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

Abstract

The petrosal anatomy and inner ear structure of Jurassic cladotherian mammals represent the ancestral morphological conditions (groundplan) from which modern therian mammals (marsupials and placentals) have evolved. We present the reconstruction of the petrosal and inner ear features of the Late Jurassic dryolestoid mammal Henkelotherium guimarotae from high-resolution computed tomography and three-dimensional imaging analysis. This study of Henkelotherium revealed a combination of derived and primitive features, including: cladotherian apomorphies, such as the promontorial sulcus for the internal carotid artery and reduced lateral trough; trechnotherian characters, such as an enclosed cochlear canaliculus for the perilymphatic duct, post-promontorial tympanic sinus and caudal tympanic process; in addition to plesiomorphic mammalian features, such as the cavum supracochleare and prootic canal. The inner ear of Henkelotherium shows a division between the utricle and saccule, a cochlear canal coiled through at least 270 ° , a distinctive primary bony lamina for the basilar membrane, and a secondary bony lamina. The development of the primary and secondary bony laminae in the cochlear canal is suggested here to be correlated with the concurrent coiling of the bony canal and membranous duct of the inner ear cochlea, apomorphies of the more inclusive cladotherian clade that also represent the ancestral morphotype of modern therian mammals. Because these features are crucial for high-frequency hearing in extant therian mammals, their early appearance in Late Jurassic cladotherians suggests a more ancient origination for high-frequency hearing in mammalian history than previously thought.

Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters

“…Hyrtl, 1845;Gray, 1907Gray, , 1908Meng & Fox, 1995;S anchezVillagra & Schmelzle, 2007;Horovitz et al 2008;Ladev eze et al 2008), but the condition exhibited in these notoungulates is not a secondary crus. The presence of a secondary crus commune (state 22.0) is likely plesiomorphic for eutherians (Meng & Fox, 1995;Ekdale & Rowe, 2011), and possibly all therians (Ekdale, 2013), based on its presence in metatherians (S anchez-Villagra & Schmelzle, 2007;Horovitz et al 2008Horovitz et al , 2009) and in dryolestoid mammals that are outgroups of crown Theria (Ruf et al 2009;Luo et al 2011Luo et al , 2012. None of the notoungulates examined here possess a secondary crus, suggesting that a loss of this feature typifies Notoungulata (state 22.1; Fig.…”

“…Hyrtl, 1845;Gray, 1907Gray, , 1908MacIntyre, 1972;Fleischer, 1973;Luo & Ketten, 1991;Meng & Fox, 1995;S anchez-Villagra & Schmelzle, 2007;Schmelzle et al 2007;Horovitz et al 2008Horovitz et al , 2009Ladev eze et al 2008;Ruf et al 2009;Ekdale, 2010Ekdale, , 2011Ekdale, , 2013Ni et al 2010;Ekdale & Rowe, 2011;Luo et al 2011;Billet & de Muizon, 2013). Fig.…”

“…4). Outside of notoungulates state 15.1 is also known in Henkelotherium (Ruf et al 2009) and Dryolestes (Luo et al 2011(Luo et al , 2012. 16 Position of chamber for utricle (in bony labyrinth) when viewed dorsally: bulge for the utricle positioned closer to the posterior end of the LSC than the anterior end (0), or centrally located between ends of the LSC (1).…”

Evolutionary Paths to Mammalian Cochleae

“…There were both primary and secondary laminae, presumably supporting the inner and outer edges of the basilar membrane, and the cochlear ganglion was itself enclosed in a canal within the bony wall. The nerve fiber bundles passed through clear openings in the bone to enter the organ of Corti (Ruf et al 2009;Luo et al 2010). It is, of course, difficult to speculate upon the selective forces at play that led to this development.…”

Digital reconstruction of the inner ear of Leptictidium auderiense (Leptictida, Mammalia) and North American leptictids reveals new insight into leptictidan locomotor agility

“…Such a structure is present not only in zhelestids, but also already in the Upper Jurassic stem-therians Dryolestes leiriensis and Henkelotherium guimarotae, as well as in many placentals (Meng and Fox 1995;Ruf et al 2009;Ekdale and Rowe 2011;Luo et al 2011Luo et al , 2012Ekdale 2013). Thus, we propose that the secondary bony lamina is a plesiomorphic character of Leptictida and Theria as well.…”