Development and evolution of the unique cetacean dentition

Abstract

The evolutionary success of mammals is rooted in their high metabolic rate. A high metabolic rate is sustainable thanks to efficient food processing and that in turn is facilitated by precise occlusion of the teeth and the acquisition of rhythmic mastication. These major evolutionary innovations characterize most members of the Class Mammalia. Cetaceans are one of the few groups of mammals in which precise occlusion has been secondarily lost. Most toothed whales have an increased number of simple crowned teeth that are similar along the tooth row. Evolution toward these specializations began immediately after the time cetaceans transitioned from terrestrial-to-marine environments. The fossil record documents the critical aspects of occlusal evolution of cetaceans, and allows us to pinpoint the evolutionary timing of the macroevolutionary events leading to their unusual dental morphology among mammals. The developmental controls of tooth differentiation and tooth number have been studied in a few mammalian clades, but nothing is known about how these controls differ between cetaceans and mammals that retain functional occlusion. Here we show that pigs, a cetacean relative with regionalized tooth morphology and complex tooth crowns, retain the typical mammalian gene expression patterns that control early tooth differentiation, expressing Bmp4 in the rostral (mesial, anterior) domain of the jaw, and Fgf8 caudally (distal, posterior). By contrast, dolphins have lost these regional differences in dental morphology and the Bmp4 domain is extended into the caudal region of the developing jaw. We hypothesize that the functional constraints underlying mammalian occlusion have been released in cetaceans, facilitating changes in the genetic control of early dental development. Such major developmental changes drive morphological evolution and are correlated with major shifts in diet and food processing during cetacean evolution.

Analysis of the FGF gene family provides insights into aquatic adaptation in cetaceans

“…FGF3 is known to play important roles in the formation of the ears and teeth in humans and mice1543. Cetaceans have undergone major changes in the ear and tooth including loss of the external ears, development of mandibular fat body, isolation of the tympanoperiotic complex from the skull, and loss of occlusion of the teeth744. Thus, the positive selection on FGF3 is potentially associated with changes in these morphological traits34744.…”

Dental anomalies in pinnipeds (Carnivora: Otariidae and Phocidae): occurrence and evolutionary implications

“…Thus, the lack of integration and occlusion in the dentition of pinnipeds may relate to a higher degree of dental variation in this group if compared to most terrestrial carnivores in which the dentition is highly integrated (Jernvall 2000;Miller et al 2007;Salazar-Ciudad and Jernvall 2010;Boessenecker 2011) and might explain the cases of agenesis of the posteriormost teeth. Other marine mammals Zoomorphology such as cetaceans also experienced loss of tooth occlusion during their evolution, generating less constrained tooth developmental mechanisms and allowing for some experimentation in tooth pattern and number (Armfield et al 2013). The homodont and commonly polydont dentition of most extant cetaceans is a result of this relaxed selective pressure, although some species have secondarily reduced the number of teeth (Werth 2006).…”

The Divination of Dentitions in Evolution

“…The serried rows of frequently replaced escalating polyphyodont teeth in sharks is the foundation of the haplodont, homodont morphology of the most primitive teeth that have been modified over eons into the diphyodont heterodont dentitions of mammals. These evolutionary dental changes were undoubtedly driven by altering dietary demands exemplified by the reversion of terrestrial ancestral cetaceans with heterodont teeth requiring masticatory capabilities to the extant marine cetaceans (whales, seals, dolphins and porpoises) with predatory piscivorous homodont dentitions [2]. The genetic basis of the reduction of multiple rows of teeth to the twogeneration deciduous and permanent dentitions has been established [3,4].…”