Meckel's Cartilage Breakdown Offers Clues to Mammalian Middle Ear Evolution

Overview

Journal Nat Ecol Evol

Publisher Springer Nature

Specialty Biology

Date 2017 May 2

PMID 28459103

Citations 20

Authors

Neal Anthwal

Daniel J Urban

Zhe Xi Luo

Karen E Sears

Abigail S Tucker

Affiliations

Soon will be listed here.

Abstract

A key transformation in mammalian ear evolution was incorporation of the primary jaw joint of premammalian synapsids into the definitive mammalian middle ear of living mammals. This evolutionary transition occurred in two-steps, starting with a partial or "transitional" mammalian middle ear in which the ectotympanic and malleus were still connected to the mandible by an ossified Meckel's Cartilage (MC), as observed in many Mesozoic mammals. This was followed by MC breakdown, freeing the ectotympanic and the malleus from the mandible and creating the definitive mammalian middle ear. Here we report novel findings on the role of chondroclasts in MC breakdown, shedding light on how therian mammals lost MC connecting the ear to the jaw. Genetic or pharmacological loss of clast cells in mice and opossums leads to persistence of embryonic MC beyond juvenile stages, with MC ossification in mutant mice. The persistent MC causes a distinctive postnatal groove on the mouse dentary. This morphology phenocopies the ossified MC and Meckelian groove observed in Mesozoic mammals. Clast cell recruitment to MC is not observed in reptiles, where MC persists as a cartilaginous structure. We hypothesize that ossification of MC is an ancestral feature of mammaliaforms, and that a shift in the timing of clast cell recruitment to MC prior to its ossification is a key developmental mechanism for the evolution of the definitive mammalian middle ear in extant therians.

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References

Smith K . Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Dev Dyn. 2006; 235(5):1181-93. DOI: 10.1002/dvdy.20676. View

Maier W, Ruf I . Evolution of the mammalian middle ear: a historical review. J Anat. 2015; 228(2):270-83. PMC: 4718169. DOI: 10.1111/joa.12379. View

Sakakura Y, Tsuruga E, Irie K, Hosokawa Y, Nakamura H, Yajima T . Immunolocalization of receptor activator of nuclear factor-kappaB ligand (RANKL) and osteoprotegerin (OPG) in Meckel's cartilage compared with developing endochondral bones in mice. J Anat. 2005; 207(4):325-37. PMC: 1571553. DOI: 10.1111/j.1469-7580.2005.00466.x. View

Abzhanov A . von Baer's law for the ages: lost and found principles of developmental evolution. Trends Genet. 2013; 29(12):712-22. DOI: 10.1016/j.tig.2013.09.004. View

Wang Z, Ovitt C, Grigoriadis A, Ruther U, Wagner E . Bone and haematopoietic defects in mice lacking c-fos. Nature. 1992; 360(6406):741-5. DOI: 10.1038/360741a0. View

Anthwal N, Joshi L, Tucker A . Evolution of the mammalian middle ear and jaw: adaptations and novel structures. J Anat. 2012; 222(1):147-60. PMC: 3552421. DOI: 10.1111/j.1469-7580.2012.01526.x. View

Ealba E, Jheon A, Hall J, Curantz C, Butcher K, Schneider R . Neural crest-mediated bone resorption is a determinant of species-specific jaw length. Dev Biol. 2015; 408(1):151-63. PMC: 4698309. DOI: 10.1016/j.ydbio.2015.10.001. View

Knowles H, Moskovsky L, Thompson M, Grunhen J, Cheng X, Kashima T . Chondroclasts are mature osteoclasts which are capable of cartilage matrix resorption. Virchows Arch. 2012; 461(2):205-10. DOI: 10.1007/s00428-012-1274-3. View

Ji Q, Luo Z, Zhang X, Yuan C, Xu L . Evolutionary development of the middle ear in Mesozoic therian mammals. Science. 2009; 326(5950):278-81. DOI: 10.1126/science.1178501. View

10.

Amin S, Tucker A . Joint formation in the middle ear: lessons from the mouse and guinea pig. Dev Dyn. 2006; 235(5):1326-33. DOI: 10.1002/dvdy.20666. View

11.

Arai A, Mizoguchi T, Harada S, Kobayashi Y, Nakamichi Y, Yasuda H . Fos plays an essential role in the upregulation of RANK expression in osteoclast precursors within the bone microenvironment. J Cell Sci. 2012; 125(Pt 12):2910-7. DOI: 10.1242/jcs.099986. View

12.

Sanchez-Villagra M, Gemballa S, Nummela S, Smith K, Maier W . Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J Morphol. 2002; 251(3):219-38. DOI: 10.1002/jmor.1085. View

13.

Takechi M, Kuratani S . History of studies on mammalian middle ear evolution: a comparative morphological and developmental biology perspective. J Exp Zool B Mol Dev Evol. 2010; 314(6):417-33. DOI: 10.1002/jez.b.21347. View

14.

Wang Y, Zheng Y, Chen D, Chen Y . Enhanced BMP signaling prevents degeneration and leads to endochondral ossification of Meckel's cartilage in mice. Dev Biol. 2013; 381(2):301-11. PMC: 3777720. DOI: 10.1016/j.ydbio.2013.07.016. View

15.

Wilson J, Tucker A . Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev Biol. 2004; 266(1):138-50. DOI: 10.1016/j.ydbio.2003.10.012. View

16.

Boyce B, Yao Z, Zhang Q, Guo R, Lu Y, Schwarz E . New roles for osteoclasts in bone. Ann N Y Acad Sci. 2007; 1116:245-54. DOI: 10.1196/annals.1402.084. View

17.

Raff R . Written in stone: fossils, genes and evo-devo. Nat Rev Genet. 2007; 8(12):911-20. DOI: 10.1038/nrg2225. View

18.

Luo Z . Transformation and diversification in early mammal evolution. Nature. 2007; 450(7172):1011-9. DOI: 10.1038/nature06277. View

19.

Rogers M, Crockett J, Coxon F, Monkkonen J . Biochemical and molecular mechanisms of action of bisphosphonates. Bone. 2010; 49(1):34-41. DOI: 10.1016/j.bone.2010.11.008. View

20.

Yang L, Tsang K, Tang H, Chan D, Cheah K . Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc Natl Acad Sci U S A. 2014; 111(33):12097-102. PMC: 4143064. DOI: 10.1073/pnas.1302703111. View