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How did human limbs evolve?

Sharks, skates, and rays are odd. They have appendages growing out of their gill arch — a small cradle of bones that supports their gills. This peculiarity has led to the idea that our own legs and arms, and longer ago the paired fins of fish, evolved from transforming gill arches in very early fish.


Genetic evidence for this theory was just published in the journal Development, by J. Andrew Gillis and co-author Brian K. Hall. Their work points out the striking similarities in the genetic mechanism that patterns gill arches (or branchial rays) and fins in fish, to limbs in animals.

Brian K. Hall DSc, LLD, is the George S. Campbell Professor of Biology and University Research, and Professor Emeritus at Dalhousie University in Halifax, Nova Scotia.


Over the course of his career, Hall’s laboratory research has focused on both developmental and evolutionary biology, playing a major role in integrating both fields into the discipline now known as Evolutionary Developmental Biology or evo-devo.


Campbell and his students have pioneered an epigenetic view of bone differentiation and vertebrate development, highlighting epigenetic interactions in vertebrate evolution. His 1975 paper “Evolutionary consequences of skeletal differentiation” published in American Zoologist, marked the beginning of “a bridge between evolutionary and developmental biology from the developmental biology side.” In 2007, Dr. Hall wrote the book Fins into Limbs, Evolution, Development, and Transformation,

Studying embryos of the skate, Gillis has focused on the gene Sonic hedgehog (SHH), which produces a protein that signals development of the animal limb. Gillis found that Sonic hedgehog's role in the structure of gills — that branch out from the hyoid and branchial arches of the skate — closely parallels the animal limb. The SHH protein sets up the axis for this development, and then maintains growth of the limb skeleton.


"The shared role of Sonic hedgehog in patterning branchial rays and limbs may be due to a deep evolutionary relationship between the two. Or it may simply be that two unrelated appendages independently use the same gene for the same function.

"Branchial rays will figure prominently in the story of the evolutionary origin of vertebrate animal appendages, either by shedding light on the evolutionary antecedent of paired fins/limbs, or by teaching us about the genetic mechanisms that animals can use to invent new appendages."

J. Andrew Gillis PhD, Research Fellow, Royal Society of the University of Cambridge, United Kingdom (UK), and Whitman Center scientist, Marine Biological Laboratory (MBL), Woods Hole, Massachusetts, USA.


Ongoing studies comparing the function of other genes during branchial ray and fin/limb development will help lead to a resolution of this question.

Abstract
Chondrichthyans (sharks, skates, rays and holocephalans) possess paired appendages that project laterally from their gill arches, known as branchial rays. This led Carl Gegenbaur to propose that paired fins (and hence tetrapod limbs) originally evolved via transformation of gill arches. Tetrapod limbs are patterned by a sonic hedgehog (Shh)-expressing signalling centre known as the zone of polarising activity, which establishes the anteroposterior axis of the limb bud and maintains proliferative expansion of limb endoskeletal progenitors. Here, we use loss-of-function, label-retention and fate-mapping approaches in the little skate to demonstrate that Shh secretion from a signalling centre in the developing gill arches establishes gill arch anteroposterior polarity and maintains the proliferative expansion of branchial ray endoskeletal progenitor cells. These findings highlight striking parallels in the axial patterning mechanisms employed by chondrichthyan branchial rays and paired fins/limbs, and provide mechanistic insight into the anatomical foundation of Gegenbaur's gill arch hypothesis.

Citation:
Gillis, J. Andrew and Brian K. Hall (2016) A shared role for sonic hedgehog signaling in patterning chondrichthyan gill arch appendages and tetrapod limbs. Development, doi:10.1242/dev.133884.

Received December 4, 2015.
Accepted February 22, 2016.

Author contributions
J.A.G. conceived the study, designed and conducted the experiments, analysed the data and wrote the manuscript with input from B.K.H.

Competing interests
The authors declare no competing or financial interests.

Funding
This research was supported by a Royal Society University Research Fellowship [UF130182 to J.A.G.]; by Plum Foundation John E. Dowling and Laura and Arthur Colwin Endowed Summer Research Fellowships at the Marine Biological Laboratory to J.A.G.; by a grant from the University of Cambridge Isaac Newton Trust [14.23z to J.A.G.]; and by a grant from the Natural Sciences and Engineering Research Council of Canada [A5056 to B.K.H.].


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May 6, 2016   Fetal Timeline   Maternal Timeline   News   News Archive   


Looking at the underside of a late stage developing baby skate (Leucoraja Erinacea),
the gill arches sit on either side of its head just below the skates' eyes.
Image Credit: J. Andrew Gillis


 


 

 


 

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