{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T16:37:37Z","timestamp":1792255057521,"version":"4.4.0"},"reference-count":56,"publisher":"PeerJ","license":[{"start":{"date-parts":[[2022,5,5]],"date-time":"2022-05-05T00:00:00Z","timestamp":1651708800000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Agencia Nacional de Promoci\u00f3n Agencia Nacional de Promoci\u00f3n de la Investigaci\u00f3n"},{"name":"el Desarrollo Tecnol\u00f3gico y la Innovaci\u00f3n","award":["PICT 2019-00327"],"award-info":[{"award-number":["PICT 2019-00327"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Along with the transition to the aquatic environment, cetaceans experienced profound changes in their skeletal anatomy, especially in the skull, including the posterodorsal 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 organization of cranial bones and their sutural contacts; however, the impact of these changes in the connectivity pattern and integration of the skull has never been addressed.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Here, we apply the novel framework provided by the Anatomical Network Analysis to quantify the organization and integration of cetacean skulls, and the impact of the telescoping process in the connectivity pattern of the skull. We built anatomical networks for 21 cetacean skulls (three stem cetaceans, three extinct and 10 extant mysticetes, and three extinct and two extant odontocetes) and estimated network parameters related to their anatomical integration, complexity, heterogeneity, and modularity. This dataset was analyzed in the context of a broader tetrapod skull sample as well (43 species of 13 taxonomic groups).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      The skulls of crown cetaceans (Neoceti) occupy a new tetrapod skull morphospace, with better integrated, more heterogeneous and simpler skulls in comparison to other tetrapods. Telescoping adds connections and improves the integration of those bones involved in the telescoping process (\n                      <jats:italic>e.g.,<\/jats:italic>\n                      maxilla, supraoccipital) as well as other ones (\n                      <jats:italic>e.g.,<\/jats:italic>\n                      vomer) not directly affected by telescoping. Other underlying evolutionary processes (such as basicranial specializations linked with hearing\/breathing adaptations) could also be responsible for the changes in the connectivity and integration of palatal bones. We also find prograde telescoped skulls of mysticetes distinct from odontocetes by an increased heterogeneity and modularity, whereas retrograde telescoped skulls 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 in the number of connections and complexity is probably linked with the dominant movement of paired bones, such as the maxilla, in retrograde telescoping. Crown mysticetes (\n                      <jats:italic>Eubalaena<\/jats:italic>\n                      ,\n                      <jats:italic>Caperea<\/jats:italic>\n                      ,\n                      <jats:italic>Piscobalaena<\/jats:italic>\n                      , and\n                      <jats:italic>Balaenoptera<\/jats:italic>\n                      )are distinguished by having more integrated skulls in comparison to stem mysticetes (\n                      <jats:italic>Aetiocetus<\/jats:italic>\n                      and\n                      <jats:italic>Yamatocetus<\/jats:italic>\n                      ), whereas crown odontocetes (\n                      <jats:italic>Waipatia<\/jats:italic>\n                      ,\n                      <jats:italic>Notocetus<\/jats:italic>\n                      ,\n                      <jats:italic>Physeter<\/jats:italic>\n                      , and\n                      <jats:italic>Tursiops<\/jats:italic>\n                      ) have more complex skulls than stem forms (\n                      <jats:italic>Albertocetus<\/jats:italic>\n                      ). Telescoping along with feeding, hearing and echolocation specializations could have driven the evolution of the different connectivity patterns of living lineages.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.7717\/peerj.13392","type":"journal-article","created":{"date-parts":[[2022,5,5]],"date-time":"2022-05-05T03:24:49Z","timestamp":1651721089000},"page":"e13392","source":"Crossref","is-referenced-by-count":8,"title":["Breaking the mold: telescoping drives the evolution of more integrated and heterogeneous skulls in cetaceans"],"prefix":"10.7717","volume":"10","author":[{"given":"M\u00f3nica R.","family":"Buono","sequence":"first","affiliation":[{"name":"Instituto Patag\u00f3nico de Geolog\u00eda y Paleontolog\u00eda, CCT CONICET-CENPAT, Puerto Madryn, Chubut,  Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Evangelos","family":"Vlachos","sequence":"additional","affiliation":[{"name":"CONICET and Museo Paleontol\u00f3gico Egidio Feruglio, Trelew, Chubut, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4443","published-online":{"date-parts":[[2022,5,5]]},"reference":[{"key":"10.7717\/peerj.13392\/ref-1","doi-asserted-by":"publisher","DOI":"10.13140\/2.1.1341.1520","article-title":"Gephi: an open source software for exploring and manipulating networks","author":"Bastian","year":"2009"},{"issue":"11","key":"10.7717\/peerj.13392\/ref-2","doi-asserted-by":"publisher","first-page":"2205","DOI":"10.1002\/ar.23034","article-title":"Review of the cetacean nose: form, function, and evolution","volume":"297","author":"Berta","year":"2014","journal-title":"The Anatomical Record"},{"issue":"11","key":"10.7717\/peerj.13392\/ref-3","doi-asserted-by":"publisher","first-page":"e0186476","DOI":"10.1371\/journal.pone.0186476","article-title":"New records of the dolphin Albertocetus meffordorum (Odontoceti: Xenorophidae) from the lower Oligocene of South Carolina: encephalization, sensory anatomy, postcranial morphology, and ontogeny of early odontocetes","volume":"12","author":"Boessenecker","year":"2017","journal-title":"PLOS ONE"},{"issue":"1","key":"10.7717\/peerj.13392\/ref-4","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1644\/1545-1542(2005)086<0139:PIOSSA>2.0.CO;2","article-title":"Phylogenetic implications of skull structure and feeding behavior in balaenopterids (Cetacea, Mysticeti)","volume":"86","author":"Bouetel","year":"2005","journal-title":"Journal of Mammalogy"},{"issue":"2","key":"10.7717\/peerj.13392\/ref-5","first-page":"319","article-title":"The anatomy and relationships of Piscobalaena nana (Cetacea, Mysticeti), a Cetotheriidae ss from the early Pliocene of Peru","volume":"28","author":"Bouetel","year":"2006","journal-title":"Geodiversitas"},{"issue":"5","key":"10.7717\/peerj.13392\/ref-6","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1111\/evo.13480","article-title":"Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti)","volume":"72","author":"Churchill","year":"2018","journal-title":"Evolution"},{"issue":"16","key":"10.7717\/peerj.13392\/ref-7","doi-asserted-by":"publisher","first-page":"2144","DOI":"10.1016\/j.cub.2016.06.004","article-title":"The origin of high-frequency hearing in whales","volume":"26","author":"Churchill","year":"2016","journal-title":"Current Biology"},{"issue":"1","key":"10.7717\/peerj.13392\/ref-8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12915-019-0728-3","article-title":"Wonky whales: the evolution of cranial asymmetry in cetaceans","volume":"18","author":"Coombs","year":"2020","journal-title":"BMC Biology"},{"issue":"3","key":"10.7717\/peerj.13392\/ref-9","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1002\/(SICI)1097-4687(199606)228:3<223::AID-JMOR1>3.0.CO;2-3","article-title":"Functional morphology and homology in the odontocete nasal complex: implications for sound generation","volume":"228","author":"Cranford","year":"1996","journal-title":"Journal of Morphology"},{"issue":"4","key":"10.7717\/peerj.13392\/ref-10","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1002\/ar.20652","article-title":"Anatomic geometry of sound transmission and reception in Cuvier\u2019s beaked whale (Ziphius cavirostris)","volume":"291","author":"Cranford","year":"2008","journal-title":"The Anatomical Record"},{"issue":"2","key":"10.7717\/peerj.13392\/ref-11","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1002\/jmor.20629","article-title":"Skull ontogeny and modularity in two species of Lagenorhynchus: morphological and ecological implications","volume":"278","author":"Del Castillo","year":"2017","journal-title":"Journal of Morphology"},{"issue":"2","key":"10.7717\/peerj.13392\/ref-12","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1111\/j.1096-3642.2008.00414.x","article-title":"Skull anatomy of the Oligocene toothed mysticete Aetioceus weltoni (Mammalia; 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