The evolutionary adaptations of ancient lobe-finned fish transformed pectoral fins used underwater into strong, bony structures that enabled emerging tetrapods, animals with limbs, to allow them crawl in shallow water or on land. 

The disconnect between paleontology and evolutionary biology has been why the modern structure called the autopod, comprising wrists and fingers or ankles and toes, has no obvious morphological counterpart in the fins of living fishes. 

In a Proceedings of the National Academy of Sciences paper, researchers argue previous efforts to connect fin and fingers fell short because they focused on the wrong fish. Instead, they found the rudimentary genetic machinery for mammalian autopod assembly in a non-model fish, the spotted gar, whose genome was recently sequenced.

The same autopod-building genetic switches from gar are able to drive gene activity (purple) in the digits of transgenic mice; an activity that was absent in other fish groups studied. Credit Andrew Gehrke, the University of Chicago

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The primary genes that shape the bones, known as the HoxD and HoxA clusters, also differ. The researchers first tested the ability of genetic "switches" that control HoxD and HoxA genes from teleosts--bony, ray-finned fish--to shape the limbs of developing transgenic mice. The fish control switches, however, did not trigger any activity in the autopod.

Teleost fish--a vast group that includes almost all of the world's important sport and commercial fish--are widely studied. But the researchers began to realize they were not the ideal comparison for studies of how ancient genes were regulated. When they searched for wrist and digit-building genetic switches, they found "a lack of sequence conservation" in teleost species.

They traced the problem to a radical change in the genetics of teleost fish. More than 300 million years ago, after the fish-like creatures that would become tetrapods split off from other bony fish, a common ancestor of the teleost lineage went through a whole-genome duplication (WGD)--a phenomenon that has occurred multiple times in evolution.

By doubling the entire genetic repertoire of teleost fish, this WGD provided them with enormous diversification potential. This may have helped teleosts to adapt, over time, to a variety of environments worldwide. In the process, "the genetic switches that control autopod-building genes were able to drift and shuffle, allowing them to change some of their function, as well as making them harder to identify in comparisons to other animals, such as mice," said Andrew Gehrke, a graduate student in the Shubin lab and lead author of the study.

Not all bony fishes went through the whole genome duplication, however. The spotted gar, a primitive freshwater fish native to North America, split off from teleost fishes before the WGD.




This study was supported by the Brinson Foundation; the National Science Foundation; the Brazilian National Council for Scientific and Technological Development grants; the National Institutes of Health; the Volkswagen Foundation, Germany; the Alexander von Humboldt-Foundation, the Spanish and Andalusian governments; and Proyecto de Excelencia.

Additional authors include Mayuri Chandran and Tetsuya Nakamura from the University of Chicago; Igor Schneider from the Instituto de Ciencias Biologicas, Universida de Federal do Para, Belem, Brazil; Elisa de la Calle-Mustienes, Juan J. Tena, Carlos Gomez-Marin and José Luis Gómez-Skarmeta from the Centro Andaluz de Biología del Desarrollo, Sevilla, Spain; and Ingo Braasch and John H. Postlethwait from the Institute of Neuroscience, University of Oregon.