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The Anatomy of the Thyroid Gland Among “Fishes”: Phylogenetic Implications for the Vertebrata

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The Anatomy of the Thyroid Gland Among “Fishes”: Phylogenetic Implications for the Vertebrata The anatomy of the thyroid gland among “fishes”: phylogenetic implications for the Vertebrata by Bruno CHANET* (1) & François Jean MEUNIER (2) Abstract. – A study on the structure of the thyroid gland of 288 vertebrate species, conducted both on 99 dissec- tions and analysis of the literature, leads to propose the following interpretations: i) the presence of this gland is a synapomorphy of Vertebrata; ii) a compact gland is a synapomorphy of Gnathostomes; iii) a diffuse gland is a possible synapomorphy of Halecostomes; iv) several independent cases of concentration in a few lobes in several groups, like Scaridae, Scombridae and some Carangimorphariae occurred and even a compact gland in Osteoglossomorphes. Moreover, the scattering of thyroidian islets in other organs (cephalic kidney, choroid,…) has occurred several times in teleost lineages and a compact thyroid gland embedded in a blood sinus appears to be a probable synapomorphy of Tetraodontiformes and Lophiiformes. © SFI Résumé. – L’anatomie de la glande thyroïde chez les “poissons” : implications phylogénétiques chez les verté- Received: 12 Feb. 2014 brés. Accepted: 10 Jun. 2014 Editor: J.Y. Sire Une étude de la structure de la thyroïde chez 288 espèces de vertébrés, menée à partir de 99 dissections et d’analyses de la littérature, permet de proposer les interprétations suivantes: i) la présence de cette glande est une synapomorphie des vertébrés ; ii) une glande compacte est une synapomorphie des gnathostomes ; iii) une thyroïde diffuse est une synapomorphie possible des halécostomes ; iv) il existe plusieurs cas indépendants de Key words concentration en quelques lobes chez les Scaridae, les Scombridae et certains Carangimorphariae, et même une thyroïde compacte chez les Osteoglossomorphes. Enfin, un éparpillement d’îlots thyroïdiens dans d’autres orga- Vertebrata nes (rein céphalique, choroïde,…) est apparu plusieurs fois chez les téléostéens et une thyroïde compacte incluse Chondrichthyes dans un sinus sanguin est une probable synapomorphie des Tetraodontiformes et des Lophiiformes. Actinopterygii Thyroid gland Anatomy Phylogeny The role of the thyroid gland in verte- thyroid structure only in some subgroups without taking into brate physiology has been, and is still, account the diversity of this clade. In a few words, the thy- the subject of many studies (e.g. Marine, 1913; Hoar, 1951; roid is often viewed as a diffuse gland in “lower” vertebrates Geven et al., 2007; Dufour et al., 2012). Its importance (i.e. “fishes”), while in “higher” vertebrates (mammals, birds for metabolism regulation, growth and metamorphosis has and relatives) this gland presents a compact structure (Por- been studied in details and for a long time (Olivereau, 1954; reca, 2010; Fagman and Nilsson, 2010). Nevertheless, the Fontaine and Fontaine, 1957, 1962; Olivereau et al., 1964; anatomic diversity cannot be considered on the basis of such Eales, 1979; Leatherland, 1982, 1988; Dufour et al., 2012, simple shortcuts and the diversity of the thyroid gland anat- among many others). Moreover, the thyroidian follicles omy has to be examined in more details before suggesting can accumulate numerous environmental chemicals (such possible hypotheses regarding the evolution of this organ. as hydrocarbons, organochlorine and organophosphorous The thyroid gland was first identified in vertebrates by pesticides, cyanide compounds, methyl bromide, phenols, the English physician Thomas Wharton in 1656 (Kunz, ammonia, metals, sex steroids, and many pharmaceutical 2004) and in “fishes” by Simon (1844), even if he confused products) (Brown et al., 2004a). Consequently, studying the this organ with the pseudobranch in several species (Todd, composition of these organs can reveal to which environ- 1849-1852; Owen, 1866; Gudernatsch, 1910). More than mental pollutants an animal has been exposed (Brown et al., twenty years before, Retzius (1819) has described a sublin- 2004a). In that perspective, localizing these follicles is the gual gland in a skate: Raja fullonica [= Leucoraja fullonica first and fundamental step of both physiological and toxico- (L., 1758)] (Retzius, 1819: 54, fig. 7). An examination of this logical investigations. However, surprisingly the anatomical figure leads us to conclude, like Todd (1849-1852) and Owen structure of this endocrine gland has not really been reported (1866), that this sublingual gland is a compact thyroid. Nev- among vertebrates and the question of its evolution within ertheless, these two authors considered that the gland was a this group has been poorly studied. A few studies related the more or less compact structure in vertebrates; Owen (1866) (1) ISYEB, UMR 7205 CNRS-MNHN-UPMC-EPHE, Muséum national d’Histoire naturelle, Département Systématique et Évolution, CP 50, 57 rue Cuvier 75005 Paris, France. (2) UMR 7208 (CNRS-IRD-MNHN-UPMC), ‘BOREA’, Département des Milieux et Peuplements aquatiques, Muséum national d’Histoire naturelle, CP 026, 43 rue Cuvier, 75231 Paris CEDEX 05, France. [[email protected]] * Corresponding author [[email protected]] Cybium 2014, 38(2): 89-116. Thyroid gland of “fishes” CHANET & MEUNIER studied the thyroid only in species where the gland forms a specimen. The used classification of “fishes” follows Nel- single and compact structure. son (2006) and Betancur-R et al. (2013b) for actinopterygian The diffuse structure of the thyroid gland in teleostean taxa. fishes was assessed later by Baber (1881), Maurer (1886) and The dissected specimens are: Gudernatsch (1910). Consequently, the structural diversity CHONDRICHTHYES, CARCHARHINIFOR M ES , Scyliorhinidae: of this gland within vertebrates was already pointed out at Scyliorhinus canicula (2) (mean SL: 81 cm), purchased at fishmon- the end of the 19th century. In some species, as skates, sharks, ger, fished off the East Atlantic Ocean coast).T ORPEDINIFOR M ES , frogs, crocodiles, birds and mammals, the gland is a com- Torpedinidae: Torpedo marmorata (1) (SL: 65 cm), purchased at pact, sometimes bilobed, encapsulated organ (Owen, 1866; fishmonger, fished off the East Atlantic Ocean coast). Baber, 1881), while in others, as teleosteans, the gland is OSTEICHTHYES, ACTINOPTERYGII , Neopterygii, Lepisostei- diffuse, not encapsulated, with scattered islets of follicles in dae: Lepisosteus osseus (1), isolated head (HL: 23 cm, fished in the branchial region, close to the ventral aorta (Gudernatsch, the Chesapeake Bay, Virginia, USA). Teleostei, Elopomorphes, 1910; Baker, 1958). Some ectopic thyroidian follicles may Anguillidae: Anguilla anguilla (1) (SL: 73 cm, purchased at fish- be present as well in the cephalic kidney as in the choroid monger, fished off the East Atlantic Ocean coast), Congridae: Con- of some species (Chavin, 1956; Baker, 1958; Fournie et al., ger conger (1), isolated head (HL: 21 cm, purchased at fishmonger, 2005). Schlumberger and Lucke (1948) and Fournie et al. fished off the East Atlantic Ocean coast), Megalopidae: Mega- (2005) noticed that these highly scattered follicles have been lops atlanticus (1), isolated head (HL: 22 cm, from the Aquarium often mistaken with invading neoplastic, tumorous structures Mare Nostrum, Montpellier, France). Osteoglossomorpha, Notop- [see Schlumberger and Lucke, 1948; Hoover, 1984; Fournie teridae: Chitala chitala (1) (SL: 57 cm, from the Aquarium de la et al., 2005) for reports of thyroidian pathologies (tumours Porte Dorée, Paris, France), Osteoglossidae: Osteoglossum bic- and goitres) in “fishes”]. Some cases of compact thyroid cirhosum (1) (SL: 75 cm) (from the Aquarium de la Porte Dorée, were described in several acanthomorphs, like scarids (Mat- Paris, France). Ostariophysii, Cypriniformes, Cyprinidae: Abramis thews and Smith, 1948), and in dipnoans (Parker, 1890; Oliv- brama (1) (SL: 25.8 cm, purchased at fishmonger, France),Cypri - ereau, 1959; Chavin, 1976) and in the Comorian coelacanth nus carpio (1) (SL: 42.3 cm, purchased at fishmonger, France). (Chavin, 1972, 1976). A peculiar thyroid gland, embedded in Salmoniformes, Salmonidae: Salvelinus alpinus (2) (SL: 34 cm, a blood sinus, was studied in the angler, Lophius piscatorius purchased at fishmonger, France), Salmo trutta (2) (SL: 25.8 cm Linnaeus, 1758 (Lophiidae) (Burne, 1927). This short sur- and 26.2 cm, purchased at fishmonger, France). Acanthomorphes, vey shows that the thyroid gland presents a diversity of ana- Lampriformes, Lampridae: Lampris immaculatus (1) (SL: 60 cm, tomical patterns within “fishes” and that the simple scheme fished in the Kerguelen Islands, Indian Ocean). Gadiformes, Gadi- assessing that this gland is diffuse in “lower” vertebrates dae: Gaidropsarus mediterraneus (1) (SL: 9.5 cm, fished in the and compact in “higher” vertebrates cannot be considered as English Channel), Pollachius pollachius (1), isolated head (HL: valid. The purpose of the present study is to question that 19 cm, purchased at fishmonger, fished off the East Atlantic Ocean item in studying the structure of the thyroid gland among coast), Trisopterus luscus (1) (SL: 23.2 cm, purchased at fishmon- vertebrates, with a special focus on “fishes” that represent ger, fished in the Atlantic Ocean). Zeiformes, Zeidae:Zeus faber (1) more than 50% of the vertebrate taxa, and to map the identi- (SL: 30.5 cm, purchased at fishmonger, fished off the East Atlantic fied states on recent phylogenies to try to decipher the evolu- Ocean coast). Syngnathiformes, Callionymidae: Callionymus lyra tion of the gland and proposing possible synapomorphies for (2) (11.7 cm and 13.2 cm, purchased at fishmonger,
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