[en] The evolution of cetaceans (whales and dolphins) represents one of the most extreme adaptive transitions known, from terrestrial mammals to a highly specialized aquatic radiation that includes the largest animals alive today. Many anatomical shifts in this transition involve the feeding, respiratory, and sensory structures of the cranium, which we quantified with a high-density, three-dimensional geometric morphometric analysis of 201 living and extinct cetacean species spanning the entirety of their ∼50-million-year evolutionary history. Our analyses demonstrate that cetacean suborders occupy distinct areas of cranial morphospace, with extinct, transitional taxa bridging the gap between archaeocetes (stem whales) and modern mysticetes (baleen whales) and odontocetes (toothed whales). This diversity was obtained through three key periods of rapid evolution: first, the initial evolution of archaeocetes in the early to mid-Eocene produced the highest evolutionary rates seen in cetaceans, concentrated in the maxilla, frontal, premaxilla, and nasal; second, the late Eocene divergence of the mysticetes and odontocetes drives a second peak in rates, with high rates and disparity sustained through the Oligocene; and third, the diversification of odontocetes, particularly sperm whales, in the Miocene (∼18-10 Mya) propels a final peak in the tempo of cetacean morphological evolution. Archaeocetes show the fastest evolutionary rates but the lowest disparity. Odontocetes exhibit the highest disparity, while mysticetes evolve at the slowest pace, particularly in the Neogene. Diet and echolocation have the strongest influence on cranial morphology, with habitat, size, dentition, and feeding method also significant factors impacting shape, disparity, and the pace of cetacean cranial evolution.
Coombs, Ellen J ; Division of Biosciences, Department of Genetics, Evolution & Environment, University College London, Gower Street, London WC1E 6BT, UK, Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. Electronic address: ellen.coombs.14@ucl.ac.uk
Felice, Ryan N; Division of Biosciences, Cell & Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK
Clavel, Julien; Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, 69622 Villeurbanne, France
Park, Travis; Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
This research was funded by the Natural Environment Research Council Doctoral Training Partnership training grant NE/L002485/1 to E.J.C. E.J.C.’s data collection was also supported by the UCL Bogue Fellowship and the Palaeontological Association Stan Wood Award. This research was also supported by National Science Foundation NSF-EAR 1349607 to J.G., B.B., A.G., and M.C., and University of Wisconsin-Oshkosh Faculty Development Grant to M.C. J.C. was funded by a Marie Skłodowska-Curie Individual Fellowship ( IF 797373-EVOTOOLS ), T.P. was funded by L everhulme Research Project Grant ( RPG-2019-323 ), and R.B. was funded by a FRIA fellowship from the F.R.S.-FNRS (grant FC 23645). Special thanks go to Richard Sabin for his help and support throughout and to Erich Fitzgerald for his helpful comments on improving the manuscript and analyses. We would like to thank Anne-Claire Fabre, Carla Bardua, Andrew Knapp, Eve Noirault, Heather White, João Vasco Leite, and Sandra Alvarez-Carretero for their comments, discussion, and help with code and Olivier Lambert, Felix Marx, and Robert Boessenecker for their helpful insights and discussion throughout E.J.C.'s research. Further thanks go to Eve Noirault for help with data collection and digitization of scans. Thanks also go to the many curators and museum staff who helped E.J.C., R.F.B., and M.C. collect scan data. Please see the list of institutions visited in the Github supplemental information. Final thanks go to the anonymous reviewers who helped us to improve the study.This research was funded by the Natural Environment Research Council Doctoral Training Partnership training grant NE/L002485/1 to E.J.C. E.J.C.’s data collection was also supported by the UCL Bogue Fellowship and the Palaeontological Association Stan Wood Award. This research was also supported by National Science Foundation NSF-EAR 1349607 to J.G. B.B. A.G. and M.C. and University of Wisconsin-Oshkosh Faculty Development Grant to M.C. J.C. was funded by a Marie Skłodowska-Curie Individual Fellowship (IF 797373-EVOTOOLS), T.P. was funded by Leverhulme Research Project Grant (RPG-2019-323), and R.B. was funded by a FRIA fellowship from the F.R.S.-FNRS (grant FC 23645). Special thanks go to Richard Sabin for his help and support throughout and to Erich Fitzgerald for his helpful comments on improving the manuscript and analyses. We would like to thank Anne-Claire Fabre, Carla Bardua, Andrew Knapp, Eve Noirault, Heather White, João Vasco Leite, and Sandra Alvarez-Carretero for their comments, discussion, and help with code and Olivier Lambert, Felix Marx, and Robert Boessenecker for their helpful insights and discussion throughout E.J.C.'s research. Further thanks go to Eve Noirault for help with data collection and digitization of scans. Thanks also go to the many curators and museum staff who helped E.J.C. R.F.B. and M.C. collect scan data. Please see the list of institutions visited in the Github supplemental information. Final thanks go to the anonymous reviewers who helped us to improve the study. Conceptualization, E.J.C. A.G. R.N.F. and J.C.; formal analysis, E.J.C. A.G. R.N.F. J.C. and T.P.; investigation, E.J.C. A.G. R.N.F. J.C. and T.P.; methodology, R.N.F. J.C. A.G. and E.J.C.; data acquisition, E.J.C. M.C. R.F.B. J.H.G. and B.B.; writing – review & editing, all authors. The authors declare no competing interests.
Gatesy, J., Geisler, J.H., Chang, J., Buell, C., Berta, A., Meredith, R.W., Springer, M.S., McGowen, M.R., A phylogenetic blueprint for a modern whale. Mol. Phylogenet. Evol. 66 (2013), 479–506, 10.1016/j.ympev.2012.10.012.
Marx, F., Lambert, O., Uhen, M., Major steps in the evolution of cetaceans. Cetacean Paleobiology, 2016, Wiley, 157–197.
Thewissen, H., The Walking Whales: From Land to Water in Eight Million Years. 2014, University of California Press.
Bianucci, G., Gingerich, P.D., Aegyptocetus tarfa, n. gen. et sp. (Mammalia, Cetacea), from the middle Eocene of Egypt: clinorhynchy, olfaction, and hearing in a protocetid whale. J. Vertebr. Paleontol. 31 (2011), 1173–1188, 10.1080/02724634.2011.607985.
Clementz, M.T., Goswami, A., Gingerich, P.D., Koch, P.L., Isotopic records from early whales and sea cows: contrasting patterns of ecological transition. J. Vertebr. Paleontol. 26 (2006), 355–370, 10.1671/0272-4634(2006)26[355:irfewa]2.0.co;2.
Uhen, M., Evolution of marine mammals: back to the sea after 300 million years. Anat. Rec. 290 (2007), 514–522.
Marx, F., Fordyce, R., Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity. R. Soc. Open Sci., 2, 2015, 140434.
Heyning, J., Mead, J., Evolution of the nasal anatomy of cetaceans. Thomas, J.A., Kastelein, R.A., (eds.) Sensory Abilities of Cetaceans, 1990, Springer, 67–79.
Klima, M., Development of the cetacean nasal skull. Adv. Anat. Embryol. Cell Biol. 149 (1999), 1–143, 10.1007/978-3-642-58612-5.
Churchill, M., Geisler, J.H., Beatty, B.L., Goswami, A., Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti). Soc. Study Evol. 72 (2018), 1092–1108, 10.1111/evo.13480.
Roston, R.A., Roth, V.L., Cetacean skull telescoping brings evolution of cranial sutures into focus. Anat. Rec. 302 (2019), 1055–1073, 10.1002/ar.24079.
Berta, A., Lanzetti, A., Ekdale, E.G., Deméré, T.A., From teeth to baleen and raptorial to bulk filter feeding in mysticete cetaceans: the role of paleontological, genetic, and geochemical data in feeding evolution and ecology. Integr. Comp. Biol. 56 (2016), 1271–1284, 10.1093/icb/icw128.
Geisler, J.H., Colbert, M.W., Carew, J.L., A new fossil species supports an early origin for toothed whale echolocation. Nature 508 (2014), 383–386, 10.1038/nature13086.
Churchill, M., Martínez-Cáceres, M., de Muizon, C., Mnieckowski, J., Geisler, J., The origin of high-frequency hearing in whales. Curr. Biol. 26 (2016), 2144–2149.
Park, T., Fitzgerald, E., Evans, A., Ultrasonic hearing and echolocation in the earliest toothed whales. Biol. Lett., 12, 2016, 20160060.
Boessenecker, R.W., Fraser, D., Churchill, M., Geisler, J.H., A toothless dwarf dolphin (Odontoceti: Xenorophidae) points to explosive feeding diversification of modern whales (Neoceti). Proc. Biol. Sci., 284, 2017, 20170531, 10.1098/rspb.2017.0531.
Coombs, E.J., Clavel, J., Park, T., Churchill, M., Goswami, A., Wonky whales: the evolution of cranial asymmetry in cetaceans. BMC Biol., 18, 2020, 10.1186/s12915-020-00805-4 86–24.
Steeman, M.E., Hebsgaard, M.B., Fordyce, R.E., Ho, S.Y.W., Rabosky, D.L., Nielsen, R., Rahbek, C., Glenner, H., Sørensen, M.V., Willerslev, E., Radiation of extant cetaceans driven by restructuring of the oceans. Syst. Biol. 58 (2009), 573–585, 10.1093/sysbio/syp060.
Marx, F.G., Uhen, M.D., Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales. Science 327 (2010), 993–996, 10.1126/science.1185581.
Jefferson, T., Webber, M., Pitman, R., Marine Mammals of the World: A Comprehensive Guide to Their Identification. 2015, Academic Press.
Bardua, C., Wilkinson, M., Gower, D.J., Sherratt, E., Goswami, A., Morphological evolution and modularity of the caecilian skull. BMC Evol. Biol., 19, 2019, 30, 10.1186/s12862-018-1342-7.
Felice, R.N., Tobias, J.A., Pigot, A.L., Goswami, A., Dietary niche and the evolution of cranial morphology in birds. Proc. Biol. Sci., 286, 2019, 20182677, 10.1098/rspb.2018.2677.
Lambert, O., Martínez-Cáceres, M., Bianucci, G., Di Celma, C., Salas-Gismondi, R., Steurbaut, E., Urbina, M., de Muizon, C., Earliest mysticete from the late Eocene of Peru sheds new light on the origin of baleen whales. Curr. Biol. 27 (2017), 1535–1541.e2, 10.1016/j.cub.2017.04.026.
Geisler, J.H., Boessenecker, R.W., Brown, M., Beatty, B.L., The origin of filter feeding in whales. Curr. Biol. 27 (2017), 2036–2042.e2, 10.1016/j.cub.2017.06.003.
Geisler, J.H., McGowen, M.R., Yang, G., Gatesy, J., A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea. BMC Evol. Biol., 11, 2011, 112, 10.1186/1471-2148-11-112.
Tsai, C.-H., Fordyce, R.E., A new archaic baleen whale Toipahautea waitaki (early Late Oligocene, New Zealand) and the origins of crown Mysticeti. R. Soc. Open Sci., 5, 2018, 172453, 10.1098/rsos.172453.
Dunn, O.J., Multiple comparisons among means. J. Am. Stat. Assoc. 56 (1961), 52–64, 10.1080/01621459.1961.10482090.
Clavel, J., Escarguel, G., Merceron, G., mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Methods Ecol. Evol. 6 (2015), 1311–1319, 10.1111/2041-210x.12420.
Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol 57 (1995), 289–300.
Benjamini, Y., Yekutieli, D., The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29 (2001), 1165–1188, 10.1214/aos/1013699998.
Boessenecker, R.W., Churchill, M., Buchholtz, E.A., Beatty, B.L., Geisler, J.H., Convergent evolution of swimming adaptations in modern whales revealed by a large macrophagous dolphin from the oligocene of South Carolina. Curr. Biol. 30 (2020), 3267–3273.e2, 10.1016/j.cub.2020.06.012.
Lambert, O., Bianucci, G., Post, K., De Muizon, C., Salas-Gismondi, R., Urbina, M., Reumer, J., The giant bite of a new raptorial sperm whale from the Miocene epoch of Peru. Nature 466 (2010), 105–108, 10.1038/nature09067.
Lipps, J.H., Mitchell, E., Trophic model for the adaptive radiations and extinctions of pelagic marine mammals. Paleobiology 2 (1976), 147–155, 10.1017/s0094837300003420.
Fitzgerald, E.M.G., The morphology and systematics of Mammalodon colliveri (Cetacea: Mysticeti), a toothed mysticete from the Oligocene of Australia. Zool. J. Linn. Soc. 158 (2010), 367–476, 10.1111/j.1096-3642.2009.00572.x.
de Muizon, C., Bianucci, G., Martínez-Cáceres, M., Lambert, O., Mystacodon selenensis, the earliest known toothed mysticete (Cetacea, Mammalia) from the late Eocene of Peru: anatomy, phylogeny, and feeding adaptations. Geodiversitas 41 (2019), 401–499, 10.5252/geodiversitas2019v41a11.
Fitzgerald, E.M.G., A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc. R. Soc. B Biol. Sci. 273 (2006), 2955–2963, 10.1098/rspb.2006.3664.
Cardini, A., Polly, P.D., Larger mammals have longer faces because of size-related constraints on skull form. Nat. Commun., 4, 2013, 2458, 10.1038/ncomms3458.
Randau, M., Sanfelice, D., Goswami, A., Shifts in cranial integration associated with ecological specialization in pinnipeds (Mammalia, Carnivora). R. Soc. Open Sci., 6, 2019, 190201, 10.1098/rsos.190201.
Vicari, D., Sabin, R.C., Brown, R.P., Lambert, O., Bianucci, G., Meloro, C., Skull morphological variation in a British stranded population of false killer whale (Pseudorca crassidens): a three-dimensional geometric morphometric approach. Can. J. Zool. 100 (2022), 119–132.
McCurry, M.R., Evans, A.R., Fitzgerald, E.M.G., Adams, J.W., Clausen, P.D., McHenry, C.R., The remarkable convergence of skull shape in crocodilians and toothed whales. Proc. R. Soc. B, 284, 2017, 20162348, 10.1098/rspb.2016.2348.
McCurry, M.R., Fitzgerald, E.M.G., Evans, A.R., Adams, J.W., McHenry, C.R., Skull shape reflects prey size niche in toothed whales. Biol. J. Linn. Soc. 121 (2017), 936–946, 10.1093/biolinnean/blx032.
Galatius, A., Racicot, R., McGowen, M., Olsen, M., Evolution and diversification of delphinid skull shapes. iScience, 23, 2020, 101543.
Slater, G., Price, S., Santini, F., Alfaro, M., Diversity versus disparity and the radiation of modern cetaceans. Proc. R. Soc. B Biol. Sci. 277 (2010), 3097–3104.
Sander, P.M., Griebeler, E.M., Klein, N., Juarbe, J.V., Wintrich, T., Revell, L.J., Schmitz, L., Early giant reveals faster evolution of large body size in ichthyosaurs than in cetaceans. Science, 374, 2021, eabf5787, 10.1126/science.abf5787.
Rivin, M.A., Early Miocene cetacean diversity in the Vaqueros Formation, Laguna Canyon, Orange County, California. 2010.
Lambert, O., Bianucci, G., de Muizon, C., Macroraptorial sperm whales (Cetacea, Odontoceti, Physeteroidea) from the Miocene of Peru. Zool. J. Linn. Soc. 179 (2017), 404–474.
Benites Palomino, A., Vélez Juarbe, J., Collareta, A., Ochoa, D., Altamirano, A., Carré, M., Laime, M., Urbina, M., Salas Gismondi, R., Nasal compartmentalization in Kogiidae (Cetacea, Physeteroidea): insights from a new late Miocene dwarf sperm whale from the Pisco Formation. Pap. Palaeontol., 7, 2021, spp2.1351.
El Adli, J., Deméré, T.A., Boessenecker, R.W., Herpetocetus morrowi (Cetacea: Mysticeti), a new species of diminutive baleen whale from the Upper Pliocene (Piacenzian) of California, USA, with observations on the evolution and relationships of the Cetotheriidae. Zool. J. Linn. Soc. 170 (2014), 400–466, 10.1111/zoj.12108.
Boessenecker, R.W., Fordyce, R.E., Cosmopolitanism and Miocene survival of Eomysticetidae (Cetacea: Mysticeti) revealed by new fossils from New Zealand. New Zealand J. Geology. Geophys. 60 (2017), 145–157, 10.1080/00288306.2017.1300176.
Barroso, C., Cranford, T.W., Berta, A., Shape analysis of odontocete mandibles: Functional and evolutionary implications. J. Morphol. 273 (2012), 1021–1030, 10.1002/jmor.20040.
Hocking, D.P., Marx, F.G., Park, T., Fitzgerald, E.M.G., Evans, A.R., A behavioural framework for the evolution of feeding in predatory aquatic mammals. Proc. R. Soc. B Biol. Sci., 284, 2017, 20162750, 10.1098/rspb.2016.2750.
Hocking, D.P., Marx, F.G., Park, T., Fitzgerald, E.M.G., Evans, A.R., Reply to comment by Kienle (2017b). Proc. R. Soc. B Biol. Sci., 284, 2017, 20171836, 10.1098/rspb.2017.1836.
Galatius, A., Goodall, R.N.P., Skull shapes of the Lissodelphininae: radiation, adaptation and asymmetry. J. Morphol. 277 (2016), 776–785, 10.1002/jmor.20535.
Turvey, S.T., Pitman, R.L., Taylor, B.L., Barlow, J., Akamatsu, T., Barrett, L.A., Zhao, X., Reeves, R.R., Stewart, B.S., Wang, K., et al. First human-caused extinction of a cetacean species. Biol. Lett. 3 (2007), 537–540, 10.1098/rsbl.2007.0292.
Cassens, I., Vicario, S., Waddell, V.G., Balchowsky, H., Van Belle, D., Ding, W., Fan, C., Mohan, R.S.L., Simoes-Lopes, P.C., Bastida, R., et al. Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proc. Natl. Acad. Sci. USA 97 (2000), 11343–11347, 10.1073/pnas.97.21.11343.
Lloyd, G.T., Slater, G.J., A total-group phylogenetic metatree for Cetacea and the importance of fossil data in diversification analyses. Syst. Biol. 70 (2021), 922–939.
R Development Core Team. R: a language and environment for statistical computing. 2020, R Foundation for Statistical Computing.
Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G., Principles for the virtual reconstruction of hominin crania. J. Hum. Evol. 57 (2009), 48–62.
Gunz, P., Mitteroecker, P., Semilandmarks: a method for quantifying curves and surfaces. Hystrix 24 (2013), 103–109.
Cardini, A., Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. J. Zool. Syst. Evol. Res. 55 (2016), 1–10, 10.1111/jzs.12144.
Cardini, A., Lost in the other half: improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Syst. Biol. 65 (2016), 1096–1106, 10.1093/sysbio/syw043.
Fahlke, J.M., Gingerich, P.D., Welsh, R.C., Wood, A.R., Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water. Proc. Natl. Acad. Sci. USA 108 (2011), 14545–14548, 10.1073/pnas.1108927108.
Bookstein, F., Morphometric Tools for Landmark Data: Geometry and Biology. 1991, Cambridge University Press.
Bookstein, F.L., Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1 (1997), 225–243, 10.1016/s1361-8415(97)85012-8.
Bardua, C., Felice, R.N., Watanabe, A., Fabre, A.C., Goswami, A., A practical guide to sliding and surface semi landmarks in morphometric analyses. Integr. Org. Biol. 1 (2019), 1–34, 10.1093/iob/obz016.
Fahlke, J., Hampe, O., Cranial symmetry in baleen whales (Cetacea, Mysticeti) and the occurrence of cranial asymmetry throughout cetacean evolution. Naturwissenschaften, 102, 2015, 58.
Coombs, E.J., Felice, R.N., Quantifying asymmetry in non-symmetrical morphologies, with an example from Cetacea. Preprint at bioRxiv, 2021, 10.1101/2021.11.17.468940.
Gunz, P., Mitteroecker, P., Bookstein, F., Chapter three: semilandmarks in three dimensions. Slice, D.E., (eds.) Modern Morphometrics in Physical Anthropology, 2005, Kluwer Academic/Plenum, 73–98.
Rohlf, F.J., Slice, D., Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39 (1990), 40–59, 10.2307/2992207.
Schlager, S., Morpho and Rvcg - shape analysis in R. Zheng, G., Li, S., Szekely, G., (eds.) Statistical Shape and Deformation Analysis, 2017, Academic Press, 217–256.
de Muizon, C., Domning, D., The anatomy of Odobenocetops (Delphinoidea, Mammalia), the walrus-like dolphin from the Pliocene of Peru and its palaeobiological implications. Zool. J. Linn. Soc. 134 (2002), 423–452, 10.1046/j.1096-3642.2002.00015.x.
Velez-Juarbe, J., Wood, A.R., De Gracia, C., Hendy, A.J.W., Evolutionary patterns among living and fossil kogiid sperm whales: evidence from the Neogene of Central America. PLoS One, 10, 2015, e0123909, 10.1371/journal.pone.0123909.
Collareta, A., Lambert, O., de Muizon, C., Urbina, M., Bianucci, G., Koristocetus pescei gen. et sp. nov., a diminutive sperm whale (Cetacea: Odontoceti: Kogiidae) from the late Miocene of Peru. Fossil Rec. 20 (2017), 259–278, 10.5194/fr-20-259-2017.
Benites-Palomino, A., Vélez-Juarbe, J., Salas-Gismondi, R., Urbina, M., Scaphokogia totajpe, sp. nov., a new bulky-faced pygmy sperm whale (Kogiidae) from the late Miocene of Peru. J. Vertebr. Paleontol., 39, 2019, e1728538, 10.1080/02724634.2019.1728538.
Peri, E., Collareta, A., Bianucci, G., A new record of Physeteroidea from the Upper Miocene of the Pietra leccese (southern Italy): systematics, paleoecology and taphonomy of a fossil macroraptorial sperm whale. Riv. It. Paleontol. Strat. 126 (2020), 751–769.
Post, K., Bosselaers, M., Late Pliocene occurrence of Hemisyntrachelus (Odontoceti, Delphinidae) in the southern North Sea. DEINSEA 11 (2005), 29–45.
Laime Molina, M.J., Urbina Schmitt, M., Chacaltana Budiel, C., Tejada Medina, L., Los delfines Lophocetinae (Mammalia: Cetacea: Kentriodontidae) de la formación pisco de cerro yesera de amara, Ocucaje, Ica. 2018, 47–50.
Lambert, O., Godfrey, S.J., Fitzgerald, E.M.G., Yaquinacetus meadi, a new latest Oligocene–early Miocene dolphin (Cetacea, Odontoceti, Squaloziphiidae, fam. nov.) from the Nye Mudstone (Oregon, U.S.A.). J. Vertebr. Paleontol., 38, 2018, e1559174, 10.1080/02724634.2018.1559174.
Rosel, P.E., Wilcox, L.A., Yamada, T.K., Mullin, K.D., A new species of baleen whale (Balaenoptera) from the Gulf of Mexico, with a review of its geographic distribution. Mar. Mamm. Sci. 37 (2021), 577–610, 10.1111/mms.12776.
Berta, A., Lanzetti, A., Feeding in marine mammals: an integration of evolution and ecology through time. Palaeontol. Electron., 23, 2020, 4, 10.26879/951.
Adams, D., Collyer, M., Kaliontzopoulou, A., Geomorph: software for geometric morphometric analyses. R package version 3.2.1. https://cran.r-project.org/package=geomorph, 2020.
Revell, L.J., Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3 (2012), 217–223, 10.1111/j.2041-210x.2011.00169.x.
Pagel, M., Inferring evolutionary processes from phylogenies. Zool. Scr. 26 (1997), 331–348, 10.1111/j.1463-6409.1997.tb00423.x.
Pagel, M., Inferring the historical patterns of biological evolution. Nature 401 (1999), 877–884, 10.1038/44766.
Gelman, A., Prior distributions for variance parameters in hierarchical models (comment on article by Browne and Draper). Bayesian Anal. 1 (2006), 515–534, 10.1214/06-ba117a.
Gelman, A., Rubin, D., Inference from iterative simulation using multiple sequences. Stat. Sci. 7 (1992), 457–472.
Plummer, M., Best, N., Cowles, K., Vines, K., CODA: convergence diagnosis and output analysis for MCMC. R News 6 (2006), 7–11.
Ferguson-Gow, H., BTprocessR: a set of tools to help with the interpretation and analysis of the output of BayesTraits MCMC analyses. 2020.
Xie, W., Lewis, P.O., Fan, Y., Kuo, L., Chen, M.H., Improving marginal likelihood estimation for bayesian phylogenetic model selection. Syst. Biol. 60 (2011), 150–160, 10.1093/sysbio/syq085.
Venditti, C., Meade, A., Pagel, M., Multiple routes to mammalian diversity. Nature 479 (2011), 393–396, 10.1038/nature10516.
Felice, R., Macroevo plots in R. https://github.com/rnfelice/macroevo.plots/tree/master/R, 2021.
Wang, L.G., Lam, T.T.Y., Xu, S., Dai, Z., Zhou, L., Feng, T., Guo, P., Dunn, C.W., Jones, B.R., Bradley, T., et al. Treeio: an R package for phylogenetic tree input and output with richly annotated and associated data. Mol. Biol. Evol. 37 (2020), 599–603, 10.1093/molbev/msz240.
Bardua, C., Fabre, A.C., Clavel, J., Bon, M., Das, K., Stanley, E.L., Blackburn, D.C., Goswami, A., Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs. Nat. Commun., 12, 2021, 2503, 10.1038/s41467-021-22792-y.
Guillerme, T., Weisbecker, V., landvR: tools for measuring landmark position variation. 2019, Zenodo, 10.5281/zenodo.2620785.
Clavel, J., Aristide, L., Morlon, H., A penalized likelihood framework for high-dimensional phylogenetic comparative methods and an application to new-world monkeys brain evolution. Syst. Biol. 68 (2019), 93–116, 10.1093/sysbio/syy045.
Clavel, J., Morlon, H., Reliable phylogenetic regressions for multivariate comparative data: illustration with the MANOVA and application to the effect of diet on mandible morphology in phyllostomid bats. Syst. Biol. 69 (2020), 927–943, 10.1093/sysbio/syaa010.