Journal of Mammalian Evolution

, Volume 20, Issue 3, pp 213–225 | Cite as

The Holes of Moles: Osteological Correlates of the Trigeminal Nerve in Talpidae

Original Paper


Talpidae consists of small insectivorous mammals exhibiting a range of environmental preferences. As all its members rely on a highly developed somatosensation system, they are an ideal study-group for investigating osteological correlates of the trigeminal nerve. We quantitatively studied cranial anatomy in 22 species of desman, shrew-mole, and true mole using microscopy and micro-CT imaging to investigate whether the infraorbital foramina within Talpidae is enlarged in semiaquatic forms and more broadly associated with habitat preference. We also investigated whether associated foramina were covariant. In order to account for a phylogenetic basis for any correlations, we reconstructed the best taxonomically sampled phylogeny for talpids in the literature to date, based on cytochrome b. Relationships among genera and species are broadly congruent with previous analyses; however, we report new placements for Neurotrichus gibbsii and Mogera tokudae. Although no correlation was found between habitat and the caliber of the V3 associated mandibular canal and foramen ovale, our results indicate that semiaquatic forms show larger infraorbital foramina in comparison to terrestrial species, and that the caliber of the sphenorbital fissure can also serve as a proxy for habitat preference. This work, therefore, supports the use of certain osteological features to infer habitat preferences in fossil species and indicates this can be achieved even when studying ecologically diverse, closely related species within the same family.


Ecological niche partitioning Micro-CT Morphology Osteology Talpidae Trigeminal nerve 



NC and RST thank Drs. Robert Asher, Adrian Friday, Lionel Hautier, and Stephanie Pierce for discussions during the development of this project and comments on the manuscript. Tom White and Russell Stebbings kindly provided USB microscopes for data collection. Alan Heaver (University of Cambridge) and Drs. Nikolay Karjilov and André Hilger (Helmholtz-Zentrum, Berlin) are thanked for their assistance during micro-CT scanning. Jacques Cuisin and Dr. Violaine Nicolas are thanked for the loan of specimens from the Muséum national d’Histoire naturelle (Paris), Matthew Lowe from the University Museum of Zoology, Cambridge, and Nora Lange and Dr. Oliver Hampe from the Museum für Naturkunde (Berlin). Dr. Peter Giere is thanked for granting access to the histological collection at the Museum für Naturkunde (Berlin). Access to the mammal stores of the British Museum of Natural History was facilitated by Louise Tomsett. Thanks go to Drs. Roger Benson and Stephen Montgomery for assistance calculating the influence of phylogenetic inertia. NC further thanks Anja Stadeler, Aodhan Butler, and Joe Flack for accommodation while visiting institutions. The manuscript was improved thanks to the helpful comments of two anonymous reviewers and Dr. John Wible. NC and RST are funded by the BBSRC. NC received support from the SYNTHESYS Project ( which is financed by European Community Research Infrastructure Action under the FP7 “Capacities” Program (DE-TAF-1108).

Supplementary material

10914_2012_9213_MOESM1_ESM.txt (34 kb)
ESM 1 (TXT 33 kb)


  1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics 11:36–42Google Scholar
  2. Angel JS, Mincer HH, Chaudhry J, Scarbecz M (2011) Cone-beam computed tomography for analysing variations in inferior alveolar canal location in adults in relation to age and sex. J Forensic Sci 56:216–219CrossRefPubMedGoogle Scholar
  3. Asher RJ (2007) A database of morphological characters and a combined-data reanalysis of placental mammal phylogeny. BMC Evol Biol 7:108CrossRefPubMedGoogle Scholar
  4. Ayers H (1884) On the structure and development of the nasal rays in Condylura cristata. Biol Zbl 4:356–360Google Scholar
  5. Blomberg SP, Lefevre JG, Wells JA, Waterhouse M (2012) Independent contrasts and PGLS regression estimators are equivalent. Syst Biol doi: 10.1093/sysbio/syr118
  6. Cabria MT, Rubines J, Gómez-Moliner B, Zardoya R (2006) On the phylogenetic position of a rare Iberian endemic mammal, the Pyrenean desman (Galemys pyrenaicus). Gene 375:1–13CrossRefPubMedGoogle Scholar
  7. Canestrelli D, Aloise G, Cecchetti S, Nascetti G (2010) Birth of a hotspot of intraspecific genetic diversity: notes from the underground. Mol Ecol 19:5432–5451CrossRefPubMedGoogle Scholar
  8. Carmona FD, Glösmann M, Ou J, Jiménez R, Collinson JM (2010a) Retinal development and function in a ‘blind’ mole. Proc R Soc Lond B Biol Sci 277:1513–1522CrossRefGoogle Scholar
  9. Carmona FD, Glösmann M, Ou J, Jiménez R, Collinson JM (2010b) Development of the cornea of true moles (Talpidea): morphogenesis and expression of PAX6 and cytokeratins. J Anat 217:488–500CrossRefPubMedGoogle Scholar
  10. Catania KC (1995) A comparison of the Eimer’s organs of three North American moles: the star-nosed mole (Condylura cristata) the hairy-tailed mole (Parascalops breweri) and the eastern mole (Scalopus aquaticus). J Comp Neurol 354:150–160CrossRefPubMedGoogle Scholar
  11. Catania KC (2000) Epidermal sensory organs of moles, shrew moles, and desmans: a study of the family Talpidae with comments on the function and evolution of Eimer’s organ. Brain Behav Evol 56:146–174CrossRefPubMedGoogle Scholar
  12. Catania KC, Kaas JH (1997) Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation. J Comp Neurol 387:215–233CrossRefPubMedGoogle Scholar
  13. Colangelo P, Bannikova AA, Krystufek B, Lebedev VS, Annesi F, Capanna E, Loy A (2010) Molecular systematics and evolutionary biogeography of the genus Talpa (Soricomorpha: Talpidae). Mol Phylogenet Evol 55:372–380CrossRefPubMedGoogle Scholar
  14. Cox PG (2008) A quantitative analysis of the eutherian orbit: correlations with masticatory apparatus. Biol Rev Camb Philos Soc 83:35–69PubMedGoogle Scholar
  15. Cox PG, Jeffery N (2011) Reviewing the morphology of the jaw-closing musculature in squirrels, rats, and guinea pigs with contrast-enhanced microCT. Anat Rec 294:915–928CrossRefGoogle Scholar
  16. Czech-Damal NU, Liebschner A, Miersch L, Klauer G, Hanke FD, Marshall C, Dehnhardt G, Hanke W (2011) Electroreception in the Guiana dolphin (Sotalia guianensis). Proc R Soc Lond B Biol Sci doi: 10.1098/rspb.2011.1127
  17. Ferretti MP, Debruyne R (2011) Anatomy and phylogenetic value of the mandibular and coronoid canals and their associated foramina in proboscideans (Mammalia). Zool J Linn Soc-Lond 161:391–413CrossRefGoogle Scholar
  18. Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364CrossRefGoogle Scholar
  19. Gingerich PD (1974) Size variability of the teeth in living mammals and the diagnosis of closely related sympatric fossil species. J Paleontol 48:895–903Google Scholar
  20. Grand TE, Gould E, Montali R (1998) Structure of the proboscis and rays of the star-nosed mole, Condylura cristata. J Mammal 79:492–501CrossRefGoogle Scholar
  21. Gregory WK (1910) The orders of mammals. Bull Am Mus Nat Hist 27:1–524Google Scholar
  22. Gustinna Wadu S, Penhall B, Townsend GC (1997) Morphological variability of the human inferior alveolar nerve. Clin Anat 10:82–87CrossRefGoogle Scholar
  23. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98Google Scholar
  24. Harvey PH, Pagel MD (1999) The Comparative Method in Evolutionary Biology. Oxford University Press, OxfordGoogle Scholar
  25. Hutterer R (2005) Order Soricomorpha. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: A Taxonomic and Geographic Reference. Volume 1. The John Hopkins University Press, Baltimore, pp 220–311Google Scholar
  26. Kawada S, Shinohara A, Yasuda M, Oda S, Liat LB (2003) The mole of Peninsular Malaysia: notes on its identification and ecology. Mammal Study 28:73–77CrossRefGoogle Scholar
  27. Kielan-Jaworowska Z, Cifelli R, Luo Z-X (2004) Mammals from the Age of Dinosaurs. Origins, Evolution and Structure. Columbia Universtiy Press, New YorkGoogle Scholar
  28. Kieser JA, Paulin M, Law B (2004) Intrabony course of the inferior alveolar nerve in the edentulous mandible. Clin Anat 17:107–111CrossRefPubMedGoogle Scholar
  29. Kilic C, Kamburog lu K, Ozen T, Balcioglu HA, Kurt B, Kutoglu T, Ozan H (2010) The position of the mandibular canal and histologic feature of the inferior alveolar nerve. Clin Anat 23:34–42PubMedGoogle Scholar
  30. Kovisto T, Ahmad M, Bowles WR (2011) Proximity of the mandibular canal to the tooth apex. J Endodont 37:311–315CrossRefGoogle Scholar
  31. Ladevèze S, Muizon C, Colbert M, Smith T (2010) 3D computational imaging of the petrosal of a new multiturberculate mammal from the Late Cretaceous of China and its paleobiological inferences. C R Palevol 9:319–330CrossRefGoogle Scholar
  32. Luo Z-X (2007) Transformation and diversification in early mammal evolution. Nature 450:1011–1019CrossRefPubMedGoogle Scholar
  33. Luo Z-X, Wible JR (2005) A Late Jurassic digging mammal and early mammalian diversification. Science 308:103–107CrossRefPubMedGoogle Scholar
  34. Macrini TE, Rowe T, VandeBerg JL (2007) Cranial endocasts from a growth series of Monodelphis domestica (Didelphidae, Marsupialia): a study of individual and ontogenetic variation. J Morphol 268:844–865CrossRefPubMedGoogle Scholar
  35. Marasco PD, Tsuruda PR, Bautista DM, Julius D, Catania KC (2006) Neuroanatomical evidence for segregation of nerve fibers conveying light touch and pain sensation in Eimer’s organ of the mole. Proc Natl Acad Sci USA 103:9339–9344CrossRefPubMedGoogle Scholar
  36. McDowell SB (1958) The greater Antillean insectivores. Bull Am Mus Nat Hist 115:113–214Google Scholar
  37. Meegaskumbura SH, Meegaskumbura MPB, Pethiyagoda R, Manamendra-Arachchi K, Schneider CJ (2007) Crocidura hikmiya, a new shrew (Mammalia: Soricomorpha: Soricidae) from Sri Lanka. Zootaxa 1665:19–30Google Scholar
  38. Motokawa M (2004) Phylogenetic relationships within the family Talpidae (Mammalia: Insectivora). J Zool 263:147–157CrossRefGoogle Scholar
  39. Muchlinski MN (2008) The relationship between the infraorbital foramen, infraorbital nerve, and maxillary mechanoreception: implications for interpreting the paleoecology of fossil mammals based on infraorbital foramen size. Anat Rec 291:1221–1226CrossRefGoogle Scholar
  40. Muchlinski MN (2010a) A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals. J Hum Evol 58:447–473CrossRefPubMedGoogle Scholar
  41. Muchlinski MN (2010b) Ecological correlates of infraorbital foramen area in primates. Am J Phys Anthropol 141:131–141PubMedGoogle Scholar
  42. Nowak RM (1999) Walker’s Mammals of the World, Sixth Edition Volume 1. John Hopkins, Baltimore and LondonGoogle Scholar
  43. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala UniversityGoogle Scholar
  44. Pettigrew JD (1999) Electroreception in monotremes. J Exp Biol 202:1447–1454PubMedGoogle Scholar
  45. Phillips MJ, Bennett TH, Lee MSY (2009) Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proc Natl Acad Sci USA 106:17089–17094CrossRefPubMedGoogle Scholar
  46. Polland KE, Munro S, Reford G, Lockhart A, Logan G, Brocklebank L, McDonald SW (2001) The mandibular canal of the edentulous jaw. Clin Anat 14:445–452CrossRefPubMedGoogle Scholar
  47. Quilliam TA (1966) The mole’s sensory apparatus. J Zool 149:76–88CrossRefGoogle Scholar
  48. Rambaut A, Drummond AJ (2009) Tracer v1.5. Available from
  49. Robinson CA, Williams FL (2010) Quantifying mental foramen position in extant hominoids and Australopithecus: implications for its use in studies of human evolution. Anat Rec 293:1337–1349CrossRefGoogle Scholar
  50. Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160PubMedGoogle Scholar
  51. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  52. Rowe T, Rich TH, Vickers-Rich P, Springer M, Woodburne MO (2008) The oldest platypus and its bearing on divergence timing of the platypus and echidna clades. Proc Natl Acad Sci USA 105:1238CrossRefPubMedGoogle Scholar
  53. Rowe TB, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332:955–957CrossRefPubMedGoogle Scholar
  54. Ruf I, Luo Z-X, Wible JR, Martin T (2009) Petrosal anatomy and inner ear structures of the Late Jurassic Henkelotherium (Mammalia, Cladotheria, Dryolestoidea): insight into the early evolution of the ear region in cladotherian mammals. J Anat 214:679–693CrossRefPubMedGoogle Scholar
  55. Sánchez-Villagra MR, Asher RJ (2002) Cranio-sensory adaptations in small faunivorous semiaquatic mammals, with special reference to olfaction and the trigeminal system. Mammalia 66:93–109CrossRefGoogle Scholar
  56. Sánchez-Villagra MR, Horovitz I, Motokawa M (2006) A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships. Cladistics 22:59–88CrossRefGoogle Scholar
  57. Sánchez-Villagra MR, Wible JR (2002) Patterns of evolutionary transformation in the petrosal bone and some basicranial features in marsupial mammals, with special reference to didelphids. J Zool Syst Evol Res 40:26–45CrossRefGoogle Scholar
  58. Saveliev SV (2008) Neurobiological approaches in vertebrate paleontology. Paleontol J 42:573–580CrossRefGoogle Scholar
  59. Shinohara A, Campbell KL, Suzuki H (2003) Molecular phylogenetic relationships of moles, shrew moles, and desmans from the New and Old Worlds. Mol Phylogenet Evol 27:247–258CrossRefPubMedGoogle Scholar
  60. Shinohara A, Suzuki H, Tsuchiya K, Zhang Y-P, Luo J, Jiang X-L, Wang Y-X, Campbell KL (2004) Evolution and biogeography of talpid moles from continental East Asia and the Japanese islands inferred from mitochondrial and nuclear gene sequences. Zool Sci 21:1177–1185CrossRefPubMedGoogle Scholar
  61. Shinohara A, Kawada S, Harada M, Koyasu K, Oda S, Suzuki H (2008) Phylogenetic relationships of the short-faced mole, Scaptochirus moschatus (Mammalia: Eulipotyphla), among Eurasian fossorial moles, as inferred from mitochondrial and nuclear gene sequences. Mammal Study 33:77–82CrossRefGoogle Scholar
  62. Silva M, Downing JA (1995) CRC Handbook of Mammalian Body Masses. CRC Press, Boca RatonGoogle Scholar
  63. Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman and Company, New YorkGoogle Scholar
  64. Tsuchiya K, Suzuki H, Shinohara A, Harada M, Wakana S, Sakaizumi M, Han S-H, Lin L-K, Kryukov AP (2000) Molecular phylogeny of East Asian moles inferred from the sequence variation of the mitochondrial cytochrome b gene. Genes Genet Syst 75:17–24CrossRefPubMedGoogle Scholar
  65. Whidden HP (2000) Comparative myology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla). Am Mus Novitates 3294:1–54CrossRefGoogle Scholar
  66. Witmer LM, Ridgely RC (2009) New insights into the brain, braincase, and ear region of tyrannosaurs (Dinosauria, Theropoda), with implications for sensory organization and behavior. Anat Rec 292:1266–1296CrossRefGoogle Scholar
  67. Yates TL, Moore DW (1990) Speciation and evolution in the family Talpidae (Mammalia: Insectivora). In: Nevo E, Reig OA (eds) Evolution of Subterranean Mammals at the Organismal and Molecular Levels. Alan R. Liss, New York, pp 1–22Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK

Personalised recommendations