Lungfish Provides Insight to Life On Land: 'Humans Are Just Modified Fish'
ScienceDaily (Oct. 7, 2011) — A study into the muscle development of several different fish has given insights into the genetic leap that set the scene for the evolution of hind legs in terrestrial animals. This innovation gave rise to the tetrapods -- four-legged creatures, and our distant ancestors -- that made the first small steps on land some 400 million years ago.
Pectoral fin muscle formation in paddlefish (Polyodon spathula) utilises the fully derived mode of appendicular muscle formation and is not associated with an epithelial extension. (Credit: Cole et al., PLoS Biology, DOI: 10.1371/journal.pbio.1001168)
A team of Australian scientists led by Professor Peter Currie, of the Australian Regenerative Medicine Institute at Monash University, and Dr Nicolas Cole, of the University of Sydney, report their results October 4 in online, open access journal PLoS Biology.
Scientists have long known that ancient lungfish species are the ancestors of the tetrapods. These fish could survive on land, breathing air and using their pelvic fins to propel themselves. Australia is home to three species of the few remaining lungfish -- two marine species and one inhabiting Queensland's Mary River basin.
There are big gaps in our knowledge, however. Most conclusions have previously been drawn from fossil skeletons, but the muscles critical to locomotion cannot be preserved in the fossil record. The team used fish living today to trace the evolution of pelvic fin muscles to find out how the load-bearing hind limbs of the tetrapods evolved. They compared embryos of the descendants of species representing key turning points in vertebrate evolution to see if there were differences in pelvic fin muscle formation. They studied "primitive" cartilaginous fish -- Australia's bamboo shark and its cousin, the elephant shark -- as well as three bony fishes -- the Australian lungfish, the zebrafish and the American paddlefish. The bony fish and in particular the lungfish are the closest living relative of the tetrapods' most recent common ancestor with fish.
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Development and Evolution of the Muscles of the Pelvic Fin
Nicholas J. Cole1,2*, Thomas E. Hall1,3, Emily K. Don2, Silke Berger1,3, Catherine A. Boisvert3,Christine Neyt1,4, Rolf Ericsson5, Jean Joss5,David B. Gurevich3, Peter D. Currie1,3*
1 Victor Chang Cardiac Research Institute, Sydney, New South Wales, Australia, 2 Anatomy & Histology, School of Medical Science and Bosch Institute, The University of Sydney, New South Wales, Australia, 3 Australian Regenerative Medicine Institute, Monash University, Clayton, Australia, 4 Expression Genomics Laboratory, Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland, Australia, 5Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia
Abstract
Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.
Author Summary
The transition of vertebrates from water to land is a fundamental step in the evolution of terrestrial life. Innovations that were critical to this transition were the evolution of a weight bearing pelvis, hindlimbs and their associated musculature, and the development of the “rear wheel drive” strategy that predominates in terrestrial locomotion. The fossil record can reveal how the skeletal framework of the load-bearing limbs of tetrapods (animals descended from fish) has evolved, but as soft tissues are rarely preserved within the fossil record, it can shed little light on how the accompanying dramatic alterations of the limb musculature arose developmentally. To examine this question we determined the mechanisms that generate fin muscles within larvae of living species representing several clades of fish across the vertebrate phylogeny. Using this comparative approach and a novel somite transplantation technique in zebrafish, we determine that the pelvic fin muscles of bony fish are generated by a bimodal mechanism that has features of limb/fin muscle formation in tetrapods and primitive cartilaginous fish. Using these data, we propose a unifying evolutionary hypothesis on the origins of the muscle of the paired fins and limbs, and speculate that the adoption of tetrapod mode of hindlimb muscle formation was also an evolutionary innovation critical to the success of the tetrapod transition.
Citation: Cole NJ, Hall TE, Don EK, Berger S, Boisvert CA, et al. (2011) Development and Evolution of the Muscles of the Pelvic Fin. PLoS Biol 9(10): e1001168.
doi:10.1371/journal.pbio.1001168
doi:10.1371/journal.pbio.1001168
Academic Editor: Anthony Graham, King's College London, United Kingdom
Received: November 21, 2010; Accepted: August 24, 2011; Published: October 4, 2011
Copyright: © 2011 Cole et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by an ARC Discovery grant to PDC. The Australian Regenerative Medicine Institute at the Monash University is supported by grants from the Australian Government and the State Government of Victoria, Australia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
