Morphological and Molecular Evidence for a Stepwise Evolutionary Transition from Teeth to Baleen in Mysticete Whales

Abstract

The origin of baleen in mysticete whales represents a major transition in the phylogenetic history of Cetacea. This key specialization, a keratinous sieve that enables filter-feeding, permitted exploitation of a new ecological niche and heralded the evolution of modern baleen-bearing whales, the largest animals on Earth. To date, all formally described mysticete fossils conform to two types: toothed species from Oligocene-age rocks ( approximately 24 to 34 million years old) and toothless species that presumably utilized baleen to feed (Recent to approximately 30 million years old). Here, we show that several Oligocene toothed mysticetes have nutrient foramina and associated sulci on the lateral portions of their palates, homologous structures in extant mysticetes house vessels that nourish baleen. The simultaneous occurrence of teeth and nutrient foramina implies that both teeth and baleen were present in these early mysticetes. Phylogenetic analyses of a supermatrix that includes extinct taxa and new data for 11 nuclear genes consistently resolve relationships at the base of Mysticeti. The combined data set of 27,340 characters supports a stepwise transition from a toothed ancestor, to a mosaic intermediate with both teeth and baleen, to modern baleen whales that lack an adult dentition but retain developmental and genetic evidence of their ancestral toothed heritage. Comparative sequence data for ENAM (enamelin) and AMBN (ameloblastin) indicate that enamel-specific loci are present in Mysticeti but have degraded to pseudogenes in this group. The dramatic transformation in mysticete feeding anatomy documents an apparently rare, stepwise mode of evolution in which a composite phenotype bridged the gap between primitive and derived morphologies; a combination of fossil and molecular evidence provides a multifaceted record of this macroevolutionary pattern.

Discovery of a sensory organ that coordinates lunge feeding in rorqual whales

“…The condition of the mandibular symphysis in grey whales (Eschrichtius robustus) has only been reported for a decayed neonatal specimen 29 , although the suggestion of a mucoid centre is broadly similar with the morphology of the organ described here. On the basis of this equivocal evidence, we propose that the organ evolved either at the node of Balaenopteroidea (grey whales and rorquals), or along the stem to crown Balaenopteridae (rorquals) 15 . If the former, the organ is a pre-adaptation for lunge feeding; if the latter, the organ evolved in tandem with VGB and specializations of the mandible morphology, such as a laterally deflected coronoid process 6 and flexible temporomandibular joints 5 , which exhibit a degree of mandible rotation and oropharyngeal cavity expansion far greater than that of grey whales 29 .…”

“…3). Our analyses showed that the organ receives neurovascular bundles that emerge from vestigial alveolar foramina of the mandibles, a structure that is homologous with the lower first incisor tooth socket of fossil 'toothed' mysticetes [14][15][16] . The presence and identity of these neurovascular bundles, which contain branches of the mandibular division of the trigeminal nerve, were confirmed by subsequent dissection of the same specimen.…”

“…Their feeding specializations thus reflect a trade-off between evolutionary innovations (for example, baleen) and fundamental constraints from a mammalian body plan (such as air breathing) 3 . The origin of suspension feeding in mysticetes represents an evolutionary novelty with no parallel in any other mammalian or known synapsid lineage 15 . Moreover, the innovation of baleen preceded the origin of extremely large body sizes in mysticetes 16 , which rank among the largest vertebrates ever.…”

Pseudogenization of the tooth gene enamelysin (MMP20) in the common ancestor of extant baleen whales

“…Cetaceans in the suborder Mysticeti, by contrast, have lost their adult teeth and instead use racks of baleen to filter zooplankton and small fish from ocean waters. Baleen is a key innovation that facilitated the exploitation of an unexploited ecological niche, bulk filter-feeding and laid the foundation for the evolution of the largest animals on the Earth [2]. In addition to including the largest extant mammal (blue whale), Mysticeti also includes the putatively longest living extant mammal (bowhead whale) [3][4][5].…”

Late Pleistocene gray whales (Eschrichtius robustus) offshore Georgia, U.S.A., and the antiquity of gray whale migration in the North Atlantic Ocean

“…5B). Lastly, as Garrison et al (2012) noted, GMNH 27372 lacks a patent, J-shaped mylohyoid sulcus on ventrolingual surface of mandible, which is a diagnostic feature in all Balaenidae (Bisconti, 2008;Deméré et al, 2008), and GMNH 27375 lacks these features as well. Because extant Eschrichtius is monotypic, there is no a priori reason to exclude the assignment of this material to the extant species, Eschrichtius robustus.…”