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Intraspecific Variation of Endocranial Structures in Extant Equus: A Prelude to Endocranial Studies in Fossil Equoids

Endocranial Intraspecific Variation in Equus

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Abstract

Intraspecific variation of endocranial structures is not widely studied in most mammals, particularly fossil mammals, which are mainly represented by a few preserved crania. However, a description of this variation is necessary to be able to study fossil mammals from an ecological and phylogenetic perspective. To facilitate further analyses on fossil equoids, digital reconstructions of the cranial endocast, petrosal bone, and bony labyrinth were created based on CT scans, taken from a wild population of 12 Equus caballus przewalskii currently being monitored. Using descriptive, biometric, and morphometric analyses, an unsuspected range of intraspecific variation for 40 endocranial characters is revealed. Intraindividual variation can be further understood through the comparison of paired organs from a single individual. These results prompt cautious consideration of these characters, as well as an index for the determination of hearing abilities or encephalization quotients.

Thanks to this work, more is now known about the intraspecific variation of the external morphology of the most frequently studied structures in the endocranium of mammals and more specifically in equoids, where no such study had been undertaken until now. This will help to improve the resolution of fossil endocranial studies.

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References

  • Achilli A, Olivieri A, Soares P, Lancioni H, Kashani BH, Perego UA, Nergadze SG, Carossa V, Santagostino M, Capomaccio S, Felicetti M, Al-Achkar W, Penedo CT, Verini-Supplizi A, Houshmand M, Woodward SR, Semino O, Silvestrelli M, Giulotto E, Pereira L, Bandelt H-J, Torroni A (2012) Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc Natl Acad Sci USA 109(7):2449–2454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anthony R, Grzybowski J de (1930) Le neopallium des Equidés. Étude du développement de ses plissements. J Anat 64(2):147–169

  • Avizo Software (2010) VSG Website [Online] (Updated 2015). Version 7. Available at: http://www.fei.com/software/avizo3d/

  • Barone R (2004) Anatomie comparée des mammifères domestiques. Tome 6 : Neurologie I. Système nerveux central. Vigot, Paris

  • Benoit J, Adnet S, El Mabrouk E, Khayatu H, Ben Haj Ali M, Marivaux L, Merzeraud G, Mérigeaud S, Vianey-Liaud M, Tabuce R (2013a) Cranial remain from Tunisia provides new clues for the origin and evolution of Sirenia (Mammalia, Afrotheria) in Africa. PLoS ONE 8(1):1–9

    Article  Google Scholar 

  • Benoit J, Crumpton N, Mérigeaud S, Tabuce R (2013b) A memory already like an elephant’s? The advanced brain morphology of the last common ancestor of Afrotheria (Mammalia). Brain Behav Evol 81(3):154–169

    Article  PubMed  Google Scholar 

  • Bernard KA, Moore-Jansen PH (2009) Quantifying male and female shape variation in the mastoid region of the temporal bone. Proceedings of the 5th Annual GRASP Symposium, Wichita State University, 80–81

  • Boddy AM, McGowen MR, Sherwood CC, Grossman LI, Goodman M, Wildman DE (2012) Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling. J Evol Biol 25:981–994

    Article  CAS  PubMed  Google Scholar 

  • Bookstein FL (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image. Anal 1:225–243

    Article  CAS  PubMed  Google Scholar 

  • Brochu CA (2000) A digitally-rendered endocast for Tyrannosaurus rex. J Vertebr Paleontol 20(1):1–6

    Article  Google Scholar 

  • Cifelli RL (1982) The petrosal structure of Hyopsodus with respect to that of some other ungulates, and its phylogenetic implications. J Paleontol 56(3):795–805

    Google Scholar 

  • Costeur L (2014) The petrosal bone and inner ear of Micromeryx flourensianus (Artiodactyla, Moschidae) and inferred potential for ruminant phylogenetics. Zitteliana B 32:1–16

    Google Scholar 

  • Cuvier G (1836) Recherches sur les ossemens fossiles où l’on rétablit les caractères de plusieurs animaux dont les révolutions du globe ont détruit les espèces. D’Ocagne, Paris

    Google Scholar 

  • Danilo L, Remy JA, Vianey-Liaud M, Marandat B, Sudre J, Lihoreau F (2013) A new Eocene locality in southern France sheds light on the basal radiation of Palaeotheriidae (Mammalia, Perissodactyla, Equoidea). J Vertebr Paleontol 33(1):195–215

    Article  Google Scholar 

  • David R, Droulez J, Allain R, Berthoz A, Janvier P, Bennequin D (2010) Motion from the past. A new method to infer vestibular capacities of extinct species. C R Palevol 9(6–7):397–410

    Article  Google Scholar 

  • Dechaseaux C (1962) Cerveaux d'animaux disparus. Masson, Paris

  • Dietrich WO (1936) Die Huftiere aus dem Obereozän von Mähringen auf der Ulmer Alb. Palaeontographica 83A:163–209

    Google Scholar 

  • Dong W (2008) Virtual cranial endocast of the oldest giant panda (Ailuropoda microta) reveals great similarity to that of its extant relative. Naturwissenschaften 95:1079–1083.

    Article  CAS  PubMed  Google Scholar 

  • Edinger T (1948) Evolution of the horse brain. Geol Soc Am Mem 25:1–177

    Article  Google Scholar 

  • Ekdale EG (2010) Ontogenic variation in the bony labyrinth of Monodelphis domestica (Mammalia: Marsupalia) following ossification of the inner ear cavities. Anat Rec 293:1896–1912

    Article  Google Scholar 

  • Ekdale EG (2011) Morphological variation in the ear region of Pleistocene Elephantimorpha (Mammalia, Proboscidea) from central Texas. J Morphol 272:452–464

    Article  PubMed  Google Scholar 

  • Ekdale EG (2013) Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS ONE 8(6):1–100

    Article  Google Scholar 

  • Francis RC (1995) Evolutionary neurobiology. Tree 10(7):276–281

    CAS  PubMed  Google Scholar 

  • Franzen JL (1968) Revision der Gattung Palaeotherium Cuvier, 1804 (Palaeotheriidae, Perissodactyla, Mammalia). Dissertation, Albert-Ludwigs Universität zu Freiburg i, B:2 vol

  • Franzen JL (2010) The Rise of Horses: 55 Million Years of Evolution. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Froehlich DJ (1999) Phylogenetic systematics of basal perissodactyls. J Vertebr Paleontol 19(1):140–159

    Article  Google Scholar 

  • Gahr M, Sonnenschein E, Wickler W (1998) Sex difference in the size of the neural song control regions in a dueting songbird with similar song repertoire size of males and females. J Neurosci 18(3):1124–1131

    CAS  PubMed  Google Scholar 

  • Geisler JH, Luo Z (1996) The petrosal and inner ear of Herpetocetus sp. (Mammalia, Cetacea) and their implications for the phylogeny and hearing of archaic mysticetes. J Paleontol 70(6):1045–1066

    Google Scholar 

  • Gorgas M (1966) Betrachtung zur Hirnschädelkapazität zentralasiatischer Wildsäugetiere und ihrer Hausformen. Zool Anz 176:227–235

    Google Scholar 

  • Gunz P, Mitteroecker P, Bookstein FL (2005). Semilandmarks in three dimensions. In: Slice DE (ed) Modern Morphometrics in Physical Anthropology. Kluwer Academic/Plenum Publishers, New York, pp 73–98

    Chapter  Google Scholar 

  • Heffner RS, Heffner HE (1983) Hearing in large mammals: horses (Equus caballus) and cattle (Bos taurus). Behav Neurosci 97(2):299–309

    Article  Google Scholar 

  • Hooker JJ (1989) Character polarities in early perissodactyls and their signifiance for Hyracotherium and infraordinal relationships. In: Prothero DR, Schoch RM (eds) The Evolution of Perissodactyls. Oxford University Press, New York, pp 79–101

    Google Scholar 

  • Hooker JJ (1994) The beginning of the equoid radiation. Zool J Linn Soc 112:29–63

    Article  Google Scholar 

  • Horner JR, Goodwin MB (2009) Extreme cranial ontogeny in the upper Cretaceous dinosaur Pachycephalosaurus. PLoS ONE 4(10):1–11

    Article  Google Scholar 

  • Iwaniuk AN (2001) Interspecific variation in sexual dimorphism in brain size in Neartic ground squirrels (Spermophilus spp.). Can J Zool 79:759–765

    Article  Google Scholar 

  • Janis CM (1990) Correlation of cranial and dental variables with body size in ungulates and macropodoids. In: Damuth J, Macfadden BJ (eds) Body Size in Mammalian Paleobiology: Estimations and Biological Implications. Cambridge University Press, Cambridge, pp 255–299

    Google Scholar 

  • Jacobs LF (1996) Sexual selection and the brain. Trends Ecol Evol 11:82–86

    Article  CAS  PubMed  Google Scholar 

  • Jerison HJ (1973) Evolution of the Brain and Intelligence. Academic Press, New York, London

  • Jerison HJ (2007) Fossils, brains, and behaviour. In: Watanabe S, Hofman MA (eds) Integration of Comparative Neuranatomy and Cognition, Kei University Press, Tokyo, pp 13–31

    Google Scholar 

  • Kaufman JA, Turner GH, Holroyd PA, Rovero F, Grossman A (2013) Brain volume of the newly-discovered species Rhynchocyon udzungwensis (Mammalia, Afrotheria, Macroscelidea): implications for encephalization in sengis. PLoS ONE 8(3):1–7

    Article  Google Scholar 

  • Kruska D (1973) Cerebralisation, Hirnevolution und domestikationsbedingte Hirngröβenänderungen innerhalb der Ordnung Perissodactyla Owen, 1848 und ein Vergleich mit der Ordnung Artiodactyla Owen, 1848. Z Zool Syst Evol Forsch 11:81–103

    Article  Google Scholar 

  • Kruska D (1982) Hirngrössenänderungen bei Tylopoden während der Stammesgeschichte und in der Domestikation. Verh Zool Ges:173–183

  • Kruska D (1987) How fast can total brain size change in mammals. J Hirnforsch 28(1):59–70

    CAS  PubMed  Google Scholar 

  • Kruska D (1988) Effects of domestication on brain structure and behavior in mammals. Hum Evol 3(6):473–485

    Article  Google Scholar 

  • Kruska D (2005) On the evolutionary significance of encephalization in some eutherian mammals: effects of adaptative radiation, domestication and feralization. Brain Behav Evol 65:73–108

    Article  PubMed  Google Scholar 

  • Kruska D (2007) The effects of domestication on brain size. In: Krubitzer L, Kaas J (eds) Evolution of Nervous Systems. Vol. 3 Mammals. Academic Press, New York, pp 143–153

  • Ladevèze S (2006) Petrosal bones of metatherian mammals from the late Paleocene of Itaborai (Brazil), and a cladistic analysis of petrosal features in metatherians. Zool J Linn Soc 150:85–115

    Article  Google Scholar 

  • Lebrun R, de Leon MP, Tafforeau P, Zollikofer C (2010) Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J Anat 216:368–380

    Article  PubMed Central  PubMed  Google Scholar 

  • MacPhee RDE (1994) Morphology, adaptations and relationships of Plesiorycteropus, and a diagnosis of a new order of eutherian mammals. Bull Am Mus Nat Hist 220:1–214

    Google Scholar 

  • Macrini TE (2009) Description of a digital cranial endocast of Bathygenys reevesi (Merycoidodontidae; Oreodontidae) and implications for apomorphy-based diagnosis of isolated, natural endocasts. J Vertebr Paleontol 29(4):1199–1211

    Article  Google Scholar 

  • Macrini TE, Flynn JJ, Ni X, Croft DA, Wyss AR (2013) Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters. J Anat 223:442–461

    PubMed  Google Scholar 

  • Macrini TE, Rougier GW, Rowe T (2007a) Description of a cranial endocast from the fossil mammal Vincelestes neuquenianus (Theriiformes) and its relevance to the evolution of endocranial characters in therians. Anat Rec 290:875–892

    Article  Google Scholar 

  • Macrini TE, Rowe T, Vandeberg JL (2007b) Cranial endocasts from a growth series of Monodelphis domestica (Didelphidae, Marsupalia): a study of individual and ontogenic variation. J Morphol 268:844–865

    Article  PubMed  Google Scholar 

  • Manger PR, Pillay P, Maseko BC, Bhagwandin A, Gravett N, Moon D-J, Jillani N, Hemingway J (2009) Acquisition of brains from the African elephant (Lexodonta africana): perfusion-fixation and dissection. J Neurosci Methods 179:16–21

    Article  PubMed  Google Scholar 

  • Manoussaki D, Chadwick RS, Ketten DR, Arruda J, Dimitriadis EK, O’Malley JT (2008) The influence of cochlear shape on low-frequency hearing. Proc Natl Acad Sci USA 105(16):6162–6166

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manoussaki D, Dimitriadis EK, Chadwick RS (2006) Cochlea’s graded curvature effect on low frequency waves. Phys Rev Lett 96:1–4

    Article  Google Scholar 

  • Mohr E (1959) Das Urwildpferd Equus przewalskii Poliakov, 1881. Die Neue Brehm Bücherei, Ziemsen

    Google Scholar 

  • Novacek MJ (1982) The brain of Leptictis dakotensis, an Oligocene leptictid (Eutheria, Mammalia) from North America. J Paleontol 56(5):1177–1186

    Google Scholar 

  • Oakenfull EA, Lim HN, Ryder OA (2001) A survey of equid mitochondrial DNA: implications for the evolution, genetic diversity and conservation of Equus. Conserv Genet 1: 341–355

    Article  Google Scholar 

  • Oakenfull EA, Ryder OA (2002) Genetics of equid species and subspecies. In: Moehlman PD (ed) Equids: Zebras, Asses and Horses: Status Survey and Conservation Action Plan. World Conservation Union, pp 108–112

    Google Scholar 

  • O’Leary MA (2010) An anatomical and phylogenetic study of the osteology of the petrosal of extant and extinct artiodactylans (Mammalia) and relatives. Bull Am Mus Nat Hist 335:1–206

    Article  Google Scholar 

  • Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PLF, Fumagalli M, Vilstrup J, Raghavan M, Korneliussen T, Malaspinas A-S, Vogt J, Szklarczyk D, Kelstrup C, Vinther J, Dolocan A, Stenderup J, Velazquez AMV, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Roed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KAS, Ryder O, Anderson L, Mundy J, Krogh A, Gilbert MTP, Kjaer K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E (2013) Recalibrating Equus evolution using the genome sequence of an early middle Pleistocene horse. Nature 499:74–78

    Article  CAS  PubMed  Google Scholar 

  • Orliac MJ (2012) The petrosal bone of extinct Suoidea (Mammali, Artiodactyla). J Syst Paleontol:1–21

  • Orliac MJ, Benoit J, O’Leary MA (2012) The inner ear of Diacodexis, the oldest artiodactyl mammal. J Anat 221(5):417–426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Poliakov IS (1881) Sistematiceskij obzor polevok, vodjascichsja v cibri. Imperatorskoj Moscow, Akademii Nauk, Zapiski

    Google Scholar 

  • Plavcan JM, Schaik CP van (1998) Intrasexual competition and body weight dimorphism in anthropoid primates. Am J Phys Anthropol 103(1):37–68

  • Racicot RA, Colbert MW (2013) Morphology and variation in porpoise (Cetacea: Phocoenidae) cranial endocasts. The Anat Rec 296:979–992

    Article  Google Scholar 

  • Radinsky LB (1967) Relative brain size: a new measure. Science 155:836–838

    Article  CAS  PubMed  Google Scholar 

  • Radinsky LB (1974) The fossil evidence of anthropoid brain evolution. Am J Phys Anthropol 41(1):15–28

    Article  Google Scholar 

  • Radinsky LB (1976) Oldest horse brains: more advanced than previously realized. Science 194:626–627

    Article  CAS  PubMed  Google Scholar 

  • Remy JA (1967) Les Palaeotheridae (Perissodactyla) de la faune de mammifères de Fons 1 (Éocene Supérieur). Palaeovertebrata 1(1):1–46

    Article  Google Scholar 

  • Remy JA (1972) Étude du crâne de Pachynolophus lavocati n. sp. (Perissodacyla, Palaeotheriidae) des Phosphorites du Quercy. Palaeovertebrata 5(2):45–78

    Google Scholar 

  • Remy JA (1978) Description d’un moulage endocrânien de Plagiolophus minor (Palaeotheriidae, Perissodactyla). Mém Trav EPHE 5:1–17

    Google Scholar 

  • Remy JA (1998) Le genre Leptolophus : morphologie et histologie dentaires, anatomie crânienne, implications fonctionnelles. Palaeovertebrata 27(1–2):45–108

    Google Scholar 

  • Remy JA (2004) Le genre Plagiolophus (Palaeotheriidae, Perissodactyla, Mammalia) : Révision systématique, morphologie et histologie dentaires, anatomie crânienne, essai d’interprétation fonctionnelle. Palaeovertebrata 33(1–4):17–281

  • Röhrs M, Ebinger P (1993) Progressive und regressive Hirngrössenveränderungen bei Equiden. Z Zool Syst Evol Forsch 31:233–239

    Article  Google Scholar 

  • Röhrs M, Ebinger P (1998) Sind Zooprzewalskipferde Hauspferde? Berl Munch Tierarztl Wochenschr 111:273–280

    PubMed  Google Scholar 

  • Rowe T, Brochu CA, Colbert M, Merck JW, Kishi K, Saglamer E, Warren S (1999) Introduction to alligator: digital atlas of the skull. J Vertebr Paleontol 19(2):1–8

    Google Scholar 

  • Rowe T, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332:955–957

  • Saïdi S, Mende C (1999) L’utilisation des pelouses caussenardes par le cheval de Przewalski. Mappemonde 53(1):9–14

    Google Scholar 

  • Saini V, Srivastava R, Rai RK, Shamal SN, Singh TB, Tripathi SK (2012) Sex estimation from the mastoid process among North Indians. J Forensic Sci 57(2):434–439

    Article  PubMed  Google Scholar 

  • Savage DE, Russell DE, Louis P (1965) European Eocene Equidae (Perissodactyla). Univ Calif Publ Geol Sci 56:1–94

    Google Scholar 

  • Scannella JB, Horner JR (2010) Torosaurus Marsh, 1891, is Triceratops Marsh, 1889 (Ceratopsidae: Chasmosaurinae): synonymy through ontogeny. J Vertebr Paleontol 30(4):1157–1168

    Article  Google Scholar 

  • Shoshani J, Kupsky WJ, Marchant GH (2006) Elephant brain. Part 1: gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124–157

    Article  PubMed  Google Scholar 

  • Silcox MT, Dalmyn CK, Bloch, JI (2009) Virtual endocast of Ignacius graybullianus (Paromomyidae, Primates) and brain evolution in early Primates. Proc Natl Acad Sci USA 106(27):10987–10992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Simpson GG (1951) Horses: the Story of the Horse Family in the Modern World and through Sixty Million Years of History. Oxford University Press, New York

    Google Scholar 

  • Specht M (2007) Spherical surface parametrization and its application to geometric morphometric analysis of the braincase. Dissertation. University of Zürich

    Google Scholar 

  • Specht M, Lebrun R, Zollikofer C (2007) Visualizing shape transformation between chimpanzee and human braincases. Vis Comput 23:743–751

    Article  Google Scholar 

  • Towe AL, Mann MD (1995) Habitat-related variations in rain and body size of pocket gophers. J Brain Res 36(2):195–201

    CAS  Google Scholar 

  • Viret J (1958) Perissodactyla. In: Piveteau JM (ed) Traité de Paléontologie, Vol 6–2, pp. 368–475

  • Volf J (2003) Przewalskipferd -ein Wild- oder ein Haustier? Zool Garten 73:312–323

    Google Scholar 

  • Walker EP (1968) Mammals of the World. Johns Hopkins Press, Baltimore

    Google Scholar 

  • Weinberg R (1903) Fossile Hirnformen. I. Anchilophus desmareti. Z Wiss Zool 74:491–500

    Google Scholar 

  • Witmer L, Chatterjee S, Franzosa J, Rowe T (2003) Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425:950–953

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Kim CK, Lee K, et al. (2007) Resultant pressure distribution pattern along the basiliar membrane in the spiral shaped cochlea. J Biol Phys 33(3):195–211

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

First, we want to thank Claudia Feh and the TAKH association for the gracious loan of all the Przewalski skulls studied in this work and all information about the life of these individuals. CT scans of the Przewalski’s horses have been possible with the assistance of the CHU Lapeyronie (Montpellier), which provided the tomograph and the technicians. To scan the two freshly cut horse heads, we also appealed to a veterinarian, Laure Poujol (veterinary clinic of Celleneuve, Montpellier), for whose help we are grateful. We are very grateful to Renaud Lebrun from the University of Montpellier who trained one of us (LD) in the use of morphometric software. Finally, we thank the two anonymous reviewers who contributed to improving the manuscript. This work has been supported by the ANR funding project Palasiafrica. This is the publication ISEM n° 2015–051.

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Danilo, L., Remy, J., Vianey-Liaud, M. et al. Intraspecific Variation of Endocranial Structures in Extant Equus: A Prelude to Endocranial Studies in Fossil Equoids. J Mammal Evol 22, 561–582 (2015). https://doi.org/10.1007/s10914-015-9293-x

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