First comparison of the bony labyrinths of some fossil hedgehogs (Erinaceomorpha, Mammalia) using high-resolution computed

tomography: phylogenetic implications and perspectivesMaridet, O.[1], Costeur, L.[2], Schwarz, C.[3], Furió, M.[4], van Glabbeek, F.M.[5] and Hoek Ostende, L.W.[5]

[1]Geologie und Paläontologie Abt., Naturhistorisches Museum Wien, Vienna, Austria; [2]Geowissenschaften Abt., Naturhistorisches Museum Basel, Basel, Switzerland; [3]Paläontologie Abt., Universität Wien, Vienna, Austria; [4]Institut Català de Paleontologia, Universitat Autònoma de Barcelona, Barcelona, Spain; [5]Naturalis Biodiversity Center, Leiden, The Netherlands

INTRODUCTION: The Erinaceidae family comprises the extant spiny hedgehogs (Erinaceinae, Fig. 1A-C) and the hairy hedgehogs, also called Moonrats (Galericinae, Fig. 1D-F). The oldest records of this family are the genera Tetracus Aymard, 1850 and Neurogymnurus Filhol, 1877 from the Early Oligocene of Europe. Due to their well-developed third upper molars and the shape of the premolars, these genera are usu-ally assigned to the Galericinae, although their phyletic relationships with the extant representatives of this subfamily remain unknown. Amph-echinus arvernensis (Blainville, 1839) from the latest Oligocene of France [1] is the earliest fossil species assigned to the Erinaceinae in this study (but they are known since the Early Oligocene in the fossil record of Asia, [2]). Both subfamilies coexist in the European fossil record until the end of the mid Pliocene. Nowadays, the subfamily Galericinae is restricted to Southeastern Asia whereas Erinaceines are present in Africa, Europe and Asia (also in New Zealand where they have been introduced by humans).

Although the extant members of this family are well-known, their phylogenetic relationships and their position among the phylogeny of mam-mals, especially among Eulipotyphla, remain controversial [e.g., 3,4,5]. Furthermore, the evolutionary history of Erinaceidae, especially the separation between the two extant subfamilies remains poorly understood (Fig. 2, [5,6]). The fossil representatives are rarely taken into account, and when they are, the studies mainly focus on the dentition and jaws although their morphology is strongly influenced by the ecology/dietary habits.

CONCLUSION AND PERSPECTIVES: The phylogeny (Fig. 5) confirms that Soricidae constitute a primitive clade with regard to Erinaceidae, and that all fossil and extant taxa ascribed to the Erinaceinae form indeed a monophyletic clade. Also, in accordance with the fossil record, the Erina-ceinae clade represents the most apomorphic trait. However, all taxa pre-viously ascribed to Galericinae seem to constitute a polyphyletic clade. The basal position of Echinosorex within Erinaceidae indicate that its clade might has evolved in Asia independently from European taxa.

This preliminary analysis emphasizes the potential of inner ear morphol-ogy to better understand the evolutionary history of Erinaceidae. Further analyses including more taxa and taking into account the morphology of the petrosal bone and the dentition will be necessary to fully understand the differentiation between the two extant subfamilies and their relation-ships with other Eulipotyphla.

REFERENCES:1. Mein, P. (1989). Updating of MN zones. In: E. Lindsay, V. Fahlbusch, P. Meins (Eds.), European Neogene Mammal Chronology. NATO Advanced

Study Institut Series, 180 Serie A, pp. 73–90.2. Ziegler, R., Dahlmann, T. and Storch, G. (2007). Marsupialia, Erinaceomorpha and Soricomorpha (Mammalia). In: G. Daxner-Höck (Editor),

Oligocene-Miocene Vertebrates from the Valley of Lakes (Central Mongolia): Morphology, phylogenetic and stratigraphic implications. Annalen des Naturhistorischen Museum in Wien, 108A: 53-164.

3. Meredith, R.W., et al. (2011). Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science, 334: 521-524.

4. Bininda-Emonds, O.R.P., et al. (2007). The delayed rise of present-day mammals. Nature, 446: 507-511.5. He, K., et al. (2012). An Estimation of Erinaceidae Phylogeny: A combined analysis approach. PLoS ONE, 7(6): e39304.6. van den Hoek Ostende, L.W. (2001). A revised generic classification of the Galericini (Insectivora, Mammalia) with some remarks on their palaeo-

biogeography and phylogeny. Geobios, 34(6): 681-695.7. Ni, X., et al. (2012). Imaging the inner ear in fossil mammals: High-resolution CT scanning and 3-D virtual reconstructions. Palaeontologia Elec-

tronica, 15(2): 18A.8. Ekdale, E. (2013). Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS ONE, 8(6): e66624.

3D RECONSTRUCTION : Thanks to high-resolution computed tomography it is now possible to virtually study the inner morphology of skulls in a non-destructive way (Fig. 3). The bony labyrinth is constituted by the organs of hearing and bal-ance and is situated within the petrosal bone. It is a fine and complex network of canals known to bear meaningful system-atic and phylogenetic information [e.g., 7,8]. The endocast of the bony labyrinth is obtained by segmenting the original CT images to produce accurate 3D virtual reconstructions [7].

ANATOMICAL COMPARISONS: For the first time, we reconstruct the bony labyrinth of four European fossil hedgehogs and three extant hedgehog skulls (Fig. 4). Used as outgroup in the following cladistic analysis, we also reconstructed the bony labyrinth of Solenodon paradoxus (Brandt, 1833). For Atelerix albiventris Wagner, 1841 and Sorex monticolus Mer-riam, 1890, we used the reconstructions of Ekdale [8].

CLADISTIC ANALYSIS: A tentative cladistic analysis is performed based on the morphology of the bony labyrinth, in order to asses the potential contribution of these characteriscs to our understanding of Erinaceidae evolutionary history. In addi-tion to the Erinaceidae taxa, Sorex monticolus (Soricidae) is used to assess the position of Erinaceidae among Eulipotyphla. 14 morphological characters are scored from the 10 inner ears resulting in one most parsimonious tree (Fig.5).

Fig. 3 - Virtually reconstructed transparent basicranium of Echinosorex gym-nura Raffles, 1822 with 3D model of the endocast of the bony labyrinth (in blue). A. ventral view; B. posterior view.

A B

Fig. 1 - Pictures of six extant Erinaceidae, three Erinaceinae (A-C) and three Galericinae (D-F): A. Erinaceus europaeus Linnaeus, 1758 from Europe; B. Atelerix albiventris Wagner, 1841 from Northern Africa; C. Hemiechinus auritus (Gmelin, 1770) from Central Asia; D. Echinosorex gymnura Raffles, 1822 from Southeastern Asia; E. Neotetracus sinensis Trouessart, 1909 from China; F. Hylomys suillus Müller, 1840 from Southeastern Asia.

GalericinaeErinaceinae

Erinaceus europaeus Atelerix albiventris Hemiechinus auritus Echinosorex gymnura Neotetracus sinensis Hylomys suillus

FEDCBA

Fig. 4 - Reconstruction of the bony labyrinths for: Neurogymnurus cayluxi Filhol, 1877 (Galericinae, Early Oligocene, France); Galerix exilis (Blainville, 1840) (Galericinae, Middle Miocene, Germany); Echinosorex gymnura Raffles, 1822 (Galericinae, Sumatra, extant); Amphechinus ed-wardsi (Filhol, 1879) (Erinaceinae, Early Miocene, France), Postpalerinaceus vireti (Crusafont and Villalta, 1947) (Late Miocene, Spain); Erinaceus europaeus Linnaeus, 1758 (Erinaceinae, Switzerland, extant); and Atelerix albiventris Wagner, 1841 (Erinaceinae, eastern Africa, extant). Orienta-tions: R. Rostral , D. Dorsal, M. Medial. Abbreviations: C. Cochlea, V. Vestibule, ASC. Anterior Semicircular cannal, LSC. Lateral semicircular canal, PSC. Posterior semicircular canal, AA. Anterior ampula, LA. Lateral ampula, PA. Posterior ampula, SL. Secondary lamina. CV. Conduct of vesti-bule, CC. Crus commune, SCC. secondary crus commune, ACF. External aperture of the cochlear fossula.

Fig. 5 - Phylogeny and stratigraphic distribution of 10 taxa (1 Solenodontidae [outgroup], 1 Soricidae, 8 Erinaceidae) and 14 scored charaters. The phylogeny is the most parsimonious tree found by an exhaustive search with the software PAUP 4.0. Consistency index=0.6207; ho-moplasy index=0.3793; retention index= 0.6563; tree length= 31.

Neo

gene

Pal

eoge

neO

ligo.

Eo.

Mio

cene

Priabonian

Rupelian

Chattian

Aquitanian

Burdigalian

Langhian

Serravallian

Tortonian

Messinian

present

5.333

7.246

11.62

13.82

15.97

20.44

23.03

28.10

33.90

38.00

Sole

nodo

n

Sore

x

Neur

ogym

nuru

sEc

hino

sore

x

Gal

erix

Amph

echi

nus

Atel

erix

Erin

aceu

s

Post

pale

rinac

eus

Para

echi

nus

Fig. 2 - Phylogeny of extant Erinaceidae based on dental and genetic characters. Modified after He et al. [4].

Solenodon

EchinosorexNeohylomysNeotetracusHylomys

AtelerixErinaceusParaechinusHemiechinusMesechinus

Galericinae

Erinaceinae

D

R

R

M

M

D

D

M

C

C

AA

AA

LA PASCC

LSC

PA

PSC

PSC

SL

V

CC

ACF

C

PSC

LSC

CV

CV

ASC

LSC