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Patterning and post-patterning modes of evolutionary digit loss in mammals

Author

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  • Kimberly L. Cooper

    (Harvard Medical School
    Present address: Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093, USA.)

  • Karen E. Sears

    (University of Illinois Urbana-Champaign)

  • Aysu Uygur

    (Harvard Medical School)

  • Jennifer Maier

    (University of Illinois Urbana-Champaign)

  • Karl-Stephan Baczkowski

    (École Normale Supérieure de Lyon, 69007 Lyon, France)

  • Margaret Brosnahan

    (Cornell University)

  • Doug Antczak

    (Cornell University)

  • Julian A. Skidmore

    (The Camel Reproduction Centre)

  • Clifford J. Tabin

    (Harvard Medical School)

Abstract

A reduction in the number of digits has evolved many times in tetrapods, particularly in cursorial mammals that travel over deserts and plains, yet the underlying developmental mechanisms have remained elusive. Here we show that digit loss can occur both during early limb patterning and at later post-patterning stages of chondrogenesis. In the ‘odd-toed’ jerboa (Dipus sagitta) and horse and the ‘even-toed’ camel, extensive cell death sculpts the tissue around the remaining toes. In contrast, digit loss in the pig is orchestrated by earlier limb patterning mechanisms including downregulation of Ptch1 expression but no increase in cell death. Together these data demonstrate remarkable plasticity in the mechanisms of vertebrate limb evolution and shed light on the complexity of morphological convergence, particularly within the artiodactyl lineage.

Suggested Citation

  • Kimberly L. Cooper & Karen E. Sears & Aysu Uygur & Jennifer Maier & Karl-Stephan Baczkowski & Margaret Brosnahan & Doug Antczak & Julian A. Skidmore & Clifford J. Tabin, 2014. "Patterning and post-patterning modes of evolutionary digit loss in mammals," Nature, Nature, vol. 511(7507), pages 41-45, July.
  • Handle: RePEc:nat:nature:v:511:y:2014:i:7507:d:10.1038_nature13496
    DOI: 10.1038/nature13496
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    Cited by:

    1. Megan Lo & Amnon Sharir & Michael D. Paul & Hayarpi Torosyan & Christopher Agnew & Amy Li & Cynthia Neben & Pauline Marangoni & Libin Xu & David R. Raleigh & Natalia Jura & Ophir D. Klein, 2022. "CNPY4 inhibits the Hedgehog pathway by modulating membrane sterol lipids," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Marketa Kaucka & Alberto Joven Araus & Marketa Tesarova & Joshua D. Currie & Johan Boström & Michaela Kavkova & Julian Petersen & Zeyu Yao & Anass Bouchnita & Andreas Hellander & Tomas Zikmund & Ahmed, 2022. "Altered developmental programs and oriented cell divisions lead to bulky bones during salamander limb regeneration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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