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.
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The probe sequence data for all genes and species has been deposited in the NCBI Probes database with the following accession numbers: CAMELBMP4, Pr032067180; CAMELFGF8, Pr032067181; CAMELGLI1, Pr032067182; CAMELHOXD13, Pr032067183; CAMELPTCH1, Pr032067184; HORSEBMP4, Pr032067185; HORSEFGF8, Pr032067186; HORSEGLI1, Pr032067187; HORSEHOXD13, Pr032067188; HORSEMSX2, Pr032067189; HORSEPTCH1, Pr032067190; HORSESHH, Pr032067191; JERBOABMP4, Pr032067192; JERBOAFGF8, Pr032067193; JERBOAGLI1, Pr032067194; JERBOAHOXD13, Pr032067195; JERBOAMSX2, Pr032067196; JERBOAPTCH1, Pr032067197; JERBOASHH, Pr032067198; MOUSEBMP4, Pr032067199; MOUSEFGF8, Pr032067200; MOUSEGLI1, Pr032067201; MOUSEHOXD13, Pr032067202; MOUSEMSX2, Pr032067203; MOUSEPTCH1, Pr032067204; MOUSESHH, Pr032067205; PIGFGF8, Pr032067206; PIGPTCH1, Pr032067207; PIGSHH, Pr032067208.
We thank J. Lopez-Rios and R. Zeller (University of Basel, Switzerland) for generously providing data and discussion before publication. We also thank J. Carlos Izpisua Belmonte and A. Aguirre for sharing space and materials to complete experiments subsequent to review. Jerboa embryos were harvested with the assistance of S. Wu and colleagues in Xinjiang, China. Pig embryos were harvested with the assistance of D. Urban. Additional horse embryos were provided by R. Turner and H. Galatino-Homer (University of Pennsylvania) and by R. Fritsche and S. Lyle (Louisiana State University). Mouse Gli1 probe plasmid, used in the pig in situ, was provided by A. Joyner. This work was supported by NIH grant R37HD032443 to C.J.T., and NSF IOS grant 1257873 to K.E.S.
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BMC Evolutionary Biology (2017)