Skip to main content
Springer Nature Link
Log in

The Endocranial Cast of Indohyus (Artiodactyla, Raoellidae): The Origin of the Cetacean Brain

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

A Publisher Correction to this article was published on 26 May 2021

This article has been updated

Abstract

We present the first description of the endocranial cast of the small raoellid artiodactyl Indohyus indirae. Raoellidae are sister group to Cetacea and the new morphological observations allow for outlining some of the early steps of the evolutionary history of the cetacean brain. The combination of primitive artiodactyl features and typical cetacean characters is unique about the Indohyus endocast. The fact that it presents the symplesiomorphic brain pattern observed in earliest Artiodactyla indicates that the cetacean brain derives from a very simple, plesiomorphic brain, with simple neocortical folding pattern, widely exposed midbrain, and concurrent small neocortex expansion. On the other hand, the Indohyus endocast shows characters that also occur in early cetaceans. These include modifications of the olfactory tract with narrow, elongated olfactory bulbs and peduncles, accompanied by a posterior location of the braincase in the cranium. The derived endocranial cast features of Indohyus mainly reflect changes in cranial architecture and these are most probably associated with modifications of the masticatory apparatus and a shift in diet. Indohyus meninges were very thin as in most terrestrial artiodactyls and it had no extensive rostral or lateral retia mirabilia. It however shows a branching pattern of ramification of intraosseous blood sinuses above the cerebellum that might represent the initial development of the caudal venous rete mirabile that would have colonized the endocranial cavity later on, in early archaeocetes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Vietnam)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Data for this study are available in the MorPhoMuseuM online platform Repository: http://dx.doi.org/10.18563/journal.m3.137; models ids: M3#710_RR207; M3#711_RR601.

Change history

References

  • Bajpai S, Thewissen JGM, Conley RW (2011) Cranial anatomy of middle Eocene Remingtonocetus (Cetacea, Mammalia) from Kutch, India. J Paleontol 85(4):703-718

    Article  Google Scholar 

  • Bajpai S, Thewissen JGM, Sahni A (1996) Indocetus (Cetacea, Mammalia) endocasts from Kachchh (India). J Vertebr Paleontol 6:582-584

    Article  Google Scholar 

  • Berta A, Ekdale EG, Cranford TW (2014) Review of the cetacean nose: form, function, and evolution. Anat Rec 297(11):2205-2215

    Article  Google Scholar 

  • Bisconti M, Damarco P, Tartarelli G, Pavia M, Carnevale G (2021). A natural endocast of an early Miocene odontocete and its implications in cetacean brain evolution. J Comp Neurol 529(6):1198-1227

    Article  PubMed  Google Scholar 

  • Breathnach AS (1955) Observations on endocranial casts of recent and fossil cetaceans. J Anat 89:532-546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butler H (1967) The development of mammalian dural venous sinuses with especial reference to the post-glenoid vein. J Anat 102:33-56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coombs MC, Coombs WP (1982) Anatomy of the ear region of four Eocene artiodactyls: Gobiohyus,? Helohyus, Diacodexis and Homacodon. J Vertebr Paleontol 2(2):219-236

    Article  Google Scholar 

  • Cooper LN, Clementz MT, Usip S, Bajpai S, Hussain ST, Hieronymus TL (2016) Aquatic habits of cetacean ancestors: integrating bone microanatomy and stable isotopes. Integr Comp Biol 56(6):1370-1384

    Article  PubMed  Google Scholar 

  • Cooper LN, Thewissen JGM, Bajpai S, Tiwari BN (2012) Postcranial morphology and locomotion of the Eocene raoellid Indohyus (Artiodactyla: Mammalia). Hist Biol 24(3):279-310

    Google Scholar 

  • Dart RMA, Andrews CW (1923) The brain of the Zeuglodonlidæ (Cetacea). Proc Zool Soc Lond 93:615-654

    Article  Google Scholar 

  • Dechaseaux C (1961) Encephales d’artiodactyles fossiles. In: Pivetau J (ed) Traité de Paléontologie Tome 6(1). Masson et Cie, Paris, pp 1085-1104

    Google Scholar 

  • Dechaseaux C (1969) Moulages endocrâniens d’artiodactyles primitifs, essai sur l’histoire du néopallium. Ann Paleontol 55:195-248

    Google Scholar 

  • Edinger T (1955) Hearing and smell in cetacean history. Europ Neurol 129(1-3):37-58.

    Article  CAS  Google Scholar 

  • Fraser FC, Purves PE (1960) Anatomy and function of the cetacean ear. Proc Roy Soc 152(946):62-77

    CAS  Google Scholar 

  • Gatesy J, Geisler JH, Chang J, Buell C, Berta A, Meredith RW, Springer MS, McGowen MR (2013) A phylogenetic blueprint for a modern whale. Mol Phylogenet Evol 66(2):479-506

    Article  PubMed  Google Scholar 

  • Geisler JH, Luo Z (1998) Relationships of Cetacea to terrestrial ungulates and the evolution of cranial vasculature in Cete. In: Thewissen JGM (ed) The Emergence of Whales. Plenum Press, New York, pp163-212

    Chapter  Google Scholar 

  • Geisler JH, Theodor JM, Uhen MD, Foss SE (2007) Phylogenetic relationships of cetaceans to terrestrial artiodactyls. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 19-31

    Google Scholar 

  • Giannini NP, Wible JR, Simmons NB (2006) On the cranial osteology of Chiroptera. I. Pteropus (Megachiroptera: Pteropodidae). Bull Am Mus Nat Hist 295:1-134

    Article  Google Scholar 

  • Gingerich PD, Arif M, Clyde WC (1995) New archaeocetes (Mammalia, Cetacea) from the middle Eocene Domanda Formation of Sulaiman Range, Punjab (Pakistan). Contrib Mus Paleontol Univ Michigan 29:291-330

    Google Scholar 

  • Glezer II, Hof PR, Leranth C, Morgane PJ (1993) Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cerebral Cortex 3(3):249-272

    Article  CAS  PubMed  Google Scholar 

  • Glezer II, Jacobs MS, Morgane PJ (1988) Implications of the “initial brain” concept for brain evolution in Cetacea. Behav Brain Sci 11(1):75-89

    Article  Google Scholar 

  • Godfrey SJ, Geisler J, Fitzgerald EM (2013) On the olfactory anatomy in an archaic whale (Protocetidae, Cetacea) and the minke whale Balaenoptera acutorostrata (Balaenopteridae, Cetacea). Anat Rec 296(2):257-272

    Article  Google Scholar 

  • Hanson A, Grisham W, Sheh C, Annese J, Ridgway S (2013) Quantitative examination of the bottlenose dolphin cerebellum. Anat Rec 296(8):1215-1228

    Article  Google Scholar 

  • Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287(1):1142-1152

    Article  Google Scholar 

  • Hof PR, Van der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290(1):1-31

    Article  Google Scholar 

  • Hoffmann A, Stoffel MH, Nitzsche B, Lobsien D, Seeger J, Schneider H, Boltze J (2014) The ovine cerebral venous system: comparative anatomy, visualization, and implications for translational research. PLoS One 9(4):e92990

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jerbi H, Pérez W (2018) Descriptive anatomy of artery of one-humped camel head (Camelus dromedarius). MOJ Anat Physiol 5:331-333

    Google Scholar 

  • Kishida T, Thewissen JGM, Hayakawa T, Imai H, Agata K (2015) Aquatic adaptation and the evolution of smell and taste in whales. Zool Lett 1(1):1-10

    Article  Google Scholar 

  • Knopf JP, Hof PR, Oelschläger HH (2016) The neocortex of Indian River dolphins (genus Platanista): comparative, qualitative and quantitative analysis. Brain Behav Evol 88(2):93-110

    Article  PubMed  Google Scholar 

  • Lebrun R, Orliac MJ (2017) MorphoMuseuM: an online platform for publication and storage of virtual specimens. Paleontol Soc Pap 22:183-195

    Article  Google Scholar 

  • Macrini TE (2009) Description of a digital cranial endocast of Bathygenys reevesi (Merocoidodontidae, Oreodontoidea) and implications for apomorphy based diagnosis of isolated, natural endocasts. J Vertebr Paleontol 29:1199-1211

    Article  Google Scholar 

  • Malmierca MS, Merchán MA, Henkel CK, Oliver DL (2002) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22(24):10891-10897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino L (2002) Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav Evol 59(1-2):21-32

    Article  PubMed  Google Scholar 

  • Marino L (1998) A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain Behav Evol 51(4):230-238

    Article  CAS  PubMed  Google Scholar 

  • Marino L, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Lusseau D, McCowan B, Nimchinsky EA, Pack AA, Rendell L, Reidenberg JS, Reiss D, Uhen MD, Van der Gucht E, Whitehead H (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5(5):e139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marino L, McShea DW, Uhen MD (2004) Origin and evolution of large brains in toothed whales. Anat Rec 281A:1247-1255

    Article  Google Scholar 

  • Marino L, Uhen MD, Frohlich B, Aldag JM, Blane C, Bohaska D, Whitmore FC (2000) Endocranial volume of mid-late Eocene archaeocetes (Order: Cetacea) revealed by computed tomography: implications for cetacean brain evolution. J Mammal Evol 7(2):81-94

    Article  Google Scholar 

  • Marino L, Uhen MD, Pyenson ND, Fröhlich B (2003) Reconstructing cetacean brain evolution using computed tomography. Anat Rec 272B:107-117

    Article  Google Scholar 

  • Martínez-Cáceres M, Lambert O, Muizon C de (2017) The anatomy and phylogenetic affinities of Cynthiacetus peruvianus, a large Dorudon-like basilosaurid (Cetacea, Mammalia) from the late Eocene of Peru. Geodiversitas 39(1):7-163

    Article  Google Scholar 

  • McFarland WL (1979) Blood supply to the brain of the dolphin Tursiops truncatus, with comparative observations on special aspects of the cerebrovascular supply of other vertebrates. Neurosci Behav Rev 3:1-93

    Google Scholar 

  • Mead JG, Fordyce RE (2009) The therian skull: a lexicon with emphasis on the odontocetes. Smithsonian Contrib Zool 627:1–248

    Article  Google Scholar 

  • Melnikov VV (1997) The arterial system of the sperm whale (Physeter macrocephalus). J Morphol 234(1):37-50

    Article  CAS  PubMed  Google Scholar 

  • Morgane PJ, Glezer II, Jacobs MS (1988) Visual cortex of the dolphin: an image analysis study. J Comp Neurol 273(1):3-25

    Article  CAS  PubMed  Google Scholar 

  • Morgane PJ, Jacobs MS, Galaburda A (1985) Conservative features of neocortical evolution in dolphin brain. Brain Behav Evol 23:176-184

    Article  Google Scholar 

  • Mourlam MJ, Orliac MJ (2019) Early evolution of the ossicular chain in cetacea: into the middle ear gears of a semi-aquatic protocetid whale. Proc R Soc B 286(1912):20191417

    Article  PubMed  PubMed Central  Google Scholar 

  • Mourlam MJ, Orliac MJ (2017) Infrasonic and ultrasonic hearing evolved after the emergence of modern whales. Curr Biol 27(12):1776-1781.e9

    Article  CAS  PubMed  Google Scholar 

  • Nummela AS, Hussain ST, Thewissen JGM (2006) Cranial anatomy of Pakicetidae (Cetacea, Mammalia). J Vertebr Paleontol 26:746-759

    Article  Google Scholar 

  • Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K (2004) Eocene evolution of whale hearing. Nature 430(7001):776-778

    Article  CAS  PubMed  Google Scholar 

  • Nummela S, Thewissen JG, Bajpai S, Hussain T, Kumar K (2007) Sound transmission in archaic and modern whales: Anatomical adaptations for underwater hearing. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 290(6):716-733

  • O’Brien HD (2015) Cranial arterial pattern of the Sri Lankan spotted chevrotain, Moschiola memmina, and comparative basicranial osteology of the Tragulidae. PeerJ 3:e1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogawa T, Arifuku S (1948) On the acoustic system in the cetacean brains. Sci Rep Whales Res Inst Tokyo 2:1-20

    Google Scholar 

  • Orliac MJ, Ducrocq S (2012) Eocene raoellids (Mammalia, Cetartiodactyla) outside the Indian Subcontinent: palaeogeographical implications. Geol Mag 149(1):80-92

    Article  Google Scholar 

  • Orliac MJ, Antoine PO, Charruault AL, Hervet S, Prodeo F, Duranthon F (2013) Specialization for amphibiosis in Brachyodus onoideus (Artiodactyla, Hippopotamoidea) from the early Miocene of France. Swiss J Geosci 106(2):265-278

    Article  Google Scholar 

  • Orliac MJ, Gilissen E (2012) Virtual endocranial cast of earliest Eocene Diacodexis (Artiodactyla, Mammalia) and morphological diversity of early artiodactyl brains. Proc Roy Soc B 279(1743):3670-3677

    Article  CAS  Google Scholar 

  • Orliac M, Guy F, Lebrun R (2014) Osteological connections of the petrosal bone of the extant Hippopotamidae Hippopotamus amphibius and Choeropsis liberiensis. MorphoMuseum J 1(1)-e1:1–6

  • Pihlstrom H (2008) Comparative anatomy and physiology of chemical senses in aquatic mammals. In: Thewissen JGM, Nummela S (eds) Sensory Evolution on the Threshold, Adaptations in Secondarily Aquatic Vertebrates. University of California Press, Berkeley, pp 95-112

    Google Scholar 

  • Pilleri G (1991) Betrachtungen über das Gehirn der Archaeoceti (Mammalia, Cetacea) aus dem Fayum Agyptens. Investigations on Cetacea 23:193-211

    Google Scholar 

  • Pilleri G (1966) Morphology of the brain of the humpback whale, Megaptera novaeangliae Borowski (Cetacea, Mysticeti, Balaenopteridae). J Hirnforsch 8(5):437-491

    CAS  PubMed  Google Scholar 

  • Pilleri G (1966) Über die Anatomie des Gehirns des Ganges Delphins, Platanista gangetica. Rev Suisse Zool 73 :113-118

    Article  Google Scholar 

  • Raghanti MA, Wicinski B, Meierovich R, Warda T, Dickstein DL, Reidenberg JS, Tang CY, George JC, Thewissen JGM, Butti C, Hof PR (2019) A comparison of the cortical structure of the bowhead whale (Balaena mysticetus), a basal mysticete, with other cetaceans. Anat Rec 302(5):745-760

    Article  Google Scholar 

  • Ranga Rao A (1972) New mammalian genera and species from the Kalakot zone of Himalayan foot hills near Kalakot, Jammu and Kashmir State, India. Special Paper of the Directorate of Geology, Oil, and Natural Gas Commission, Dehra Dun, India 1:1-22

    Google Scholar 

  • Ranga Rao A (1971) New mammals from Murree (Kalakot Zone) of the Himalayan foot hills near Kalakot, Jammu and Kashmir state, India. J Geol Soc India 12:125-134

    Google Scholar 

  • Ridgway SH, Tarple VRJ (1996) Brain mass comparisons in Cetacea. Proc Internatl Assoc Aquat Anim Med 27:55-57

    Google Scholar 

  • Ries FA, Langworthy OR (1937). A study of the surface structure of the brain of the whale (Balaenoptera physalus and Physeter catodon). J Comp Neurol 68(1):1-47

    Article  Google Scholar 

  • Sahni A, Khare SK (1971) Three new Eocene mammals from Rajouri District, Jammu and Kashmir. J Palaeontol Soc India 14:41-53

    Google Scholar 

  • Slijper EJ (1936) Die Cetaceen. Vergleichend-anatomisch und systematisch. Capita Zoologica 7-8:1-590

    Google Scholar 

  • Smith GE (1903) The brain of the Archaeoceti. Proc Roy Soc 71:322-331

    Google Scholar 

  • Theodor JM, Erfurt J, Métais G (2007) The earliest artiodactyls. In The evolution of Artiodactyla (eds D.R. Prothero & S. E. Foss), pp. 32–58. Baltimore: John Hopkins University Press.

  • Thewissen JGM (2014) The Walking Whales: from Land to Water in Eight Million Years. University of California Press, Berkeley, 245 pp

    Book  Google Scholar 

  • Thewissen JGM, Bajpai S (2009) New skeletal material of Andrewsiphius and Kutchicetus, two Eocene cetaceans from India. J Paleontol 83(5):635-663

    Article  Google Scholar 

  • Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN (2007) Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450(7173):1190-1194

    Article  CAS  PubMed  Google Scholar 

  • Thewissen JGM, Cooper LN, George JC, Bajpai S (2009) From land to water: the origin of whales, dolphins, and porpoises. Evolution: Education and Outreach 2:272–288

  • Thewissen JGM, Madar SI, Hussain ST (1996) Ambulocetus natans an Eocene cetacean (Mammalia) from Pakistan. Cour Forsch-Inst Senckenberg 191:1-86

    Google Scholar 

  • Thewissen JGM, Nanda AC, Bajpai S (2020) Indohyus, endemic radiation of raoellid artiodactyls in the Eocene of India and Pakistan. In: Prasad GVR, Patnaik R (eds) Biological Consequences of Plate Tectonics New Perspectives on Post-Gondwana: Break-up-A Tribute to Ashok Sahni. Springer, Cham, pp 337-346

    Chapter  Google Scholar 

  • Thewissen JGM, Williams EM, Hussain SM (2001) Eocene mammal faunas from northern Indo-Pakistan. J Vertebr Paleontol 21:347-366

    Article  Google Scholar 

  • Uhen MD (2004) Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): an archaeocete from the middle to late Eocene of Egypt. Pap Paleontol 34:1-222

    Google Scholar 

  • Vogl AW, Fisher HD (1981) Arterial circulation of the spinal cord and brain in the Monodontidae (Order Cetacea). J Morphol 170(2):171-180

    Article  CAS  PubMed  Google Scholar 

  • Wible JR (1990) Petrosals of Late Cretaceous marsupials from North America and a cladistic analysis of the petrosal in therian mammals. J Vertebr Paleontol 10(2):183-205

    Article  Google Scholar 

  • Wible JR (1993) Cranial circulation and relationships of the colugo Cynocephalus (Dermoptera, Mammalia). Am Mus Novitates 3072:1-27

    Google Scholar 

  • Wible JR (2008) On the cranial osteology of the Hispaniolan solenodon, Solenodon paradoxus Brandt, 1833 (Mammalia, Lipotyphla, Solenodontidae). Ann Carnegie Mus 77(3):321–402

    Article  Google Scholar 

  • Wible JR (2011) On the treeshrew skull (Mammalia, Placentalia, Scandentia). Ann Carnegie Mus 79(3):149-230

    Article  Google Scholar 

  • Whitmore FC (1953) Cranial morphology of some Oligocene Artiodactyla. Geol Surv Prof Pap 243:117-160

    Google Scholar 

  • Worthy GA, Hickie JP (1986) Relative brain size in marine mammals. Am Nat 128(4):445-459

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to G. Thiery and S. Ducroqc (PALEVOPRIM) for granting access to the µCT scan data of the Microbunodon minimum cranium from La Milloque. We thank J. Maugoust 5ISEM) for fruitful discussions on brain structures. J.G.M. Thewissen would like to thank the Hennecke Family Foundation for funding. We thanks M. Mourlam (ISEM) for his help during scanning, and R. Lebrun for the access of scanning facilities (MRI platform member of the national infrastructure France-BioImaging supported by the French National Research Agency [ANR-10-INBS-04, «Investments for the future»], the LabEx CEMEB [ANR-10-LABX-0004] and NUMEV [ANR-10-LABX-0020]). We are grateful to the two anonymous reviewers for their helpful comments and to J.R. Wible for his thorough proofreading and useful remarks. This work was supported by the ANR DEADENDER [ANR-18-CE02-0003-01].

Funding

This work was, in part, financially supported by the ANR program DEADENDER (ANR-18-CE02-0003–01) headed by M. J. Orliac.

Author information

Authors and Affiliations

  1. Institut Des Sciences de L’Évolution de Montpellier, Université de Montpellier, CNRS, EPHE, Place Eugène Bataillon, 34095, Cedex 5, Montpellier, IRD, France

    Maeva J. Orliac

  2. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, 4209 State Route 44, Rootstown, OH, 44272, USA

    J. G. M. Thewissen

Authors
  1. Maeva J. Orliac
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. G. M. Thewissen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maeva J. Orliac.

Ethics declarations

Competing Interests

The authors declare having no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 837 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orliac, M.J., Thewissen, J.G.M. The Endocranial Cast of Indohyus (Artiodactyla, Raoellidae): The Origin of the Cetacean Brain. J Mammal Evol 28, 831–843 (2021). https://doi.org/10.1007/s10914-021-09552-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-021-09552-x

Keywords