Evolutionary aspects of the development of teeth and baleen in the bowhead whale

Abstract

In utero, baleen whales initiate the development of several dozens of teeth in upper and lower jaws. These tooth germs reach the bell stage and are sometimes mineralized, but toward the end of prenatal life they are resorbed and no trace remains after birth. Around the time that the germs disappear, the keratinous baleen plates start to form in the upper jaw, and these form the food-collecting mechanism. Baleen whale ancestors had two generations of teeth and never developed baleen, and the prenatal teeth of modern fetuses are usually interpreted as an evolutionary leftover. We investigated the development of teeth and baleen in bowhead whale fetuses using histological and immunohistochemical evidence. We found that upper and lower dentition initially follow similar developmental pathways. As development proceeds, upper and lower tooth germs diverge developmentally. Lower tooth germs differ along the length of the jaw, reminiscent of a heterodont dentition of cetacean ancestors, and lingual processes of the dental lamina represent initiation of tooth bud formation of replacement teeth. Upper tooth germs remain homodont and there is no evidence of a secondary dentition. After these germs disappear, the oral epithelium thickens to form the baleen plates, and the protein FGF-4 displays a signaling pattern reminiscent of baleen plates. In laboratory mammals, FGF-4 is not involved in the formation of hair or palatal rugae, but it is involved in tooth development. This leads us to propose that the signaling cascade that forms teeth in most mammals has been exapted to be involved in baleen plate ontogeny in mysticetes.

Decoupling Tooth Loss from the Evolution of Baleen in Whales

“…While molecular data have recently illuminated enamel and tooth loss in extant mammals, including cetaceans (Meredith et al, 2009(Meredith et al, , 2011, the underpinnings of baleen development and its morphogenesis are unknown. A recent study on bowhead whale (Balaena mysticetus) ontogeny provided the first strong evidence that baleen morphogenesis recruits developmental patterning from tooth bud signaling (Thewissen et al, 2017). Pending studies that more broadly sample these traits across mysticete phylogeny, we argue that patterns of dental evolution and loss in cetaceans should not be a priori linked, neither in step-wise nor correlative models.…”

“…Van Dissel-Scherft and Vervoort (1954a,b) instead argued that both Eschricht (1849) and Julin (1880) correctly interpreted the dentition of living mysticetes as heterodont. Notably, the recent work by Thewissen et al (2017) suggests that this condition may not be consistent between the upper and lower dentition. Thewissen et al (2017) indicate that, at least in bowhead whales, the upper dentition is homodont while the lower is heterodont.…”

“…More crucially, most studies center on the genetics of tooth loss in cetaceans; the genetic underpinnings of baleen morphogenesis has only recently become a topic of study (Thewissen et al, 2017).…”

“…This pattern implies that C4orf26, unlike the other genes mentioned above, is tooth-specific but not enamel-specific; moreover, it reinforces a decoupling between the processes responsible for tooth and enamel production. Recently, Thewissen et al (2017) provided the first study to shed light on the genetic underpinnings of baleen morphogenesis. This study examined the development of teeth and baleen in bowhead whales and demonstrated that the fibroglast growth factor family (specifically FGF4) is critical in the development of baleen.…”

“…FGF4 is a protein typically associated with the development of teeth, not with those of hair or palatal rugae. Thewissen et al (2017) thus suggested that the genetic underpinnings of baleen morphogenesis may be more closely tied to those of tooth development than morphological studies may suggest. In sum, the evolution of tooth loss is a more complex process than indicated by morphological observations alone and it remains unclear how it relates to the origin of baleen.…”