skimming, as seen in extant stoneflies Finally, wings acquired the mechanical strength and flexibility with corrugation and veins and the supporting musculature to support active flight.
Recent studies of the developmental regulatory mechanisms controlling wing formation and number in Drosophila suggest a close ontogenetic and evolutionary relationship between legs and wings. For example, in Drosophila 68 and other Diptera, the wing arises in close association with the leg. Cells that give rise to the wing field in Drosophila actually migrate out of the developing ventral limb field There are important regulatory differences that distinguish the development of the sheet-like wing from the tubular structure of the leg.
One key difference is that adult and developing wings are divided into discrete dorsal and ventral compartments whereas legs are not. In Drosophila , the definition of dorsal versus ventral cell fates is orchestrated by the apterous gene which is expressed only in dorsal cells and is necessary for wing but not leg formation Clearly, apterous , which regulates several crucial downstream signalling components, and is involved in a conserved dorsal pattern of expression in insect wings 70 , was coopted into a distinct role in dorsoventral patterning at some stage of wing evolution.
Remarkably, this is exactly what has been found in a recent study The dorsal branch of a branchiopod crustacean respiratory epipodite specifically expresses the apterous gene and one other developmental marker of the insect wing field Fig. This suggests that Recent wings evolved from the respiratory lobe of an ancestral polyramous limb, probably first appearing in the immature aquatic stages as gill-like structures, such as those found on all trunk segments of extinct Paleodictyoptera or extant mayfly larvae Fig.
Wings subsequently emerged as adult appendages and acquired greater strength and flexibility for sustained flight Fig. Interestingly, if the respiratory epipodite origin of insect wings is correct, then wings may have an even deeper origin, not just in the aquatic ancestor of pterygotes, but in lobopodans. The origin of the biramous limb has been postulated to involve the fusion of the gill-like structure of lateral lobes such as those in Opabinia with the ventral lobopod 43 , 45 , 46 , 47 Fig.
If this is true, then the wing may indeed be derived from lateral lobes, not of a terrestrial insect as once thought, but of a much more distant lobopodan ancestor. It is clear from the fossil record that chordates and arthropods diverged at least by the Cambrian. The appendages of these two groups are not homologous because phylogenetically intermediate taxa particularly basal chordates do not possess comparable structures. The most surprising discovery of recent molecular studies, however, is that much of the genetic machinery that patterns the appendages of arthropods, vertebrates and other phyla is similar.
These findings suggest that the common ancestor of many animal phyla could have had body-wall outgrowths that were organized by elements of the regulatory systems found in extant appendages.
We now describe these similarities and use them to consider the origin of animal limbs. In Drosophila , the anteroposterior AP axis of the leg or wing imaginal disc the larval precursor to the adult appendages is divided into two compartments reviewed in ref. The posterior half of the disc expresses the gene hedgehog 72 , 73 , which encodes the key signal that initiates AP patterning Fig. In response to hedgehog , a thin layer of cells running along the border of the anterior and posterior compartments is induced to produce another secreted protein encoded by the gene decapentaplegic dpp Misexpression of either hedgehog or dpp in the anterior of the disc results in AP mirror-image duplications of limb structures Homologous signals are deployed in similar locations in the limb primordia of arthropods a , Drosophila and vertebrates b , chick.
Equivalent orientations dorsal up, anterior left of a chick left wing bud and a Drosophila left wing imaginal disc are shown. Sonic hedgehog red in the chick, and its homologue hedgehog red and purple, where coexpressed with apterous in the fly are produced in a posterior domain.
These factors induce the expression of secondary patterning signals in the appendages: overlapping expression of Bmp-2 green in the chick and adjacent expression of dpp green , the Bmp-2 -homologue, in the fly. Dorsal cell fates are specified in both systems by LIM homeodomain transcription factors expressed throughout the dorsal half of the appendage primordia: Lmx -1 blue in the chick, and apterous blue and purple, where coexpressed with hedgehog in the fly.
The outgrowth of both appendages is driven by a specialized group of cells the AER in the chick and the wing margin in the fly running along the anteroposterior axis at the junction of the dorsal and ventral compartments yellow. These key groups of cells are specified in both the chick and the fly by the border between dorsal cells expressing the gene fringe and ventral cells not expressing fringe.
For simplicity in viewing, conserved genes in signal transduction such as the hedgehog receptor, patched and other parallels between the two systems such as the expression of Wnt genes are not shown. Distal-less homologues Dll in Drosophila and Dlx in the chick are drawn in orange. Distal-less orthologues are expressed in a wide variety of animal appendages, including the lobopods of onycophorans, the tube feet of echinoderm, and the wings of birds and flies orange. The limbs of these taxa are not homologous as appendages because phylogenetically intermediate groups do not possess comparable structures.
This suggests at least two phylogenetic possibilities: either similar genetic circuits were convergently recruited to make the limbs of different taxa, or these signalling and regulatory systems are ancient and patterned a different structure presumably another type of outgrowth in the common ancestor of protostomes and deuterostomes The AP axis of the vertebrate limb is set up in a very similar manner Fig. A key organizing signal is Sonic hedgehog Shh , one of the three direct homologues of the Drosophila gene hedgehog 80 , 81 , 82 , Like hedgehog , Shh is localized posteriorly in the limb bud.
Misexpression of Shh anteriorly causes AP mirror-image duplications analogous to those caused by hedgehog misexpression in the fly imaginal disc 74 , In addition, Bmp-2 , one of the two vertebrate homologues of the arthropod dpp signalling protein, is expressed in the limb bud in response to Shh Unlike Drosophila dpp , Bmp -2 does not have the ability to cause full limb duplications. However, it clearly functions as a secondary signal in the Shh pathway, polarizing the overlying ectoderm Signals organizing proximodistal PD outgrowth in vertebrate and insect appendages also operate similarly.
The dorsal compartment of the wing is characterized by the expression of the transcription factor apterous. The interface between cells expressing and cells not expressing fringe becomes the wing edge or margin A key downstream effector of fringe activity is encoded by Serrate In response to fringe , Serrate is induced, leading to the activation of several downstream effector genes 87 , 88 , 89 , 90 and the production of a signal at the margin which organizes the growth of the wing blade 87 , 88 , Unexpectedly, outgrowth of vertebrate limbs appears to be established by a very similar genetic cascade.
Outgrowth of the limb bud is driven by signals from a specialized ectodermal structure, the apical ectodermal ridge 91 AER , which, like the wing margin, runs along the DV border of the limb. Remarkably, a vertebrate homologue of fringe , called Radical-fringe , is expressed in the dorsal half of the limb ectoderm prior to formation of the AER At the border between cells expressing Radical-fringe and cells not expressing Radical-fringe , a homologue of Serrate , Ser-2 , is induced and the AER forms.
A Radical-fringe boundary is required to form the AER and ectopic radical fringe can induce an additional AER on the ventral surface There are also parallels between the regulation of the DV axis in vertebrate and arthropod appendages Fig. Genes specifying DV polarity in both groups have been identified. In Drosophila , the early ventral expression of the gene wingless , a member of the Wnt family of secreted factors, is necessary for the proper DV patterning of the wing 94 , Subsequently, the expression of the transcription factor apterous defines the dorsal compartment and specifies dorsal cell fates In the vertebrate limb, the early expression of a different Wnt family member is also required for DV patterning.
Wnt7a is specifically expressed throughout the dorsal ectoderm and is necessary and sufficient for many aspects of dorsal patterning 96 , 97 , Wnt7a acts by inducing mesodermal expression of Lmx-1 97 , Like apterous , Lmx-1 is a related member of the LIM-homeodomain family of transcription factors.
As with apterous Drosophila , Lmx-1 vertebrates expression defines a dorsal compartment, being expressed early throughout the dorsal half of the limb bud, and it is sufficient to convey dorsal cell fate 97 , The simplest phylogenetic implication to draw from these comparisons is that individual genes that are expressed in the three orthogonal axes are more ancient than either insect or vertebrate limbs Fig 6.
Indeed, several of the regulatory systems seen in arthropod and vertebrate limbs are also involved in the development of other organs in a variety of taxa. The phylogenetic distribution of regulatory circuits and morphological structures presents two major interpretations: either similar genetic circuits were convergently recruited to make the limbs of different taxa or a set of these signalling and regulatory systems are ancient and patterned a structure in the common ancestor of protostomes and deuterostomes These genes would not be involved in appendage development in the common ancestor of vertebrates and arthropods; each gene or circuit was involved in other developmental events.
This notion would require the parallel cooption of members of similar gene families, acting along different developmental axes to pattern an outgrowth of the body wall in at least two taxa.
The evolution of limbs in each group would, then, have involved the convergent recruitment of numerous genes to define similar developmental axes. If confirmed, this hypothesis would provide a stunning case of convergent evolution. The second model is that some of these genes or circuits were components of an ancestral genetic regulatory system that was used to pattern a structure in the common ancestor of vertebrates and arthropods.
This ancestral structure need not have been homologous to arthropod or vertebrate limbs; the regulatory system could have originally patterned any one of a number of outgrowths of the body wall in a primitive bilaterian for example. The genes themselves were initially involved in other developmental events; the key step in animal limb evolution was the establishment of an integrated genetic system to promote and pattern the development of certain outgrowths.
Once established, this system provided the genetic and developmental foundation for the evolution of structures as diverse as wings, fins, antennae and lobopodia. The evaluation of these two alternative models requires consideration of several factors that could affect the identity and deployment of appendate-patterning genes. First, given the independent histories spanning more than Myr of the lineages being compared, one should expect regulatory differences among patterning systems.
Even the insect wing and leg, which are both probably derived from an ancestral polyramous appendage, have acquired different patterning mechanisms. Because individual regulatory components appear to have been gained, lost and modified during insect wing and leg evolution there is no apriori reason to expect that either structure would be more genetically similar to vertebrate limbs.
Second, one member of a gene family may substitute for another during normal development. Indeed, some of the genes that are deployed similarly in arthropods and vertebrates are not strictly orthologous. Such substitution could be the product of either convergent evolution or descent with modification by substitution among redundant genes.
Third, it could be argued that the presumed inversion of the DV body axis during deuterostome evolution would imply a corresponding inversion of appendage DV axis patterning signals, an expectation that is not met by the observed expression of apterous- and fringe -related genes in vertebrate limb buds.
A parallel in reversal of the DV axes of the body and the limbs would be expected if vertebrate and insect limbs were structurally homologous to a common ancestral appendage which predated the reversal. However, we know that the modern vertebrate limb evolved after the DV inversion of the body axis. Thus, a DV inversion in the patterning of the limbs would not necessarily be predicted, whether the axis patterning genes were independently coopted for appendage formation according to the first model, or whether they were coopted as a unit, but regulated independently of the body axis, according to the second model.
One can argue many ways from the comparison of only two taxa: the alternative phylogenetic hyopotheses need to be tested by additional comparative data. Evidence in support of an ancient common mechanism for the formation of outgrowths of the body wall comes from phylogenetic comparison of the expression of the transcription factor Distal-less Dll Fig. Dll is expressed at the distal end of growing insect limbs 55 , 60 , 61 , and is essential for appendage outgrowth Dll orthologues are expressed in the distal portion AER of the embryonic limb buds of vertebrates, the ampullae and siphons of tunicates, the tubefeet of echinoderms, the parapodia of annelids, as well as Onychophoran lobopodia The expression of Dll -related genes could represent convergent utilization of the gene.
However, the fact that out of the hundreds of transcription factors that potentially could have been used, Dll is expressed in the distal portions of appendages in six coelomate phyla makes it more likely that Dll was already involved in regulating body wall outgrowth in a common ancestor of these taxa Fig.
The additional parallels between vertebrate and arthropod limbs suggest that this ancestral outgrowth may have also been patterned along the three orthogonal axes. If a conserved outgrowth patterning system was available for co-option in the evolution of vertebrate limbs, then it must have been used in patterning non-limb outgrowths in basal taxa.
Genetic studies provide an example of at least one secondary outgrowth patterned along these axes that predated the evolution of vertebrate limbs: the branchial arches. As the branchial arches grow out from the cranial region of the chick embryo, they express important components of the limb patterning system in similar developmental regions , Like arthropod and vertebrate limbs, the branchial arches contain localized, posterior expression of a hedgehog gene, in this case Shh , Furthermore, Shh is coexpressed with Bmp posteriorly Yet more similarities lie in the DV and AP axes: fringe -expressing cells are initially confined to the dorsal ectoderm and later are restricted to distal regions of the outgrowth where Distal-less orthologues are also expressed The ectopic deployment and modification of an existing patterning program, such as that of the branchial arches, may have given rise to the predecessors of vertebrate appendages.
Determination of whether two structures are homologous depends on the hierarchical level at which they are compared , , For example, bird wings and bat wings are analogous as wings, having evolved independently for flight in each lineage.
However, at a deeper hierarchical level that includes all tetrapods, they are homologous as forelimbs, being derived from a corresponding appendage of a common ancestor. Similarly, we suggest that whereas vertebrate and insect wings are analogous as appendages, the genetic mechanisms that pattern them may be homologous at a level including most protostomes and deuterostomes.
Furthermore, we propose that the regulatory systems that pattern extant arthropod and vertebrate appendages patterned an ancestral outgrowth and that these circuits were later modified during the evolution of different types of animal appendages. Novelty in evolution: Restructuring the concept. Article Google Scholar. Coates, M.
The origin of vertebrate limbs. Development suppl. Fish fins or tetrapod limbs—a simple twist of fate? Shubin, N. The evolution of paired fins and the origin of tetrapod limbs. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution.
Johnson, R. The long and short of hedgehog signaling. Cell 81 , — Nelson, C. Analysis of Hox gene expression in the chick limb bud. Development , — Tabin, C. Hox genes and serial homology. Nature , — Sordino, P. Hox gene expression in teleost fins and the origin of vertebrate digits.
Kessel, M. Murine developmental control genes. Science , — Mackem, S. Limb-type differences in expression domains of certain chick Hox -4 genes and relationship to pattern modification for flight. Google Scholar. Peterson, R. The murine Hoxc cluster contains five neighboring abdB -related Hox genes that show unique spatially coordinated expression in posterior embryonic subregions. Gibson-Brown, J. Davis, A. Absence of radius and ulna in mice lacking hoxa and hoxd Vorobyeva, E. From fins to limbs.
Hinchliffe, J. Holmgren, N. On the origin of the tetrapod limb. Acta Zoologica 14 , — Contribution on the question of the origin of the tetrapod limb.
Acta Zoologica 20 , 89— Watson, D. On the primitive tetrapod limb. Anzeiger 44 , 24—27 Gregory, W. Studies on the origin and early evolution of paired fins and limbs. Amolecular approach to the evolution of vertebrate paired appendages. Trends Ecol. Ahlberg, P. The origin and early diversification of tetrapods.
Yokouchi, Y. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Gerard, M. Cooperation of regulatory elements involved in the activation of the Hoxd gene. III , — CAS Google Scholar. Beckers, J. Transgenic analysis of a potential Hoxd limb regulatory element present in tetrapods and fish. Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls.
Cell 85 , — Amorphogenetic approach to the origin and basic organization of the tetrapod limb. Why we have only five fingers per hand: hox genes and the evolution of paired limbs. Holder, N. Developmental constraints and the evolution of vertebrate digit patterns. Morse, E. On the tarsus and carpus of birds. Morphological variation in the limbs of Taricha granulosa Caudata: Salamandridae : Evolutionary and phylogenetic implications. Evolution 49 , — Greer, A.
Limb reduction in the Scincid lizard genus Lerista. Variation in the bone complements of the front and rear limbs and the number of postsacral vertebrae. Lande, R. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32 , 73—92 Gauthier, J. Saurischian monophyly and the origin of birds.
MacFadden, B. Fossil Horses Cambridge Univ. Press, Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd Favier, B.
Functional cooperation between the non-paralogous genes Hoxa and Hoxd0 in the developing forelimb and axial skeleton. Disruption of the Hoxd gene induces localized heterochrony leading to mice with neotenic limbs.
Cell 75 , — Axial skeleton homeosis and forelimb malformations in Hoxd mutant mice. Natl Acad. USA 92 , — Capecchi, M. Function of homeobox genes in skeletal development.
Wigglesworth, V. Evolution of insect wings and flight. Budd, G. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29 , 1—14 Hou, X. Cambrian lobopodians—ancestors of extant onychophorans? Simonetta, A. ACambrian gilled lobopod from Greenland. Chen, J. Evidence for monophyly and arthropod affinity of Cambrian giant predators. Carroll, S. Homeotic genes and the evolution of arthropods and chordates Nature , — Struhl, G.
Genes controlling segmental specification in the Drosophila thorax. USA 79 , — Ahomoeotic mutation transforming leg to antenna in Drosophila.
Gibson, G. Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development. Stuart, J. Adeficiency of the homeotic complex of the beetle Tribolium. Nature , 72—47 Averof, M. Hox genes and the diversification of insect—crustacean body plans. Vachon, G. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene. Cell 71 , — Panganiban, G.
The development of crustacean limbs and the evolution of arthropods. Manton, S. Mandibular Mechanisms and the Evolution of Arthropods Vol. Wheeler, W. Arthropod phylogeny: a combined approach.
Cladistics 9 , 1—39 Boore, J. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Cohen, S. Proximal—distal pattern formation in Drosophila : cell autonomous requirement for Distal-less gene activity in limb development.
EMBO J. Distal-less encodes a homeodomain protein required for limb development in Drosophila. The development and evolution of insect limb types. Popadic, A. Origin of the arthropod mandible. Nature , Jeram, A. Land animals in the Silurian: Arachinids and myriapods from Shropshire, England. Snodgrass, R. Kukalova-Peck, J. Origin and evolution of insect wings and their relation to metamorphosis, as documented from the fossil record. Marden, J.
Surface-skimming stoneflies: A possible intermediate stage in insect flight evolution. Cohen, B. Allocation of the thoracic imaginal primordia in the Drosophila embryo. Diaz-Benjumea, F. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Pattern formation and eyespot determination in butterfly wings. Evolutionary origin of insect wings from ancestral gills.
Lee, J. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71 , 33—50 Tabata, T. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. Basler, D. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Posakony, L. Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior—posterior compartment boundary.
Capdevila, J. The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. Sanicola, M. Drawing a stripe in Drosophila imaginal discs: negative regulation of decapentaplegic and patched expression. Genetics , — Nellen, D.
Direct and long-range actions of a Dpp morphogen gradient. Lecuit, T. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing.
Echelard, Y. Sonic hedgehog , a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Krauss, S. Afunctionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos.
Chang, D. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Riddle, R. Sonic hedgehog mediates the polarizing activity of the ZPA. Tickle, C. Genetics and limb development. Irvine, K. Cell 79 , — Spreicher, S. The Serrate locus of Drosophila and its role in morphogenesis or imaginal discs: control of cell proliferation.
Kim, J. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82 , — Couso, J. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Todt, W. Development of the apical ectodermal ridge in the chick wing bud.
Rodriguez-Estaban, C. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Laufer, E. Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation.
Williams, J. Pattern formation in a secondary field: A hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete sub-regions. A wingless -dependent polar coordinate system in Drosophila imaginal discs. Parr, B. Induction of the LIM homeobox gene Lmx-1 by Wnt-7a establishes dorsoventral pattern in the vertebrate limb.
Cell 83 , — Vogel, A. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Raff, R. The Shape of Life Univ. Chicago Press, The origin and evolution of animal appendages.
USA 94 , — Wall, N. Marigo, V. Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb.
Roth, V. Homology and hierarchies: Problems solved and unresolved. Wagner, G. The origin of morphological characters and the biological basis of homology. Evolution 43 , — Bolker, J.
Developmental genetics and traditional homology. BioEssays 18 , — Carroll, R. Vertebrate Paleontology Freeman, San Francisco, Jarvik, E. The Structure and Evolution of the Vertebrates Vol. Chiefly in phrase make a leg. Synonyms side of a right triangle : cathetus. Exemple Insects have six legs. The left leg of these jeans has a tear. A stunning performance from the Republic of Ireland all but sealed progress to Euro as they crushed nine-man Estonia in the first leg of the qualifying play-off tie in A Le Coq Arena in Tallinn.
This proposal has no legs. Almost everyone opposes it. Synonym: on; Antonym: off Ponsonby-Smythe hit a thumping drive through the leg fielders. Hickman came in, making his legs, and stroking his cravat and ruffles. Verb To remove the legs from an animal carcass. To build legs onto a platform or stage for support. To put a series of three or more options strikes into the stock market. Noun An external body part that projects from the body.
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