Breaking the mold: telescoping drives the evolution of more integrated and heterogeneous skulls in cetaceans

BUONO, MÓNICA R.; VLACHOS, EVANGELOS

PeerJ

PeerJ

Lugar: Londres; Año: 2022 vol. 10

2167-8359

Background. Along with the transition to the aquatic environment, cetaceans experienced profound changes in their skeletal anatomy, especially in the skull, including theposterodorsal migration of the external bony nares, the reorganization of skull bones (=telescoping) and the development of an extreme cranial asymmetry (in odontocetes).Telescoping represents an important anatomical shift in the topological organizationof cranial bones and their sutural contacts; however, the impact of these changes in theconnectivity pattern and integration of the skull has never been addressed.Methods. Here, we apply the novel framework provided by the Anatomical NetworkAnalysis to quantify the organization and integration of cetacean skulls, and the impactof the telescoping process in the connectivity pattern of the skull. We built anatomicalnetworks for 21 cetacean skulls (three stem cetaceans, three extinct and 10 extantmysticetes, and three extinct and two extant odontocetes) and estimated networkparameters related to their anatomical integration, complexity, heterogeneity, andmodularity. This dataset was analyzed in the context of a broader tetrapod skull sampleas well (43 species of 13 taxonomic groups).Results. The skulls of crown cetaceans (Neoceti) occupy a new tetrapod skull morphospace, with better integrated, more heterogeneous and simpler skulls in comparisonto other tetrapods. Telescoping adds connections and improves the integration of thosebones involved in the telescoping process (e.g., maxilla, supraoccipital) as well as otherones (e.g., vomer) not directly affected by telescoping. Other underlying evolutionaryprocesses (such as basicranial specializations linked with hearing/breathing adaptations) could also be responsible for the changes in the connectivity and integration ofpalatal bones. We also find prograde telescoped skulls of mysticetes distinct from odontocetes by an increased heterogeneity and modularity, whereas retrograde telescopedskulls of odontocetes are characterized by higher complexity. In mysticetes, as expected,the supraoccipital gains importance and centrality in comparison to odontocetes,increasing the heterogeneity of the skull network. In odontocetes, an increase inthe number of connections and complexity is probably linked with the dominantmovement of paired bones, such as the maxilla, in retrograde telescoping. Crownmysticetes (Eubalaena, Caperea, Piscobalaena, and Balaenoptera)are distinguishedby having more integrated skulls in comparison to stem mysticetes (Aetiocetus andYamatocetus), whereas crown odontocetes (Waipatia, Notocetus, Physeter, and Tursiops)have more complex skulls than stem forms (Albertocetus). Telescoping along with feeding, hearing and echolocation specializations could have driven the evolution ofthe different connectivity patterns of living lineages.