Cetacean Skull Telescoping Brings Evolution of Cranial Sutures into Focus

Abstract

Many modifications to the mammalian bauplan associated with the obligate aquatic lives of cetaceans-fusiform bodies, flukes, flippers, and blowholes-are evident at a glance. But among the most strikingly unusual and divergent features of modern cetacean anatomy are the arrangements of their cranial bones: (1) bones that are situated at opposite ends of the skull in other mammals are positioned close together, their proximity resulting from (2) these bones extensively overlapping the bones that ordinarily would separate them. The term "telescoping" is commonly used to describe the odd anatomy of modern cetacean skulls, yet its usage and the particular skull features to which it refers vary widely. Placing the term in historical and biological context, this review offers an explicit definition of telescoping that includes the two criteria enumerated above. Defining telescoping in this way draws attention to many specific biological questions that are raised by the unusual anatomy of cetacean skulls; highlights the central role of sutures as the locus for changes in the sizes, shapes, mechanical properties, and connectivity of cranial bones; and emphasizes the importance of sutures in skull development and evolution. The unusual arrangements of cranial bones and sutures referred to as telescoping are not easily explained by what is known about cranial development in more conventional mammals. Discovering the evolutionary-developmental processes that produce the extensive overlap characteristic of cetacean telescoping will give insights into both cetacean evolution and the "rules" that more generally govern mammalian skull function, development, and evolution. Anat Rec, 302:1055-1073, 2019. © 2019 Wiley Periodicals, Inc.

Keywords: Cetacea; cranial sutures; evo-devo; skull; telescoping.

Fig. 1.

Telescoping as a metaphor for two aspects of cetacean skull morphology. (A) An old-fashioned collapsible telescope (spyglass). Collapsing the telescope decreases its length as the overlap of intervening elements increases. (B) A mammal skull that adheres to the conserved structure and pattern of articulation observed in most mammals (Canis familiaris, NCSM 17631). Arrows highlight the distances between the sutural boundaries delineating the maxilla, frontal, and interparietal + occipital. (C) A dolphin skull (Tursiops truncatus, NCSM 8293). Arrows show the shortened distance between the maxilla and occipital on the dorsal surface of the dolphin skull relative to (B). Only a small portion of the frontal is observed externally. (D) A disarticulated dolphin skull (modified from Kellogg, 1928a). With the maxilla and premaxilla removed, the full extent of the frontal is observed. Extensive overlap of the maxilla over the frontal nearly hides the frontal from external view, resulting in the shortened distance in (C). Maxilla (blue), premaxilla (blue), frontal (green), interparietal + occipital (orange; fused), nasal (yellow).

Fig. 2.

Examples of articular surfaces that underlie extensive bone overlap in a disarticulated fetal balaenopterid mysticete (LACM 84179). (A) Left frontal, lateral view. (B) Left parietal, lateral view. (C) Left frontal, dorsal view. (D) Left and right parietals, dorsal view. Articular surfaces that underlie extensive overlap are outlined, and the bone articulating with that surface is noted in parentheses. Skull diagrams in the upper right corners indicate the photographed bone with color. White arrows in (C and D) show the perspective from which the bones in dorsal view were photographed. (Note that most of the dorsal surface of the parietals underlies the occipitals and is not visible from a dorsal view of the skull, therefore the position of the parietals is shown with hashmarks in the dorsal-view diagram in D.)

Fig. 3.

CT scans show extensive bone overlap of an immature minke whale (Balaenoptera acutorostrata, a mysticete; USNM 571236) (left) and of a juvenile dolphin (T. truncatus, an odontocete; WAM 704) (right). (A, B) 3D surface reconstructions in dorsal view; red line indicates the plane of the parasagittal slice in C and D. (C, D) Parasagittal CT slices showing broad maxilla-frontal overlap. (E, F) Color-coded diagrams drawn from CT slices. Regions of extensive overlap are indicated with correspondingly colored horizontal lines.

Fig. 4.

(A–E) Illustrations of skull vertices in dorsal view for select taxa. Note the proximity of the maxillae and premaxillae to the supraoccipital (+interparietal) in the four cetacean species (B–E) compared to the outgroup (A) (Hippopotamus). (F–H) Schematics comparing dorsal views of the skulls of (F) a “typical” mammal with the telescoped skulls of (G) an archetypal odontocete and (H) archetypal mysticete. The topological relationships illustrated are characteristic of the odontocete and mysticete bauplans, but anatomical details such as the relative sizes and shapes of bones may vary by species. Regions of overlap described as telescoped are indicated with parallel diagonal lines in the color of the underlying bone. (A) Hippopotamus amphibius (AMNH 90230). (B) Tursiops truncatus (Odontoceti: Delphinidae) (based on/modified from Kellogg, 1928a). (C) Balaenoptera physalus (USNM 16039) (Mysticeti: Balaenopteridae) (modified from Miller, 1923). (D) Ziphius cavirostris (NCSM 12806) (Odontoceti: Ziphiidae). (E) Eubalaena glacialis (USNM 23077) (Mysticeti: Balaenidae) (modified from Miller, 1923). (F) A generalized “typical” mammalian skull. (G) A generalized odontocete bauplan, modeled after a delphinid. (No attempt has been made to represent the bilateral asymmetry characteristic of odontocete skulls.) (H) A generalized mysticete bauplan, modeled after a balaenopterid.

Fig. 5.

Phylogeny of taxa discussed in this article (based on Gatesy et al., 2013). The origins of crown cetaceans (Neoceti) (star), odontocetestyle telescoping (blue circle; O), and mysticete-style telescoping (orange circle; M) are indicated. Illustrations (also in Fig. 4) on the right show a representative skull vertex for extant families.