The Role of Timing in the Development and Evolution of the Limb

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2023 May 18

PMID 37200627

Authors

Meng Zhu

Clifford J Tabin

Affiliations

Soon will be listed here.

Abstract

The term heterochrony was coined to describe changes in the timing of developmental processes relative to an ancestral state. Limb development is a well-suited system to address the contribution of heterochrony to morphological evolution. We illustrate how timing mechanisms have been used to establish the correct pattern of the limb and provide cases where natural variations in timing have led to changes in limb morphology.

Citing Articles

Convergent Degenerated Regulatory Elements Associated with Limb Loss in Limbless Amphibians and Reptiles.

Zhu C, Li S, Zhang D, Zhang J, Wang G, Zhou B Mol Biol Evol. 2024; 41(11).

PMID: 39530343 PMC: 11600591. DOI: 10.1093/molbev/msae239.

Splicing is dynamically regulated during limb development.

Driscoll S, Merkuri F, Chain F, Fish J Sci Rep. 2024; 14(1):19944.

PMID: 39198579 PMC: 11358489. DOI: 10.1038/s41598-024-68608-z.

On the evolutionary developmental biology of the cell.

Babonis L Trends Genet. 2024; 40(10):822-833.

PMID: 38971670 PMC: 11619940. DOI: 10.1016/j.tig.2024.06.003.

Metabolic mechanisms of species-specific developmental tempo.

Iwata R, Vanderhaeghen P Dev Cell. 2024; 59(13):1628-1639.

PMID: 38906137 PMC: 11266843. DOI: 10.1016/j.devcel.2024.05.027.

References

Richardson M, Oelschlager H . Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper. Evol Dev. 2002; 4(6):435-44. DOI: 10.1046/j.1525-142x.2002.02032.x. View

Naiche L, Papaioannou V . Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development. 2003; 130(12):2681-93. DOI: 10.1242/dev.00504. View

Chiang C, Litingtung Y, Harris M, Simandl B, Li Y, Beachy P . Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev Biol. 2001; 236(2):421-35. DOI: 10.1006/dbio.2001.0346. View

Towers M, Mahood R, Yin Y, Tickle C . Integration of growth and specification in chick wing digit-patterning. Nature. 2008; 452(7189):882-6. DOI: 10.1038/nature06718. View

Bastida M, Sheth R, Ros M . A BMP-Shh negative-feedback loop restricts Shh expression during limb development. Development. 2009; 136(22):3779-89. DOI: 10.1242/dev.036418. View

Xu X, Weinstein M, Li C, Naski M, Cohen R, Ornitz D . Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development. 1998; 125(4):753-65. DOI: 10.1242/dev.125.4.753. View

Matsubara Y, Hirasawa T, Egawa S, Hattori A, Suganuma T, Kohara Y . Anatomical integration of the sacral-hindlimb unit coordinated by GDF11 underlies variation in hindlimb positioning in tetrapods. Nat Ecol Evol. 2017; 1(9):1392-1399. DOI: 10.1038/s41559-017-0247-y. View

Cook L, Newton A, Hipsley C, Pask A . Postnatal development in a marsupial model, the fat-tailed dunnart (Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae). Commun Biol. 2021; 4(1):1028. PMC: 8413461. DOI: 10.1038/s42003-021-02506-2. View

Khokha M, Hsu D, Brunet L, Dionne M, Harland R . Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet. 2003; 34(3):303-7. DOI: 10.1038/ng1178. View

10.

Zhu J, Nakamura E, Nguyen M, Bao X, Akiyama H, Mackem S . Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell. 2008; 14(4):624-32. PMC: 8284562. DOI: 10.1016/j.devcel.2008.01.008. View

11.

Apesteguia S, Zaher H . A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature. 2006; 440(7087):1037-40. DOI: 10.1038/nature04413. View

12.

Tabin C, Wolpert L . Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev. 2007; 21(12):1433-42. DOI: 10.1101/gad.1547407. View

13.

Riddle R, Johnson R, Laufer E, Tabin C . Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 1993; 75(7):1401-16. DOI: 10.1016/0092-8674(93)90626-2. View

14.

Blueweiss L, Fox H, Kudzma V, Nakashima D, Peters R, Sams S . Relationships between body size and some life history parameters. Oecologia. 2017; 37(2):257-272. DOI: 10.1007/BF00344996. View

15.

Rallis C, Bruneau B, del Buono J, Seidman C, Seidman J, Nissim S . Tbx5 is required for forelimb bud formation and continued outgrowth. Development. 2003; 130(12):2741-51. DOI: 10.1242/dev.00473. View

16.

Lettice L, Hill A, Devenney P, Hill R . Point mutations in a distant sonic hedgehog cis-regulator generate a variable regulatory output responsible for preaxial polydactyly. Hum Mol Genet. 2007; 17(7):978-85. DOI: 10.1093/hmg/ddm370. View

17.

Cooper L, Berta A, Dawson S, Reidenberg J . Evolution of hyperphalangy and digit reduction in the cetacean manus. Anat Rec (Hoboken). 2007; 290(6):654-72. DOI: 10.1002/ar.20532. View

18.

Wolpert L . Positional information and the spatial pattern of cellular differentiation. J Theor Biol. 1969; 25(1):1-47. DOI: 10.1016/s0022-5193(69)80016-0. View

19.

MacLean G, Dolle P, Tahayato A, Chambon P, Petkovich M . Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech Dev. 2001; 107(1-2):195-201. DOI: 10.1016/s0925-4773(01)00463-4. View

20.

Zuniga A, Haramis A, McMahon A, Zeller R . Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature. 1999; 401(6753):598-602. DOI: 10.1038/44157. View