Forelimb-hindlimb developmental timing changes across tetrapod phylogeny

Bininda‐Emonds, Olaf R. P.; Jeffery, Jonathan E.; Sánchez‐Villagra, Marcelo R.; Howard, James L.; Colbert, Matthew W.; Pieau, Claude; Selwood, Lynne; Cate, Carel ten; Raynaud, A; Osabutey, Casmile K.; Richardson, Michael K.

doi:10.1186/1471-2148-7-182

Cited by 103 publications

(136 citation statements)

References 23 publications

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“…This lag is less pronounced in salamanders that develop as larvae dwelling in streams, and even less so in direct developing salamanders (Blanco and Alberch, 1992;Wake and Shubin, 1998;Vorobyeva et al, 2000;Shubin and Wake, 2003). Differences in the timing of forelimb and hind limb development are known from many tetrapod clades (Bininda-Emonds et al, 2007), but they are particularly pronounced in urodeles.…”

Section: Developmentmentioning

confidence: 99%

Salamander limb development: Integrating genes, morphology, and fossils

Fröbisch

Shubin

2011

Developmental Dynamics

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The development of the tetrapod limb during skeletogenesis follows a highly conservative pattern characterized by a general proximo‐distal progression in the establishment of skeletal elements and a postaxial polarity in digit development. Salamanders represent the only exception to this pattern and display an early establishment of distal autopodial structures, specifically the basale commune, an amalgamation of distal carpal and tarsal 1 and 2, and a distinct preaxial polarity in digit development. This deviance from the conserved tetrapod pattern has resulted in a number of hypotheses to explain its developmental basis and evolutionary history. Here we summarize the current knowledge of salamander limb development under consideration of the fossil record to provide a deep time perspective of this evolutionary pathway and highlight what data will be needed in the future to gain a better understanding of salamander limb development specifically and tetrapod limb development and evolution more broadly. Developmental Dynamics 240:1087–1099, 2011. © 2011 Wiley‐Liss, Inc.

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Section: Developmentmentioning

confidence: 99%

Salamander limb development: Integrating genes, morphology, and fossils

Fröbisch

Shubin

2011

Developmental Dynamics

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“…Moreover, one of the best studied systems of evolutionary and developmental biology is the tetrapod limb. Heterochrony, or a change in the timing of developmental processes (Smith, 2003), during early limb development and chondrogenesis of tetrapods has led to a wealth of morphological variation: for instance, the precocial development of forelimbs of marsupials (Smith, 2003;BinindaEmonds et al, 2007), the regenerative abilities of amphibian limbs (Galis et al, 2003), the precocial hindlimb development of frogs (Schlosser, 2001;Bininda-Emonds et al, 2007), the elongated digits of bats (Sears et al, 2006), and the supernumary phalanges in the digits of dolphins (Richardson & Oelschläger, 2002). This study investigates the role of heterochrony in shaping the limb of the porpoise.…”

Section: Introductionmentioning

confidence: 99%

Paedomorphic Ossification in Porpoises with an Emphasis on the Vaquita (<I>Phocoena sinus</I>)

Mellor¹,

Cooper²,

Torre³

et al. 2009

aquatic mammals

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Heterochrony, the change in timing of developmental processes, is thought to be a key process shaping the numerous limb morphologies of tetrapods. Through a delayed offset in digit development, all cetaceans (i.e., whales, dolphins, and porpoises) have evolved supernumary phalanges (hyperphalangy). Moreover, some toothed cetaceans further alter digital morphologies by delayed endochondral and perichondral ossification of individual elements. In the harbor porpoise (Phocoena phocoena), these paedomorphic patterns have created poorly ossified phalangeal elements. However, no studies have addressed this morphology in other porpoise taxa. This study documents the timing of carpal and digital epiphyseal ossification in the poorly studied vaquita (Phocoena sinus) based on radiographs (n = 18) of known-age specimens. Patterns of vaquita manus ossification were compared between other porpoise and delphinid taxa. Adult vaquitas are paedomorphic in carpal, metacarpal, and digital development as they maintain a juvenile ossification pattern relative to that of other porpoise species of equivalent ages. Vaquitas also ossify fewer carpal elements as compared to other porpoise and some delphinid cetaceans, and ossification arrests relative to that of the harbor porpoise. Vaquitas also display sexual dimorphism as females reach a greater body size and display more ossified elements in the manus relative to their paedomorphic male cohorts.

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“…However, fore-and hind-limb bud development in both D. aeneus and P. cinereus occurs relatively concurrently in comparison to metamorphosing species in which the hind limb may form months after advanced forelimb digit formation (see Watson and Russell, 2000;Nye et al, 2003;Wong and Liversage, 2005; but see Wake and Shubin, 1998 for an exception in streamdwelling Dicamptodon). The coordination of fore-and hind limb development is relatively fixed within amniote clades, but can be extremely variable within Lissamphibia (Bininda-Emonds et al, 2007). This variation occurs between plethodontid genera (Collazo and Marks, 1994) and within different Ambystoma species (Watson and Russell, 2000).…”

Section: Other Salamander Staging Tablesmentioning

confidence: 99%

Embryonic Staging Table for a Direct‐Developing Salamander, Plethodon cinereus (Plethodontidae)

Kerney

2011

The Anatomical Record

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This work presents a refined staging table for the direct-developing red-backed salamander Plethodon cinereus, which is based on the incomplete staging system of James Norman Dent (J Morphol 1942; 71:577-601). This common species from eastern North America is a member of the species-rich lungless salamander family Plethodontidae. The staging table presented here covers several stages omitted by Dent and reveals novel developmental features of P. cinereus embryos. These include putative Leydig cells and open gill clefts, which are found in larvae of metamorphosing species but were previously reported as absent in direct-developing Plethodon. Other features found in larvae of metamorphosing salamander species, such as the palatopterygoid bone and lateral line neuromasts, were not observed in this material. The occurrence of larval and metamorphic features in these embryos has direct bearing on the patterns of life history evolution within the plethodontidae family. This study emphasizes the degree to which typically larval structures are retained in this direct-developing species and provides a staging table for further investigations into the development and evolution of plethodontid salamanders.

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Forelimb-hindlimb developmental timing changes across tetrapod phylogeny

Cited by 103 publications

References 23 publications

Salamander limb development: Integrating genes, morphology, and fossils

Salamander limb development: Integrating genes, morphology, and fossils

Paedomorphic Ossification in Porpoises with an Emphasis on the Vaquita (<I>Phocoena sinus</I>)

Embryonic Staging Table for a Direct‐Developing Salamander, Plethodon cinereus (Plethodontidae)

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