Atavisms in the Avian Hindlimb and Early Developmental Polarity of the Limb

Overview

Journal Dev Dyn

Publisher Wiley

Specialty Anatomy & Histology

Date 2021 Feb 19

PMID 33605505

Citations 3

Authors

Christian L Bonatto Paese

Michael Brent Hawkins

Samantha A Brugmann

Matthew P Harris

Affiliations

Soon will be listed here.

Abstract

Background: The naturally occurring chicken mutant talpid (ta ), best known for its limb and craniofacial defects, has long served as a valuable tool for developmental biologists studying growth and patterning of craniofacial structures and the limb. The mutant provides a unique tool to examine the molecular and cellular processes regulating limb development.

Results: This mutant also provides unique insights into the evolution of developmental genetic programs. Previous work defined the appearance of atavistic dentition in ta embryos. Herein we describe the appearance of ancestral characters of the hindlimb in embryonic ta chicken embryos.

Conclusion: As the ta phenotype arises as a result of mutation in C2CD3 and disrupted cilia function, this mutant provides genetic and developmental insight into the causes of asymmetry in the limb and also a model for the evolution of the avian hindlimb.

Citing Articles

The ciliary protein C2cd3 is required for mandibular musculoskeletal tissue patterning.

Brooks E, Han S, Bonatto Paese C, Lewis A, Aarnio-Peterson M, Brugmann S Differentiation. 2024; 138:100782.

PMID: 38810379 PMC: 11227401. DOI: 10.1016/j.diff.2024.100782.

Atavistic and vestigial anatomical structures in the head, neck, and spine: an overview.

Dhawan S, Yedavalli V, Massoud T Anat Sci Int. 2023; 98(3):370-390.

PMID: 36680662 DOI: 10.1007/s12565-022-00701-7.

(Non)Parallel developmental mechanisms in vertebrate appendage reduction and loss.

Swank S, Sanger T, Stuart Y Ecol Evol. 2021; 11(22):15484-15497.

PMID: 34824770 PMC: 8601893. DOI: 10.1002/ece3.8226.

References

Seki R, Kamiyama N, Tadokoro A, Nomura N, Tsuihiji T, Manabe M . Evolutionary and developmental aspects of avian-specific traits in limb skeletal pattern. Zoolog Sci. 2012; 29(10):631-44. DOI: 10.2108/zsj.29.631. View

Harris M, Hasso S, Ferguson M, Fallon J . The development of archosaurian first-generation teeth in a chicken mutant. Curr Biol. 2006; 16(4):371-7. DOI: 10.1016/j.cub.2005.12.047. View

Smith C, Farlie P, Davidson N, Roeszler K, Hirst C, Oshlack A . Limb patterning genes and heterochronic development of the emu wing bud. Evodevo. 2016; 7:26. PMC: 5168868. DOI: 10.1186/s13227-016-0063-5. View

Hampe A . [The competition between the osseous elements of the zeugopod of the chicken]. J Embryol Exp Morphol. 1960; 8:241-5. View

Huangfu D, Liu A, Rakeman A, Murcia N, Niswander L, Anderson K . Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature. 2003; 426(6962):83-7. DOI: 10.1038/nature02061. View

Charite J, McFADDEN D, Olson E . The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of the zone of polarizing activity during limb development. Development. 2000; 127(11):2461-70. DOI: 10.1242/dev.127.11.2461. View

Hall B . Development mechanisms underlying the formation of atavisms. Biol Rev Camb Philos Soc. 1984; 59(1):89-124. DOI: 10.1111/j.1469-185x.1984.tb00402.x. View

Goff D, Tabin C . Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. Development. 1997; 124(3):627-36. DOI: 10.1242/dev.124.3.627. View

Wang S, Stiegler J, Amiot R, Wang X, Du G, Clark J . Extreme Ontogenetic Changes in a Ceratosaurian Theropod. Curr Biol. 2016; 27(1):144-148. DOI: 10.1016/j.cub.2016.10.043. View

10.

Caruccio N, Martinez-Lopez A, Harris M, Dvorak L, Bitgood J, Simandl B . Constitutive activation of sonic hedgehog signaling in the chicken mutant talpid(2): Shh-independent outgrowth and polarizing activity. Dev Biol. 1999; 212(1):137-49. DOI: 10.1006/dbio.1999.9321. View

11.

Dvorak L, Fallon J . Talpid2 mutant chick limb has anteroposterior polarity and altered patterns of programmed cell death. Anat Rec. 1991; 231(2):251-60. DOI: 10.1002/ar.1092310213. View

12.

Te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans H, Meijlink F . Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science. 2002; 298(5594):827-30. DOI: 10.1126/science.1075620. View

13.

Muller G, Alberch P . Ontogeny of the limb skeleton in Alligator mississippiensis: Developmental invariance and change in the evolution of archosaur limbs. J Morphol. 2018; 203(2):151-164. DOI: 10.1002/jmor.1052030204. View

14.

Dahn R, Fallon J . Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science. 2000; 289(5478):438-41. DOI: 10.1126/science.289.5478.438. View

15.

Hamburger V, HAMILTON H . A series of normal stages in the development of the chick embryo. J Morphol. 2014; 88(1):49-92. View

16.

Tomic N, Meyer-Rochow V . Atavisms: medical, genetic, and evolutionary implications. Perspect Biol Med. 2011; 54(3):332-53. DOI: 10.1353/pbm.2011.0034. View

17.

Litingtung Y, Dahn R, Li Y, Fallon J, Chiang C . Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature. 2002; 418(6901):979-83. DOI: 10.1038/nature01033. View

18.

Wang B, Fallon J, Beachy P . Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell. 2000; 100(4):423-34. DOI: 10.1016/s0092-8674(00)80678-9. View

19.

BAUR G . A complete fibula in an adult living carinatebird. Science. 1885; 5(118):375. DOI: 10.1126/science.ns-5.118.375-a. View

20.

Young J, Grayson P, Edwards S, Tabin C . Attenuated Fgf Signaling Underlies the Forelimb Heterochrony in the Emu Dromaius novaehollandiae. Curr Biol. 2019; 29(21):3681-3691.e5. PMC: 6834345. DOI: 10.1016/j.cub.2019.09.014. View