Atavisms and the Homology of Hyobranchial Elements in Lower Vertebrates

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 "ceratobranchials" 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 evidence suggest that it is more parsimonious to interpret urodele branchial arch segments as being homologous with those of other vertebrate clades-1) comparative osteology, 2) comparative myology, and 3) the discovery of cartilaginous 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 resolving questions of homology recognition. For more than a century, detailed descriptions of hyobranchial morphology in lower vertebrates have appeared in the scientific literature (Gegenbaur, 1865; Parker, 1877; Wiedersheim, 1877). As traditionally described, the hyobranchial apparatus of vertebrates contains postmandibular visceral arches consisting of the hyoid arch (visceral arch 2) and the branchial arches posterior to the hyoid arch, usually five in number in fishes. The hyoid and branchial visceral arches are involved, at least primitively, in cranial functions such as feeding and respiration. The paired visceral arches are segmented and meet midventrally to articulate with one or more median elements. In the generalized vertebrate configuration, the branchial arch on each side of the head is composed of five basic elements, each of which originates developmentally as a cartilaginous structure that may ossify later (Nelson, '69; Jollie, '73, '86). The nomenclature of these five branchial arch elements has been widely accepted (see Nelson, '69 for a review), and is described (at least generally) in all textbooks of comparative anatomy (e.g., Jollie, '73; Romer and Parsons, '77; Walker, '87). The midline structures of the hyobranchial apparatus are called basibranchials because they lie at the base of the branchial basket. The segmental component of each left and right branchial arch that articulates with the basibranchial is called the hypobranchial (Fig. 1). Distal to the hypobranchial is the ceratobranchial, which articulates distally with the segmental component called the epibranchial. Finally, the anterodorsally oriented elements of the branchial basket are called pharyngobranchials (Fig. 1). Anatomically, the hypobranchials and ceratobranchials are ventral elements of the branchial basket, whereas epibranchials and pharyngobranchials are dorsal elements. This terminology for the branchial arch segments has been used widely by morphologists, except in the literature dealing with salamander morphology and evolution. Here, elements that would be called hypobranchials in fishes often are referred to as ceratobranchials and the next distal elements are called epibranchials (e.g., Alberch et al., '85; Dock and DeVree, '86; Erdman and Cundall, '84; Krogh and Tanner, '72; Larsen and Guthrie, '75; Lombard and Wake, '76, '77; Ozeti and Wake, '69; Regal, '66; Wake, '82).