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New Virtual Endocasts of Eocene Ischyromyidae and Their Relevance in Evaluating Neurological Changes Occurring Through Time in Rodentia

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Abstract

Little is known about the early evolution of the brain in rodents. We report on nine new virtual endocasts for one of the most primitive family of rodents, Ischyromyidae, based on five specimens of Pseudotomus and Notoparamys (Paramyinae) and four specimens of Reithroparamys and Rapamys (Reithroparamyinae), dating from the early Eocene to the late middle Eocene of North America (Colorado, Wyoming, Utah and Montana). The virtual endocasts were obtained from high-resolution X-ray micro-computed tomography data. Comparisons with previously described ischyromyid virtual endocasts allow us to make inferences about the ancestral condition of the brain in rodents. Since Reithroparamyinae are suggested to be more closely related to the squirrel-related clade than other Ischyromyidae, comparisons were also made with the oldest virtual endocast for a squirrel, which gave us the opportunity to look at finer neurological changes occurring in the early evolution of squirrels. These new data permit a preliminary assessment of the endocranial diversity in Ischyromyidae. The results do not show evidence for a clear increase in Encephalization Quotient through time for early rodents. Instead, variation among species could be due to ecological factors (e.g., locomotion). Significant expansion in the neocortex and increase in paraflocculi ratios may have occurred in the transition from Ischyromyidae to Sciuridae, as previously hypothesized. Large olfactory bulbs and exposed midbrain are inferred to have been features present in the common ancestor of rodents, while neocortical expansion is reconstructed as having occurred twice independently within Ischyromyidae.

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References

  • Anderson D (2008) Ischyromyidae. In: Janis CM, Gunnell GF, Uhen MD (eds) Evolution of Tertiary Mammals of North America, Volume 2. Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, Cambridge, pp 311-325

    Chapter  Google Scholar 

  • Bhagat R, Bertrand OB, Silcox MT (2017) Locomotor behavior reconstruction from the semicircular canals of early fossil rodents: insights into major evolutionary transitions from the inner ear. J Vertebr Paleontol: 80-81

  • Bertrand OC, Amador-Mughal F, Silcox MT (2016a) Virtual endocasts of Paramys (Paramyinae): oldest endocranial record for Rodentia and early brain evolution in Euarchontoglires. Proc R Soc Lond [Biol] 283 (2316):1–8. https://doi.org/10.1098/rspb.2015.2316

  • Bertrand OC, Amador-Mughal F, Silcox MT (2017) Virtual endocast of the early Oligocene Cedromus wilsoni (Cedromurinae) and brain evolution in squirrels. J Anat 230:128–151. https://doi.org/10.1111/joa.12537

    Article  PubMed  Google Scholar 

  • Bertrand OC, Schillaci MA, Silcox MT (2016b) Cranial dimensions as estimators of body mass and locomotor habits in extant and fossil rodents. J Vertebr Paleontol 36:1–10. https://doi.org/10.1080/02724634.2015.1014905

    Article  Google Scholar 

  • Bertrand OC, Silcox MT (2016) First virtual endocasts of a fossil rodent: Ischyromys typus (Ischyromyidae) and brain evolution in rodents. J Vertebr Paleontol 36:1–19. https://doi.org/10.1080/02724634.2016.1095762

    Article  Google Scholar 

  • Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D (2009) Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol 9:1–71. https://doi.org/10.1186/1471-2148-9-71

    Article  CAS  Google Scholar 

  • Bloch JI (2001) Mammalian paleontology of freshwater limestones from the Paleocene-Eocene of the Clarks Fork Basin, Wyoming. Dissertation, University of Michigan, Ann Abor

  • Boyer DM, Kaufman S, Gunnell GF, Rosenberger AL, Delson E (2014) Managing 3D digital data sets of morphology: Morphosource is a new project-based data archiving and distribution tool. Am J Phys Anthropol 153(Suppl 58):84

    Google Scholar 

  • Brauer K, Schober W (1970) Katalog der Säugetiergehirne. Catalogue of Mammalian Brains. Gustav Fischer, Jena

  • Bugge J (1985) Systematic value of the carotid arterial pattern in rodents. In: Luckett WP, Hartenberger J-L (eds) Evolutionary Relationships Among Rodents: A Multidisciplinary Approach. Plenum Press, New York, pp 355–379

    Chapter  Google Scholar 

  • Cerminara NL, Apps R (2011) Behavioural significance of cerebellar modules. Cerebellum 10:484–494. https://doi.org/10.1007/s12311-010-0209-2

    Article  PubMed  Google Scholar 

  • Christensen GC, Evans HE (1979) Miller’s Anatomy of the Dog, 2nd ed. W.B. Saunders, Philadelphia

    Google Scholar 

  • Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J (2010) Rodent evolution: back to the root. Mol Biol Evol 276:1315–1326. https://doi.org/10.1093/molbev/msq019

    Article  CAS  Google Scholar 

  • Cope ED (1872) Second account of new Vertebrata from the Bridger Eocene. Proc Am Philos Soc 12:466–468

    Google Scholar 

  • Dawson MR (2003) Paleogene rodents of Eurasia. In: Reumer JWF, Wessels W (eds) Distribution and Migration of Tertiary Mammals in Eurasia. A volume in honour of Hans de Bruijn. Deinsea 10: 97–126.

  • Dozo MT (1997) Paleoneurologıa de Dolicavia minuscula (Rodentia, Caviidae) y Paedotherium insigne (Notoungulata, Hegetotheriidae) del Plioceno de Buenos Aires, Argentina. Ameghiniana 34:427–435

    Google Scholar 

  • Dozo MT, Martínez G (2016) First digital cranial endocasts of late Oligocene Notohippidae (Notoungulata): implications for endemic South American ungulates brain evolution. J Mamm Evol 23:1–16. https://doi.org/10.1007/s10914-015-9298-5

    Article  Google Scholar 

  • Dunn RH, Rasmussen DT (2007) Skeletal morphology and locomotor behavior of Pseudotomus eugenei (Rodentia, Paramyinae) from the Uinta Formation, Utah. J Vertebr Paleontol 27:987-1006. https://doi.org/10.1671/0272-4634(2007)27[987:SMALBO]2.0.CO;2

  • Edinger T (1964) Midbrain exposure and overlap in mammals. Am Zool 4:5–19.

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg JF (1981) The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation, and Behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Eisenberg JF, Wilson DE (1978) Relative brain size and feeding strategies in the Chiroptera. Evolution 32:740–751

    Article  PubMed  Google Scholar 

  • Emry RJ, Thorington RW Jr (1982) Descriptive and comparative osteology of the oldest fossil squirrel, Protosciurus (Rodentia: Sciuridae). Smithson Contrib Paleobiol 47: 1–35

    Article  Google Scholar 

  • Fabre PH, Hautier L, Dimitrov D, Douzery EJ (2012) A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol 12:1–19. https://doi.org/10.1186/1471-2148-12-88

    Article  Google Scholar 

  • Falk D (2007) Evolution of the primate brain. In: Henke W, Tattersall I (eds) Handbook of Paleoanthropology, vol. 2. Springer, Heidelberg, pp 1133–1162

    Chapter  Google Scholar 

  • Flynn LJ, Jacobs LL, Cheema IU (1986) Baluchimyinae, a new ctenodactyloid rodent subfamily from the Miocene of Baluchistan. Am Mus Novit 2841:1–58

    Google Scholar 

  • Gingerich PD, Gunnell GF (2005) Brain of Plesiadapis cookei (Mammalia, Proprimates): surface morphology and encephalization compared to those of primates and Dermoptera. Contrib Mus Paleontol Univ Michigan 31:185–195

    Google Scholar 

  • Gurche JA (1982) Early primate brain evolution. In: Armstrong E, Falk D (eds) Primate Brain Evolution: Methods and Concepts. Plenum Press, New York, pp 227–246

    Chapter  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Harrington AR, Silcox MT, Yapuncich GS, Boyer DM, Bloch JI (2016) First virtual endocasts of adapiform primates. J Hum Evol 99:52–78. https://doi.org/10.1016/j.jhevol.2016.06.005

    Article  PubMed  Google Scholar 

  • Hofman MA (1983) Encephalization in hominids: evidence for the model of punctuationalism. Brain Behav Evol 122:102–117

    Article  Google Scholar 

  • Howell AB (1944) Speed in Animals. University of Chicago Press, Chicago

    Google Scholar 

  • Janis CM, Gunnell GF, Uhen MD (2008) Evolution of Tertiary Mammals of North America, Volume 2. Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, Cambridge

    Book  Google Scholar 

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

    Google Scholar 

  • Jerison HJ (2012) Digitized fossil brains: neocorticalization. Biol Ther Dent 6:383–392

    Google Scholar 

  • Korth WW (1985) The rodents Pseudotomus and Quadratomus and the content of the tribe Manitshini (Paramyinae, Ischyromyidae). J Vertebr Paleontol 5:139–152

    Article  Google Scholar 

  • Korth WW (1994) The Tertiary Record of Rodents in North America. Plenum Press, New York

    Book  Google Scholar 

  • Korth WW, Emry RJ (1991) The skull of Cedromus and a review of the Cedromurinae (Rodentia, Sciuridae). J Paleontol 65:984–994

    Article  Google Scholar 

  • Krubitzer L, Campi KL, Cooke DF (2011) All rodents are not the same: a modern synthesis of cortical organization. Brain Behav Evol 78:51–93. https://doi.org/10.1159/000327320

  • Leidy J (1871) Notice of some extinct rodents. Proc Acad Nat Sci Philadelphia 22:230–232

    Google Scholar 

  • Long A, Bloch JI, Silcox MT (2015) Quantification of neocortical ratios in stem primates. Am J Phys Anthropol 157:363–373. https://doi.org/10.1002/ajpa.22724

    Article  PubMed  Google Scholar 

  • Mace GM, Harvey PH, Clutton-Brock TH (1981) Brain size and ecology in small mammals. J Zool 193:333–354

    Article  Google Scholar 

  • Macrini TE, Rougier GW, Rowe T (2007) 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, Archer M (2006) Description of a cranial endocast from a fossil platypus, Obdurodon dicksoni (Monotremata, Ornithorhynchidae), and the relevance of endocranial characters to monotreme monophyly. J Morphol 267:1000–1015

    Article  PubMed  Google Scholar 

  • Marivaux L, Vianey-Liaud MO, Jaeger JJ (2004) High-level phylogeny of early Tertiary rodents: dental evidence. Zool J Linn Soc 142:105–134

    Article  Google Scholar 

  • Marsh OC (1872) Preliminary description of new Tertiary mammals. Am J Sci 4:202–224

    Article  Google Scholar 

  • Martin RD (1990) Primate Origins and Evolution: A Phylogenetic Reconstruction. Chapman and Hall, London

    Google Scholar 

  • Matthew WD (1910) On the osteology and relationships of Paramys and the affinities of the Ischyromyidae. Bull Am Mus Nat Hist 28:43–71

    Google Scholar 

  • Meier P (1983) Relative brain size within the North American Sciuridae. J Mammal 64:642–647. https://doi.org/10.2307/1380520

    Article  Google Scholar 

  • Meng J (1990) The auditory region of Reithroparamys delicatissimus (Mammalia, Rodentia) and its systematic implications. Am Mus Novit 2972:1–35

    Google Scholar 

  • Meng J, Hu Y, Li C (2003) The osteology of Rhombomylus (Mammalia, Glires): implications for phylogeny and evolution of Glires. Bull Am Mus Nat Hist 275:1–247. https://doi.org/10.1206/0003-0090(2003)275,0001:TOORMG.2.0.CO;2

    Article  Google Scholar 

  • Michaux J (1968) Les Paramyidae (Rodentia) de l’Éocène inférieur du Bassin de Paris. Palaeovertebrata 1:135–193

  • Novacek MJ (1986) The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bull Am Mus Nat Hist 183:1–112

    Google Scholar 

  • O'Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo Z-X, Meng J, Ni X, Novacek MJ, Perini FA, Randall ZS, Rougier GW, Sargis EJ, Silcox MT, Simmons NB, Spaulding M, Velazco PM, Weksler M, Wible JR, Cirranello AL (2013) The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339:662–667

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Orliac MJ, Ladevèze S, Gingerich PD, Lebrun R, Smith T (2014) Endocranial morphology of Palaeocene Plesiadapis tricuspidens and evolution of the early primate brain. Proc R Soc Lond (Biol) 281:2013–2792

    Article  Google Scholar 

  • Pilleri G, Gihr M, Kraus C (1984) Cephalization in rodents with particular reference to the Canadian beaver (Castor canadensis). In: Pilleri G (ed) Investigations on Beavers. Brain Anatomy Institute, Berne, pp 11–102

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (2002) Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J Neurophysiol 87:912–924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramdarshan A, Orliac MJ (2015) Endocranial morphology of Microchoerus erinaceus (Euprimates, Tarsiiformes) and early evolution of the Euprimates brain. Am J Phys Anthropol 159:5–16. https://doi.org/10.1002/ajpa.22868

    Article  PubMed  Google Scholar 

  • Rasband WS (1997–2014) ImageJ. U. S. National Institutes of Health, Bethesda. Available at: http://imagej.nih.gov/ij/. Accessed 10 June 2013.

  • Rocha RG, Leite YLR, Costa LP, Rojas D (2016) Independent reversals to terrestriality in squirrels (Rodentia: Sciuridae) support ecologically mediated modes of adaptation. J Evol Biol 29:2471–2479. https://doi.org/10.1111/jeb.12975

    Article  CAS  PubMed  Google Scholar 

  • Rose KD, Chinnery BJ (2004) The postcranial skeleton of early Eocene rodents. Bull Carnegie Mus Nat Hist 36:211–244

    Article  Google Scholar 

  • Rose KD, von Koenigswald W (2007) The marmot-sized paramyid rodent Notoparamys costilloi from the early Eocene of Wyoming, with comments on dental variation and occlusion in paramyids. Bull Carnegie Mus Nat Hist 39:111–125. https://doi.org/10.2992/0145-9058(2007)39[111:TMPRNC]2.0.CO;2

    Article  Google Scholar 

  • Roth VL, Thorington RW (1982) Relative brain size among African squirrels. J Mammal 63:168–173

    Article  Google Scholar 

  • Scott WB, Osborn HF (1887) Preliminary report on the vertebrate fossils of the Uinta formation, collected by the Princeton Expedition of 1886. Proc Am Phil Soc 24:255–264

  • Silcox MT, Benham AE, Bloch JI (2010) Endocasts of Microsyops (Microsyopidae, Primates) and the evolution of the brain in primitive primates. J Hum Evol 58:505–521

    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 106:10987–10992

    Article  PubMed  Google Scholar 

  • Silcox MT, Dalmyn CK, Hrenchuk A, Bloch JI, Boyer DM, Houde P (2011) Endocranial morphology of Labidolemur kayi (Apatemyidae, Apatotheria) and its relevance to the study of brain evolution in Euarchontoglires. J Vertebr Paleontol 31:1314–1325

    Article  Google Scholar 

  • Sillitoe RV, Marzban H, Larouche M, Zahedi S, Affanni J, Hawkes R (2005) Conservation of the architecture of the anterior lobe vermis of the cerebellur across mammalian species. Prog Brain Res 148:283–297

    Article  PubMed  Google Scholar 

  • Visualization Sciences Group (1995–2010) AVIZO® 6.2.0 Konrad-Zuse-Zentrum für Informationstechnik, Berlin (ZIB), Germany

  • Visualization Sciences Group (1995–2012) AVIZO® 7.0.1 Konrad-Zuse-Zentrum für Informationstechnik, Berlin (ZIB), Germany

  • Visualization Sciences Group (1995–2014) AVIZO® 8.1.1 Konrad-Zuse-Zentrum für Informationstechnik, Berlin (ZIB), Germany

  • Visualization Sciences Group (1995–2015) AVIZO® 9.0.1 Konrad-Zuse-Zentrum für Informationstechnik, Berlin (ZIB), Germany

  • Wahlert JH (1974) The cranial foramina of protrogomorphous rodents; an anatomical and phylogenetic study. Bull Mus Comp Zool 146:363–410

    Google Scholar 

  • Wahlert JH (2000) Morphology of the auditory region in Paramys copei and other Eocene rodents from North America. Am Mus Novit 3307:1–16. https://doi.org/10.1206/0003-0082(2000)307,0001:MOTARI.2.0.CO;2

    Article  Google Scholar 

  • Wahlert JH, Korth WW, McKenna MC (2006) The skull of Rapamys (Ischyromyidae, Rodentia) and description of a new species from the Duchesnean (late middle Eocene) of Montana. Palaeontogr Abt A 26:39–51

    Google Scholar 

  • Wible JR (1987) The eutherian stapedial artery: character analysis and implications for superordinal relationships. Zool J Linnean Soc 91:107–135

    Article  Google Scholar 

  • Wible JR, Rougier GW (2000) Cranial anatomy of Kryptobaatar dashzevegi (Mammalia, Multituberculata), and its bearing on the evolution of mammalian characters. Bull Am Mus Nat Hist 247:1–120

    Article  Google Scholar 

  • Wible JR, Wang Y, Li C, Dawson MR (2005) Cranial anatomy and relationships of a new ctenodactyloid (Mammalia, Rodentia) from the early Eocene of Hubei Province, China. Ann Carnegie Museum 74:91–150. https://doi.org/10.2992/0097-4463(2005)74[91:CAAROA]2.0.CO;2

  • Wilson RW (1949) Additional Eocene rodent material from southern California. Carnegie Inst Wash Publ 584:1–25

    Google Scholar 

  • Wood AE (1937) The mammalian fauna of the White River Oligocene. Part II. Rodentia. Trans Am Philos Soc 28:157–269

    Google Scholar 

  • Wood AE (1962) The early Tertiary rodents of the family Paramyidae. Trans Am Philos Soc 52:1–261

    Article  Google Scholar 

  • Wood AE (1974) Early Tertiary vertebrate faunas Vieja Group Trans-Pecos Texas: Rodentia. Bull Texas Mem Mus 21:1–112

    Google Scholar 

  • Wood AE (1976) The paramyid rodent Ailuravus from the Middle and Late Eocene of Europe, and its relationships. Palaeovertebrata 7:117-149

  • Yao L, Brown JP, Stampanoni M, Marone F, Isler K, Martin RD (2012) Evolutionary change in the brain size of bats. Brain Behav Evol 80:15–25. https://doi.org/10.1159/000338324

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank D. Bohaska and N.D. Pyenson from the Paleobiology Department of the Smithsonian (NMNH), J. Meng and R. O’Leary from the American Museum of Natural History (AMNH), as well as D. Brinkman, M. Fox, and Chris Norris from the Yale Peabody Museum for providing access to the specimen to be scanned. The authors also thank J. Thostenson and D.M. Boyer for facilitating the scanning of the specimens at the SMIF (Duke University). We also thank M. Hill from the AMNH Microscopy and Imaging Facility for scanning the specimens. Thank you to E. Seiffert for fruitful discussions and for providing very generous access to resources in his lab. This research was supported by an NSERC Discovery Grant to MTS, School of Graduate Studies Travel Grant from the University of Toronto, and a Research Expenses Grant from the Department of Anthropology (University of Toronto) to OCB. The authors also thank two anonymous reviewers for comments that improved the paper.

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OCB and MTS both contributed to conception and design of the study. OCB acquired the CT data, FAM and MML segmented out the fossil specimens in order to obtain the endocasts. OCB and MTS carried out the analyses and interpretations of the data. OCB drafted the article, and OCB, MML, and MTS revised it critically for important intellectual content. All authors gave final approval before submission.

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Correspondence to Ornella C. Bertrand.

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Bertrand, O.C., Amador-Mughal, F., Lang, M.M. et al. New Virtual Endocasts of Eocene Ischyromyidae and Their Relevance in Evaluating Neurological Changes Occurring Through Time in Rodentia. J Mammal Evol 26, 345–371 (2019). https://doi.org/10.1007/s10914-017-9425-6

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