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Atavisms and the Homology of Hyobranchial Elements in Lower Vertebrates

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Atavisms and the Homology of Hyobranchial Elements in Lower Vertebrates JOURNAL OF MORPHOLOGY 195237-245 (1988) Atavisms and the Homology of Hyobranchial Elements in Lower Vertebrates STEPHEN M. REILLY AND GEORGE V.LAUDER Department of Developmental and Cell Biology, University of California, Iruine, CA 92717 ABSTRACT The homology of branchial arch segments in salamanders has been a matter of controversy since the last century. Many investigators term the most medial paired elements of salamander branchial arches "ceratobran- chials" and the next distal paired elements "epibranchials." This suggests that the first two segmental elements of the salamander branchial arch are not homologous with elements occupying the same position in ray-finned fishes, Latimeria, "rhipidistians," and lungfishes, in which these bones are called hypobranchials and ceratobranchials, respectively. Three lines of evi- dence suggest that it is more parsimonious to interpret urodele branchial arch segments as being homologous with those of other vertebrate clades-1) com- parative osteology, 2) comparative myology, and 3) the discovery of cartilagi- nous structures forming a third segmental unit that we interpret as atavistic epibranchials of the branchial arch in one population of the salamander Note phthalmus uiridescens. These structures possess all the defining attributes of atavisms, and illustrate the special role that atavistic features play in resolv- ing questions of homology recognition. For more than a century, detailed descrip- structures of the hyobranchial apparatus are tions of hyobranchial morphology in lower called basibranchials because they lie at the vertebrates have appeared in the scientific base of the branchial basket. The segmental literature (Gegenbaur, 1865; Parker, 1877; component of each left and right branchial Wiedersheim, 1877). As traditionally de- arch that articulates with the basibranchial scribed, the hyobranchial apparatus of ver- is called the hypobranchial (Fig. 1). Distal to tebrates contains postmandibular visceral the hypobranchial is the ceratobranchial, arches consisting of the hyoid arch (visceral which articulates distally with the segmen- arch 2) and the branchial arches posterior to tal component called the epibranchial. Fi- the hyoid arch, usually five in number in nally, the anterodorsally oriented elements fishes. The hyoid and branchial visceral of the branchial basket are called pharyngo- arches are involved, at least primitively, in branchials (Fig. 1). Anatomically, the hypo- cranial functions such as feeding and branchials and ceratobranchials are ventral respiration. elements of the branchial basket, whereas The paired visceral arches are segmented epibranchials and pharyngobranchials are and meet midventrally to articulate with one dorsal elements. or more median elements. In the generalized This terminology for the branchial arch vertebrate configuration, the branchial arch segments has been used widely by morphol- on each side of the head is composed of five ogists, except in the literature dealing with basic elements, each of which originates de- salamander morphology and evolution. Here, velopmentally as a cartilaginous structure elements that would be called hypobranchi- that may ossify later (Nelson, '69; Jollie, '73, als in fishes often are referred to as cerato- '86). The nomenclature of these five bran- branchials and the next distal elements are chial arch elements has been widely accepted called epibranchials (e.g., Alberch et al., '85; (see Nelson, '69 for a review), and is de- Dock and DeVree, '86; Erdman and Cun- scribed (at least generally) in all textbooks of dall, '84; Krogh and Tanner, '72; Larsen and comparative anatomy (e.g., Jollie, '73; Romer Guthrie, '75; Lombard and Wake, '76, '77; and Parsons, '77; Walker, '87). The midline Ozeti and Wake, '69; Regal, '66; Wake, '82). 0 1988 ALAN R. LISS, INC. 238 S.M. REILLY AND G.V. LAUDER in vertebrates. Here, we attempt to resolve c ANTERIOR the question of branchial-arch segmental ho- mology in salamanders (Caudata) by present- ing three lines of evidence. First, the morphology of hyobranchial skeletal ele- PB ments in fishes and salamanders is com- pared. Second, muscles associated with these hyobranchial elements are compared and discussed in relation to the positional infor- mation that they provide on the homology of their insertions. Finally, we present new data on the occurrence of distal branchial arch elements in a population of newts. We inter- pret these elements as atavisms and as evi- Fig, 1. Lateral view of the left first gill arch of Polyp dence that the true epibranchials have been terus senegalua The gill arch consists of a segmented series of endochondral ossifications in the following or- lost in salamanders. der (ventral to dorsal): Hypobranchial (HB), ceratobran- We contend that the most parsimonious chial (CB), epibranchial (EB), and pharyngobranchial interpretation of the comparative morpholog- (PB). Note the position of both the cartilaginous and ical data, together with the novel informa- bony portions of the epibranchial in relation to the tip of is the ceratobranchial, and its similarity to the location of tion on atavistic branchial arch segments, the additional segmental elements (which we term epi- that the most medial two paired structural branchials) in Figure 3. Bony tissue is white, cartilage elements of salamander branchial arches are is stippled. Scale = 0.5 cm. hypobranchials and ceratobranchials. MATERIALS AND METHODS Use of this nomenclature assumes that the Specimens hypobranchial of all other lower vertebrates Branchial morphology was examined in 65 either is lost or fused with the ceratobran- branchiate adult Notophthalmus uiridescens, chial, and that the epibranchials, which fre- collected from McGuire’s Pond, 9.7 km south quently are lost in vertebrates, are retained of Carbondale, Jackson Co., Illinois. All spec- in salamanders. The first authors to use the imens were killed in chlorotone and fixed in terms ceratobranchials and epibranchials in 10% formalin. This population was used in salamanders (Huxley, 1874; Parker, 1877; two previous morphological analyses of Wiedersheim, 1877) stressed the importance metamorphosis in salamanders (Reilly, ’86, of ascertaining the homology of structures ’87). Sex, snout-vent length, and condition of among lower vertebrates, yet did not discuss external gills were recorded before the speci- their choice of the term ceratobranchial for mens were cleared and double-stained for the most medial branchial element of each bone and cartilage following the procedure of arch in caudates, when it is termed the hy- Dingerkus and Uhler (’77). Metamorphic pobranchial in all other lower vertebrates. condition of the skull and hyobranchial ap- Also, they did not offer any explanation of paratus were examined and photographed the fate of the hypobranchial. using a Zeiss SV-8 binocular dissecting mi- Marche and Durand (’83)discussed the dis- croscope. Voucher specimens are deposited in cordance of branchial arch terminology the Museum of Natural History, The Univer- within salamanders and marshaled evidence sity of Kansas (KU 203963-203987, KU to support their view that salamanders have 206794-206833). true hypobranchials and ceratobranchials. Duellman and Trueb (’86) briefly reviewed Comparative analyses this controversy, noting that although they Branchial arch morphology in several adopted the term “ceratobranchial” in lieu lower vertebrate clades was examined to pro- of the often used “epibranchial” for caudates, vide a basis for positional analyses of seg- there were no data in the literature that mental homology. Relevant clades for permitted a resolution of the homology of comparison were chosen on the basis of cur- these gill arch segments. rent phylogenetic hypotheses relating tetra- The terminological confusion present in the pods, lungfishes, coelacanths, ray-finned literature reflects differing views on the ho- fishes, and chondrichthyans (Lauder and mology of the segmental gill arch elements Liem, ’83; Maisey, ’86). ATAVISMS AND HYOBRANCHIAL HOMOLOGY 239 A C Fig. 2. Morphology of the hyobranchial apparatus in ure and Figure 3: BB, basibranchial; CB 1-5, Cerato- three lower vertebrates: A Polypterus senegalus, a ray- branchials 1to 5; CH, ceratohyal; EB1, Epibranchial 1; finned fish (Actinopterygii); B: Eusthenopteron fordii HB 1-2, Hypobranchials 1 and 2 (solid black); HH, Hy- (after Jarvik, 'BO), a "rhipidistian;" C: Ambystoma ti- pohyal; W,transversus ventralis muscle. grinum (larval morphology). Abbreviations for this fig- Information on hyobranchial osteology and ogy (Figs. 1, 2). In chondrichthyans, the hyo- myology in lower vertebrates is derived from branchial apparatus consists of median both descriptive and comparative studies of basibranchial elements which articulate with fishes and amphibians in the literature (e.g., four or five hypobranchials, each of which in Allis, '17, '22; Druner, '02, '04;Eaton, '36; turn, articulates with the ceratobranchials, Edgeworth, '35; Jarvik,. '80; Jollie, '82; Lom- epibranchials, and pharyngobranchials in se- bard and Wake, '76; Ozeti and Wake, '69; ries. This arrangement forms a complete Piatt, '39, '40;Rosen et al., '81; Wiedersheim, branchial basket posterior to the skull (Ed- 1877; Wiley, '79a,b; Winterbottom, '74), as geworth, '35; Jollie, '73). well as from our own previous studies of In primitive actinopterygians (e.g., Polyp branchial arch morphology and function in terus, Figs. 1, 2A), the same general pattern lower vertebrates (Lauder, '80; '83; Lauder of elements
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