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. 2013 Dec;223(6):557-67.
doi: 10.1111/joa.12114. Epub 2013 Sep 24.

The inner ear of Megatherium and the evolution of the vestibular system in sloths

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The inner ear of Megatherium and the evolution of the vestibular system in sloths

G Billet et al. J Anat. 2013 Dec.

Abstract

Extant tree sloths are uniquely slow mammals with a very specialized suspensory behavior. To improve our understanding of their peculiar evolution, we investigated the inner ear morphology of one of the largest and most popular fossil ground sloths, Megatherium americanum. We first address the predicted agility of this animal from the scaling of its semicircular canals (SC) relative to body mass, based on recent work that provided evidence that the size of the SC in mammals correlates with body mass and levels of agility. Our analyses predict intermediate levels of agility for Megatherium, contrasting with the extreme slowness of extant sloths. Secondly, we focus on the morphology of the SC at the inner ear scale and investigate the shape and proportions of these structures in Megatherium and in a large diversity of extant xenarthrans represented in our database. Our morphometric analyses demonstrate that the giant ground sloth clearly departs from the SC morphology of both extant sloth genera (Choloepus, Bradypus) and is in some aspects closer to that of armadillos and anteaters. Given the close phylogenetic relationships of Megatherium with the extant genus Choloepus, these results are evidence of substantial homoplasy of the SC anatomy in sloths. This homoplasy most likely corresponds to an outstanding convergent evolution between extant suspensory sloth genera.

Keywords: Folivora; Xenarthra; allometry; bony labyrinth; fossil; semicircular canals; shape.

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Figures

Fig. 1
Fig. 1
Views of the 3D reconstructed skull and inner ear of Megatherium americanum MNHN-F-PAM 276. (A) Right lateral view of skull. (B) Same than (A) but reconstructed with transparency of bone leaving apparent the right bony labyrinth of the inner ear in opaque red at the rear of the skull. (C) Close-up on the right bony labyrinth of the inner ear, lateral view. ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal. Scale bar: (A,B) 100 mm, (C) 5 mm.
Fig. 2
Fig. 2
Graphical relationship between semicircular canal sizes, body mass and agility. Double logarithmic plots of average semicircular canal radius (SCR) against body mass for 210 mammals (modified from fig. 1b in Spoor et al. 2007) and two specimens of Megatherium. Note that Megatherium (considered at 3950 kg; Fariña et al. 1998) plots well above similar-sized and medium slow taxa (i.e. elephants, represented by the two circles below Megatherium), and that the three extant sloth specimens (the three black crosses indicated with an arrow) plot below all similar-sized mammals.
Fig. 3
Fig. 3
Relative size of the semicircular canals (SC) scaled with the inner ear in extant xenarthrans and Megatherium. Bar graph showing the values of the ratio ‘SC size/inner ear height’ (=SCR/IEH) in various specimens. The thick dotted line in the background emphasizes a distinction between most xenarthrans and extant tree sloths in the relative size of the semicircular canals. Taxonomic abbreviations are for Bradypus variegatus (Brad. v.), Bradypus tridactylus (Brad. t.), Chaetophractus vellerosus (Cha. v.), Chlamyphorus truncatus (Chl. t.), Choloepus hoffmani (Chol. h.), Choloepus didactylus (Chol. d.), Cyclopes didactylus (Cycl. d.), Dasypus novemcinctus (Das. n.), Dasypus hybridus (Das. h.), Euphractus sexcinctus (Eup. s.), Megatherium (Megath.), Myrmecophaga tridactyla (Myrm. t.), Priodontes maximus (Prio. m.), Tamandua tetradactyla (Tam. t.), Tolypeutes matacus (Tol. m.); see Supporting Information Table S5 for more details on specimens (e.g. designed with letters). ASCR, radius of curvature of anterior semicircular canal; IEH, inner ear height = distance between the apex of common crus and the apex of cochlea; SCR, average radius of curvature of the three semicircular canals.
Fig. 4
Fig. 4
Shape differentiation of the bony labyrinth of xenarthrans on the first two axes (52.67% of the among-group variance) of the principal component analysis (PCA) performed on a set of 10 variables on the semicircular canals (SCs) and 35 specimens. Taxonomic abbreviations are for Bradypus variegatus (Brad_v); B. Bradypus tridactylus (Brad_t), Chaetophractus vellerosus (Cha_v), Chlamyphorus truncatus (Chl_t), Choloepus didactylus (Cho_d), Choloepus hoffmani (Cho_h), Cyclopes didactylus (Cyc_d), Dasypus novemcinctus (Das_n); Dasypus hybridus (Das_h), Euphractus sexcinctus (Eup_s), Myrmecophaga tridactyla (Mym_t), Priodontes maximus (Pri_m), Tamandua tetradactyla (Tam_t), Tolypeutes matacus (Tol_m).
Fig. 5
Fig. 5
Evolution of semicircular canal (SC) proportions in Xenarthra. Illustration of the two most parsimonious hypotheses (A,B) of phylogenetic evolution of small SC relative to the inner ear height (as shown in Fig. 3), mapped on a cladogram of extant Xenarthra and Megatherium (consensus of Gaudin, ; Billet et al. ; Delsuc et al. 2012). Note that an alternative phylogenetic pattern of relationships with Megatherium closer to Bradypus than to Choloepus – as proposed by Poinar et al. (2003) for the ground sloth Nothrotheriops, a possible relative of Megatherium (Gaudin, 2004) – would also support homoplastic scenarios within Folivora.

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