Links between Thyroid Hormone Alterations and Developmental Changes in the Evolution of the Weberian Apparatus

doi:10.1017/9781316832172.014

13 - Links between Thyroid Hormone Alterations and Developmental Changes in the Evolution of the Weberian Apparatus

Published online by Cambridge University Press: 31 December 2018

Fedor N. Shkil and

Daria V. Kapitanova

Edited by

Zerina Johanson ,

Charlie Underwood and

Martha Richter

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Zerina Johanson: Affiliation:
Natural History Museum, London
Charlie Underwood: Affiliation:
Birkbeck, University of London
Martha Richter: Affiliation:
Natural History Museum, London

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Summary

The Weberian apparatus (WA), a structure consisting of the greatly modified four anteriormost vertebral elements, enhances the hearing in Otophysi. Since WA is one of the most spectacular examples of vertebral column transformation and regionalization, the mechanisms underpinning WA origin and evolution have received considerable attention. A number of hypotheses exist, but a consensus has not been reached, primarily due to the relative paucity of experimental data. One of the most plausible propositions concerning the leading role of specific developmental changes in WA evolution, likely constituting differences in gene expression, was offered by Bird and Hernandez (2009). Here, we provide an analysis of developmental and morphological data obtained from experiments with cyprinids, in which developmental deviations were caused by induced hypo- and hyperthyroidism. The synthesis of our results with morphological and developmental data obtained in different teleosts empirically demonstrates the involvement of different developmental changes in WA evolution. Moreover, our results emphasize the potential role of thyroid signaling pathway in bony fish (Osteichthyes) evolution, including the origin of various types of morphological novelties.

Type: Chapter
Information: Evolution and Development of Fishes , pp. 227 - 240

DOI: https://doi.org/10.1017/9781316832172.014 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2019

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References

Abouheif, E, Favé, MJ, Ibarrarán-Viniegra, AS, Lesoway, MP, Rafiqi, AM, Rajakumar, R. 2014. Eco-evo-devo: The time has come. Adv Exp Med Biol 781:107–125.Google Scholar

Alberch, P, Alberch, J. 1981. Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander Bolitoglossa occidentalis (Amphibia: Plethodontidae). J Morph 167:249–264.CrossRef Google Scholar PubMed

Alexander, RMcN. 1962. The structure of the Weberian apparatus in the Cyprini. Proc Zool Soc Lond 139:451–473.CrossRef Google Scholar

Alexander, RMcN. 1964. The structure of the Weberian apparatus in the Siluri. Proc Zool Soc Lond 142:419–440.Google Scholar

Aranda, A, Pascual, A. 2001. Nuclear hormone receptors and gene expression. Physiol Rev 81:1269–1304.Google Scholar

Arratia, G. 1987. Description of the primitive family Diplomystidae (Siluriformes, Teleostei, Pisces): Morphology, taxonomy and phylogenetic implications. Bonn Zool Forschung Mus Alexander Koenig. pp 1–120.Google Scholar

Bassett, JHD, Williams, GR. 2016. Role of thyroid hormones in skeletal development and bone maintenance. Endocr Rev 37:135–187.CrossRef Google Scholar PubMed

Beer de, GR. 1940. Embryos and Ancestors. Oxford: Clarendon Press.Google Scholar

Berardi, AC, Oliva, F, Berardocco, M, la Rovere, M, Accorsi, P, Maffulli, N. 2014. Thyroid hormones increase collagen I and cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J 4:285–291.Google Scholar

Bird, NC, Hernandez, LP. 2007. Morphological variation in the Weberian apparatus of Cypriniformes. J Morph 268:739–757.Google Scholar

Bird, NC, Hernandez, LP. 2009. Building an evolutionary innovation: Differential growth in the modified vertebral elements of the zebrafish Weberian apparatus. Zootaxa 112:97–112.Google Scholar

Bird, NC, Mabee, PM. 2003. Developmental morphology of the axial skeleton of the zebrafish Danio rerio (Ostariophysi: Cyprinidae). Dev Dyn 228:337–357.Google Scholar

Blanton, ML, Specker, JL. 2007. The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37:97–115.Google Scholar

Bogutskaya, NG. 1991. Development of the Weberian apparatus in the ontogeny of some species of Cyprinidae. Vopr Ikhtiol 31:363–372.Google Scholar

Brent, GA. 2012. Mechanisms of thyroid hormone action. J Clin Invest 122:3035–3043.Google Scholar

Britz, R, Conway, KW. 2009. Osteology of Paedocypris, a miniature and highly developmentally truncated fish (Teleostei: Ostariophysi: Cyprinidae). J Morph 270:389–412.Google Scholar

Britz, R, Hoffmann, M. 2006. Ontogeny and homology of the claustra in Otophysan Ostariophysi (Teleostei). J Morph 267:909–923.Google Scholar

Brown, DD. 1997. The role of thyroid hormone in zebrafish and axolotl development. Proc Natl Acad Sci USA 94:13011–13016.Google Scholar

Chardon, M, Parmentier, E, Vandewalle, P. 2003. Morphology, development and evolution of the Weberian apparatus in catfish. In: Arratia, G, Kapoor, BG, Chardon, M, Diogo, R, editors. Catfishes. Vol. 1. Enfield: Science Publishers. pp. 71–120.Google Scholar

Chardon, M, Vandewalle, P. 1997. Evolutionary trends and possible origin of the Weberian apparatus. Neth J Zool 47:383–403.Google Scholar

Coburn, MM, Futey, LM. 1996. The ontogeny of supraneurals and neural arches in the cypriniform Weberian apparatus (Teleostei: Ostariophysi). Zool J Linn Soc 116:333–346.Google Scholar

Colnot, C, Alliston, T. 2010. Tissue interaction in long bone development. Bone Dev 6:25–37.Google Scholar

Conway, KW, Chen, WJ, Mayden, RL. 2008. The “celestial pearl danio” is a miniature Danio (ss) (Ostariophysi: Cyprinidae): Evidence from morphology and molecules. Zootaxa 1686:1–28.Google Scholar

Depew, MJ. 2008. Analysis of skeletal ontogenesis through differential staining of bone and cartilage. Methods Mol Biol 461:37–45.Google Scholar

de Pinna, M, Grande, T. 2003. Ontogeny of the accessory neural arch in pristigasteroid clupeomorphs and its bearing on the homology of the otophysan claustrum (Teleostei). Copeia 2003:838–845.Google Scholar

Desjardin, C, Charles, C, Benoist-Lasselin, C, Riviere, J, Gilles, M, Chassande, O, Morgenthaler, C, Laloé, D, Lecardonnel, J, Flamant, F, Legeai-Mallet, L, Schibler, L. 2014. Chondrocytes play a major role in the stimulation of bone growth by thyroid hormone. Endocrinology 155:3123–3135.Google Scholar

Diogo, R. 2009. Origin, evolution and homologies of the Weberian apparatus: A new insight. Int J Morph 27:333–354.Google Scholar

Fink, SV, Fink, WL. 1981. Interrelationships of the ostariophysan fishes (Teleostei). Zool J Linn Soc 72:297–353.Google Scholar

Gayet, M. 1986. About ostariophysan fishes: A reply to S. V. Fink, P. H. Greenwood, and W. L. Fink’s criticism. Bull mus nat d’hist natur Paris Sect C 8:393–409.Google Scholar

Glantz, SA. 1999. Mediko-biologicheskaya statistika (Biomedical Statistics). Moscow: Praktika.Google Scholar

Goldschmidt, R. 1940. The Material Basis of Evolution. New Haven, CT: Yale University Press.Google Scholar

Gould, SJ. 1977. Ontogeny and Phylogeny. Cambridge: Harvard University Press.Google Scholar

Grande, T, de Pinna, M. 2004. The evolution of the Weberian apparatus: A phylogenetic perspective. In: Arratia, G, Tintori, A, editors. Mesozoic Fishes: Systematics and Biodiversity. München: Verlag Pfeil. pp. 429–448.Google Scholar

Grande, T, Shardo, JD. 2002. Morphology and development of the postcranial skeleton in the channel catfish Ictalurus punctatus (Ostariophysi: Siluriformes). Fieldiana Zool 99:1–30.Google Scholar

Grande, T, Young, B. 2004. The ontogeny and homology of the Weberian apparatus in the zebrafish Danio rerio (Ostariophysi: Cypriniformes). Zool J Linn Soc 140:241–254.Google Scholar

Hall, BK. 1984. Developmental mechanisms underlying the formation of atavisms. Biol Rev Camb Philos Soc 59:89–122.Google Scholar

Hall, BK. 2005. Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. Elsevier: Academic Press.Google Scholar

Heyland, A, Hodin, J, Reitzel, AM. 2005. Hormone signaling in evolution and development: A non-model system approach. Bioessays 27:64–75.Google Scholar

Hoffmann, M, Britz, R. 2006. Ontogeny and homology of the neural complex of otophysan Ostariophysi. Zool J Linn Soc 147:301–330.Google Scholar

Hulbert, AJ. 2000. Thyroid hormones and their effects: A new perspective. Biol Rev Camb Philos Soc 75:519–631.Google Scholar

De Jesus, EGT, Toledo, JD, Simpas, MS. 1998. Thyroid hormones promote early metamorphosis in grouper (Epinephelus coioides) larvae. Gen Comp Endocrinol 112:10–16.Google Scholar

Kapitanova, DV, Shkil, FN. 2014a. Effects of thyroid hormone level alterations on the development of supraneural series in zebrafish, Danio rerio. J Appl Ichthyol 30:821–824.Google Scholar

Kapitanova, DV, Shkil, FN. 2014b. Effects of thyroid hormone level alterations on the Weberian apparatus ontogeny of cyprinids (Cyprinidae; Teleostei). Rus J Dev Biol 45:313–323.Google Scholar

Kitano, J, Lema, SC, Luckenbach, JA, Mori, S, Kawagishi, Y, Kusakabe, M, Swanson, P, Peichel, CL. 2010. Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr Biol 20:2124–2130.Google Scholar

Kress, E, Samarut, J, Plateroti, M. 2008. Thyroid hormones and the control of cell proliferation or cell differentiation: Paradox or duality? Mol Cell Endocrin 313:36–49.Google Scholar

Laudet, V. 2011. The origins and evolution of vertebrate metamorphosis. Curr Biol 21:R726–737.Google Scholar

Little, AG, Seebacher, F. 2014. The evolution of endothermy is explained by thyroid hormone-mediated responses to cold in early vertebrates. J Exp Biol 217:1642–1648.CrossRef Google Scholar PubMed

McNamara, KJ. 2012. Heterochrony: The evolution of development. Evol Educ Outreach 5:203–218.Google Scholar

Nelson, EM. 1948. The comparative morphology of the Weberian apparatus of the Catostomidae and its significance in systematics. J Morph 83:225–251.Google Scholar

Nelson, EM. 1949. The swim bladder and Weberian apparatus of Rhaphiodon vulpinus Agassiz, with notes on some additional morphological features. J Morph 84:495–523.Google Scholar

Patterson, C. 1984. Chanoides, a marine Eocene otophysan fish (Teleostei: Ostariophysi). J Vert Paleo 4:430–456.Google Scholar

Peterson, T, Müller, GB. 2016. Phenotypic novelty in EvoDevo: The distinction between continuous and discontinuous variation and its importance in evolutionary theory. Evol Biol 43:314–335.Google Scholar

Porcu, E, Medici, M, Pistis, G, Volpato, CB, Wilson, SG, et al. 2013. A meta-analysis of thyroid-related traits reveals novel loci and gender-specific differences in the regulation of thyroid function. PLoS Genet 9:e1003266.Google Scholar

Raff, RA, Kaufman, TC. 1983. Embryos, Genes, and Evolution: The Developmental-Genetic Basis of Evolutionary Change. New York: Macmillan.Google Scholar

Ramaswami, LS. 1955. Skeleton of Cyprinoid fishes in relation to phylogenetic studies. VII. The skull and Weberian apparatus of Cyprininae (Cyprinidae). Acta Zool 36:199–242.Google Scholar

Rastorguev, SM, Nedoluzhko, AV, Levina, MA, Prokhorchuk, EB, Skryabin, KG, Levin, BA. 2016. Pleiotropic effect of thyroid hormones on gene expression in fish as exemplified from the blue bream Ballerus ballerus (Cyprinidae): Results of transcriptomic analysis. Dokl Biochem Biophys 467:124–127.Google Scholar

Rosen, DE, Greenwood, PH. 1970. Origin of the Weberian apparatus and the relationships of the ostariophysan and gonorynchiform fishes. Am Mus Novit 2428:1–25.Google Scholar

Sabet, A, Yen, PM. 2009. Thyroid hormone action. In: Wondisford, FE, Radovick, S, editors. Clinical Management of Thyroid Disease. Elsevier Inc. pp. 43–56.Google Scholar

Saha, S, Ghosh, P, Mitra, D, Mukherjee, S, Bhattacharya, S, Roy, SS. 2007. Localization and thyroid hormone influenced expression of collagen II in ovarian tissue. Cell Physio Biochem 19:67–76.Google Scholar

Schmalhausen, II. 1938. Organizm kak tseloe v individual’nom i istoricheskom razvitii (Organism as a whole in individual and historical development). Moscow-Leningrad: Akad. Nauk SSSR.Google Scholar

Shkil, FN, Kapitanova, DV, Borisov, VB, Abdissa, B, Smirnov, SV. 2012. Thyroid hormone in skeletal development of cyprinids: Effects and morphological consequences. J Appl Ichthyol 28:398–405.Google Scholar

Sinha, R, Yen, PM. 2014. Cellular action of thyroid hormone. In: De Groot, LJ, Chrousos, G, Dungan, K, Feingold, KR, Grossman, A, et al., editors. Endotext [Internet]. South Dartmouth, Maryland: MDText.com, Inc.Google Scholar

Viguerie, N, Langin, D. 2003. Effect of thyroid hormone on gene expression. Curr Opin Clin Nutr Metab Care 6:377–381.Google Scholar

Walker, MB, Kimmel, CB. 2007. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 82:23–28.Google Scholar

Wang, L, Shao, Y, Ballock, T. 2007. Thyroid hormone interacts with the Wnt/β-catenin signaling pathway in the terminal differentiation of growth plate chondrocytes. J Bone Miner Res 22:1988–1995.Google Scholar

Watson, JM. 1939. The development of the Weberian ossicles and anterior vertebrae in the goldfish. Proc R Soc Lond B Biol Sci 127:452–472.Google Scholar

West-Eberhard, MJ. 2003. Developmental Plasticity and Evolution. Oxford: Oxford University Press.CrossRef Google Scholar

Williams, GR. 2009. Actions of thyroid hormones in bone. Endokrynol Pol 60:380–388.Google Scholar

Xing, W, Cheng, S, Wergedal, J, Mohan, S. 2014. Epiphyseal chondrocyte secondary ossification centers require thyroid hormone activation of Indian hedgehog and osterix signaling. J Bone Miner Res 29:2262–2275.Google Scholar

The Zebrafish Model Organism Database. https://zfin.org. Accessed 11 February 2014.Google Scholar

Zhou, R, Bonneaud, N, Yuan, C-X, de Santa, Barbara P, Boizet, B, Tibor, S, Scherer, G, Roeder, RG, Poulat, F, Berta, P. 2002. SOX9 interacts with a component of the human thyroid hormone receptor-associated protein complex. Nucleic Acids Res 30:3245–3252.Google Scholar