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MBE Advance Access originally published online on December 10, 2008
Molecular Biology and Evolution 2009 26(3):613-622; doi:10.1093/molbev/msn282
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Adaptive Evolution of 5'HoxD Genes in the Origin and Diversification of the Cetacean Flipper

Zhe Wang*, Lihong Yuan{dagger}, Stephen J. Rossiter{ddagger}, Xueguo Zuo*, Binghua Ru*, Hui Zhong*, Naijian Han§, Gareth Jones||, Paul D. Jepson and Shuyi Zhang*

* School of Life Science, East China Normal University, Shanghai, China
{dagger} Guangdong Entomological Institute, Guangzhou, China
{ddagger} School of Biological and Chemical Sciences, Queen Mary, University of London, London, United Kingdom
§ Institute of Zoology, Chinese Academy of Sciences, Beijing, China
|| School of Biological Sciences, University of Bristol, Bristol, United Kingdom
Institute of Zoology, Zoological Society of London, Regent's Park, London, United Kingdom

E-mail: syzhang{at}bio.ecnu.edu.cn; s.j.rossiter{at}qmul.ac.uk.

Accepted for publication December 6, 2008.

The homeobox (Hox) genes Hoxd12 and Hoxd13 control digit patterning and limb formation in tetrapods. Both show strong expression in the limb bud during embryonic development, are highly conserved across vertebrates, and show mutations that are associated with carpal, metacarpal, and phalangeal deformities. The most dramatic evolutionary reorganization of the mammalian limb has occurred in cetaceans (whales, dolphins, and porpoises), in which the hind limbs have been lost and the forelimbs have evolved into paddle-shaped flippers. We reconstructed the phylogeny of digit patterning in mammals and inferred that digit number has changed twice in the evolution of the cetacean forelimb. First, the divergence of the early cetaceans from their even-toed relatives coincided with the reacquisition of the pentadactyl forelimb, whereas the ancestors of tetradactyl baleen whales (Mysticeti) later lost a digit again. To test whether the evolution of the cetacean forelimb is associated with positive selection or relaxation of Hoxd12 and Hoxd13, we sequenced these genes in a wide range of mammals. In Hoxd12, we found evidence of Darwinian selection associated with both episodes of cetacean forelimb reorganization. In Hoxd13, we found a novel expansion of a polyalanine tract in cetaceans compared with other mammals (17/18 residues vs. 14/15 residues, respectively), lengthening of which has previously been shown to be linked to synpolydactyly in humans and mice. Both genes also show much greater sequence variation among cetaceans than across other mammalian lineages. Our results strongly implicate 5'HoxD genes in the modulation of digit number, web forming, and the high morphological diversity of the cetacean manus.

Key Words: Hoxd12 • Hoxd13 • adaptive evolution • cetaceans • digits • flipper

The research was performed at East China Normal University.

Claudia Kappen, Associate Editor


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