Anatomical, Ontogenetic, and Genomic Homologies Guide Reconstructions of the Teeth-to-Baleen Transition in Mysticete Whales

Abstract

The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a 'transitional chimaeric feeder' scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of 'dental genes' related to enamel formation before the emergence of crown Mysticeti, while 'baleen genes' that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

“…The uncertainty over the evolutionary relationships of this group is probably due to convergent evolution of similar filter feeding modes displayed in specimens found in different parts of the world, as well as to the unique mixture of traits they presented (Berta et al, 2016). For example, some of them had short baleen plates that closely resemble the morphology of Caperea (Marx et al, 2017), which has been proposed to be included as the last living representative of the group (Fordyce & Marx, 2013), although this is still debated (Berta et al, 2016; Gatesy et al, 2022), but lacked some morphological features seen in the modern species. Similar fossils from the same locality have been found with fish fossilized in their stomach, hinting that they had a diet more similar to modern rorquals in contrast with the copepod‐specialist pygmy right whales (Collareta et al, 2015).…”

From teeth to pad: tooth loss and development of keratinous structures in sirenians

“…A close relationship between tooth development and the evolution of keratinized innovations of the feeding apparatus was proposed in several toothless mammals [1,14,15,61]. In cetaceans, several studies [62,63] proposed that the neurovascular anatomy of the upper teeth was co-opted for nourishing baleen. Lanzetti [14] showed that baleen rudiments develop alongside tooth germs within the alveolar canals of minke whales.…”

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

“…The uncertainty over the evolutionary relationships of this group is probably due to convergent evolution of similar filter feeding modes displayed in specimens found in different parts of the world, as well as to the unique mixture of traits they presented (Bisconti, 2015; Gol’din et al, 2015; Berta et al, 2016). For example, some of them had short baleen plates that closely resemble the morphology of Caperea (Marx et al, 2017), which has been proposed to be included as the last living representative of the group (Fordyce and Marx, 2013; Marx et al, 2019), although this is still debated (Berta et al, 2016; Gatesy et al, 2022), but lacked some morphological features seen in the modern species.…”