High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1744, 2012, Pages 3932-3939

  Billet, Guillaume ^a   Hautier, Lionel ^b   Asher, Robert J ^b   Schwarz, Cathrin ^a,c   Crumpton, Nick ^b   Martin, Thomas ^a   Ruf, Irina ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

Constraint; Inner ear; Semicircular canals; Shape; Variability; Xenarthra

Indexed keywords

ADAPTATION; LOCOMOTION; MAMMAL; MORPHOLOGY; MOVEMENT; PHENOTYPIC PLASTICITY; SHAPE; TOMOGRAPHY;

EID: 84865382925     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.1212     Document Type: Article

References (55)

1. Sipla, J. & Spoor, F. 2008 The physics and physiology of balance. In Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates (eds J. G. M. Thewissen & S. Nummela), pp 227-232. Berkeley, CA: University California Press.
2. David, R., Droulez, J., Allain, R., Berthoz, A., Janvier, P. & Bennequin, D. 2010 Motion from the past. A new method to infer vestibular capacities of extinct species. C. R. Palevol. 9, 397-410. (doi:10.1016/j.crpv.2010.07.012)
3. Jeffery, N. & Cox, P. G. 2010 Do agility and skull architecture influence the geometry of the mammalian vestibulo-ocular reflex? J. Anat. 216, 496-509. (doi:10.1111/j.1469-7580.2010.01211.x)
4. Silcox, M. T., Bloch, J. I., Boyer, D. M., Godinot, M., Ryan, T. M., Spoor, F. & Walker, A. 2009 Semicircular canal system in early primates. J. Hum. Evol. 56, 315-327. (doi:10.1016/j.jhevol.2008.10.007)
5. Spoor, F., Garland Jr, T., Krovitz, G., Ryan, T. M., Silcox, M. T. & Walker, A. 2007 The primate semicircular canal system and locomotion. Proc. Natl Acad. Sci. USA 104, 10808-10812. (doi:10.1073/pnas.0704250104)
6. Ryan, T.M. et al. 2012 Evolution of locomotion in Anthropoidea: the semicircular canal evidence. Proc. R. Soc. B 279, 3467-3475. (doi:10.1098/rspb.2012.0939)
7. Cox, P. G. & Jeffery, N. 2008 Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids and modern humans. J. Anat. 213, 83-596. (doi:10.1111/j.1469-7580.2008.00983.x)
8. Ekdale, E. G. & Rowe, T. 2011 Morphology and variation within the bony labyrinth of zhelestids (Mammalia, Eutheria) and other therian mammals. J. Vert. Paleontol. 31, 658-675. (doi:10.1080/02724634.2011.557284)
9. Lange, S., Stalleicken, J. & Burda, H. 2004 Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris. J. Morphol. 262, 770-779.(doi:10.1002/jmor.10277)
10. Sánchez-Villagra, M. & Schmelzle, T. 2007 Anatomy and development of the bony inner ear in the woolly opossum, Caluromys philander (Didelphimorphia, Marsupialia). Mastozoologia Neotrop. 14, 53-60.
11. Lindenlaub, T. & Burda, H. 1993 Morphometry of the vestibular organ in neonate and adult African mole-rats Cryptomys species. Anat. Embryol. 188, 159-162.(doi:10.1007/BF00186249)
12. Sunquist, M. E. & Montgomery, G. G. 1973 Activity patterns and rates of movement of two-toed and threetoed sloths (Choloepus hoffmanni and Bradypus infuscatus). J. Mammal. 54, 946-954. (doi:10.2307/1379088)
13. Adam, P. J. 1999 Choloepus didactylus. Mamm. Species 621, 1-8. (doi:10.2307/3504332)
14. Brattstrom, B. H. 1966 Sloth behavior. J. Mammal. 47, 348. (doi:10.2307/1378148)
15. Britton, S. W. & Kline, R. F. 1939 Augmentation of activity in the sloth by adrenal extract, emotion and other conditions. Am. J. Physiol. 127, 127-130.
16. Gray, A. A. 1907 The labyrinth of animals, vol 1. London, UK: Churchill.
17. Walker, A., Ryan, T. M., Silcox, M. T., Symons, E. L. & Spoor, F. 2008 The semicircular canal system and locomotion: the case of extinct lemuroids and lorisoids. Evol. Anthropol. 17, 135-145. (doi:10.1002/evan.20165)
18. Darwin, C. 1859 The origin of species by means of natural selection or the preservation of favoured races in the struggle for life. London, UK: John Murray.
19. Walker-Larsen, J. & Harder, L. J. 2001 Vestigial organs as opportunities for functional innovation: the example of the Penstemon staminode. Evolution 55, 477-487.(doi:10.1111/j.0014-3820.2001.tb00782.x)
20. Crespi, B. J. & Vanderkist, B. A. 1997 Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity 79, 624-630. (doi:10.1038/hdy.1997.208)
21. Birkhead, T. R., Pellat, E. J., Brekke, P., Yeates, R. & Castillo-Juarez, H. 2005 Genetic effects on sperm design in the zebra finch. Nature 434, 383-387.(doi:10.1038/nature03374)
22. Calhim, S., Immler, S. & Birkhead, T. R. 2007 Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2, e413.(doi:10.1371/journal.pone.0000413)
23. Westphal, M. F., Massie, J. L., Bronkema, J. M., Smith, B. E. & Morgan, T. J. 2011 Heritable variation in garter nake color patterns in postglacial populations. PLoS ONE 6, e24199. (doi:10.1371/journal.pone.0024199)
24. Moraes-Barros, N., de Silva, J. A. B. & Stenghel Morgante, J. 2011 Morphology, molecular phylogeny, and taxonomic inconsistencies in the study of Bradypus sloths (Pilosa: Bradypodidae). J. Mammal. 92, 86-100.(doi:10.1644/10-MAMM-A-086.1)
25. Wetzel, R. M. 1985 The Identification and distribution of recent Xenarthra (Edentata). In The ecology and evolution of armadillos, sloths, and vermilinguas (ed. G. G. Montgomery), pp 5-21. Washington, DC, USA: Smithsonian Institution Press.
26. McBee, K. & Baker, R. J. 1982 Dasypus novemcinctus. Mamm. Species 162, 1-9. (doi:10.2307/3503864)
27. Bradshaw, A. P., Curthoys, I. S., Todd, M. J., Magnussen, J. S., Taubman, D. S., Aw, S. T. & Halmagiy, G. M. 2010 A mathematical model of human semicircular canal geometry: a new basis for interpreting vestibular physiology. J. Assoc. Res. Otolaryngol. 11, 145-159.(doi:10.1007/s10162-009-0195-6)
28. Hammer, Ø., Harper, D. A. T. & Ryan, P. D. 2001 PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9.
29. Van Valen, L. 2005 The statistics of variation. In Variation: a central concept in biology (eds B. Hallgrimsson & B. K. Hall), pp 29-47. Boston, MA: Elsevier Academic.
30. Welker, K. L., Orkin, J. D. & Ryan, T. M. 2009 Analysis of intraindividual and intraspecific variation in semicircular canal dimensions using high-resolution x-ray computed tomography. J. Anat. 215, 444-451. (doi:10.1111/j.1469-7580.2009.01124.x)
31. Ekdale, E. G. 2010 Ontogenetic variation in the bony labyrinth of Monodelphis domestica (Mammalia: Marsupialia) following ossification of the inner ear cavities. Anat. Rec. 293, 1896-1912. (doi:10.1002/ar.21234)
32. Spoor, F. & Zonneveld, F. 1998 Comparative review of the human bony labyrinth. Phys. Anthropol. 41, 211-251. (doi:10.1002/(SICI)1096-8644(1998)107:27)
33. Gunz, P., Ramsier, M., Kuhrig, M., Hublin, J.-J. & Spoor, F. 2012 The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. J. Anat. 220, 529-543. (doi:10.1111/j.1469-7580.2012.01493.x)
34. Calabrese, D. R. & Hullar, T. E. 2006 Planar relationships of the two semicircular canals in two strains of mice. J. Assoc. Res. Otolaryngol. 7, 151-159. (doi:10.1007/s10162-006-0031-1)
35. Curthoys, I. S., Curthoys, E. J., Blanks, R. H. I. & Markham, C. H. 1975 The orientation of the semicircular canals in the guinea pig. Acta Otolaryngol. 80, 197-205. (doi:10.3109/00016487509121319)
36. Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D. & Wolpert, L. 1985 Developmental constraints and evolution. Q. Rev. Biol. 60, 265-287. (doi:10.1086/414425)
37. Arnold, S. J. 1992 Constraints on phenotypic variation. Am. Nat. 140, 85-107. (doi:10.1086/285398)
38. Klingenberg, C. P. 2011 Evolution and development of shape: integrating quantitative approaches. Nat. Rev. Genet. 11, 623-635. (doi:10.1038/nrg2829)
39. Pearce, T. 2011 Evolution and constraints on variation: variant specification and range of assessment. Philos. Sci. 78, 739-751. (doi:10.1086/664568)
40. Walker, J. A. 2007 A general model of functional constraints on phenotypic evolution. Am. Nat. 170, 681-689. (doi:10.1086/521957)
41. Hullar, T. E.& Williams, C.D. 2006. Geometry of the semicircular canals of the chinchilla (Chinchilla laniger). Hear. Res. 213, 17-24. (doi:10.1016/j.heares.2005.11.009)
42. Anderson, R. P. & Handley Jr, C. O. 2001 A new species of three-toed sloth (Mammalia: Xenarthra) from Panama, with a review of the genus Bradypus. Proc. Biol. Soc. Wash. 114, 1-33.
43. Hayssen, V. 2010 Bradypus variegatus (Pilosa: Bradypodidae). Mamm. Species 850, 19-32. (doi:10.1644/850.1)
44. Asher, R. J., Lin, K. H., Kardjilov, N. & Hautier, L. J. 2011 Variability and constraint in the mammalian vertebral column. J. Evol. Biol. 24, 1080-1090. (doi:10.1111/j.1420-9101.2011.02240.x)
45. Hautier, L. J., Weisbecker, V., Sánchez-Villagra, M. R., Goswami, A. & Asher, R. J. 2010 Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc. Natl Acad. Sci. USA 107, 1803-18 908.(doi:10.1073/pnas.1010335107)
46. Buchholtz, E. A. & Stepien, C. C. 2009 Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evol. Dev. 11, 69-79. (doi:10.1111/j.1525-142X.2008.00303.x)
47. Rager, L. & Sánchez Villagra, M.R. 2011 Heterochrony in cranial suture closure of recent and fossil Xenarthra. In Program and Abstracts of the 9th Annual Meeting of the European Association of Vertebrate Palaeontologists, 14-19 June, Heraklion, Crete, Greece (eds A. van der Geer & A. Athanassiou), p. 49. See: http://www.eavp.org.
48. Asher, R. J., Bennett, N. & Lehmann, T. 2009 The new framework for understanding placental mammal evolution. Bioessays 31, 853-864. (doi:10.1186/1741-7007-6-14)
49. Ciancio, M. R., Castro, M. C., Galliari, F. C., Carlini, A. A. & Asher, R. J. 2012 Evolutionary implications of dental eruption in Dasypus (Xenarthra). J. Mamm. Evol. 19, 1-8. (doi:10.1007/s10914-011-9177-7)
50. Delsuc, F. & Douzery, E. J. P. 2009 Armadillos, anteaters and sloths (Xenarthra). In The timetree of life (eds S. B. Hedges & S. Kumar), pp. 475-478. Oxford, UK: Oxford University Press.
51. Gaudin, T. J. 2004 Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zool. J. Linn. Soc. 140, 255-305.(doi:10.1111/j.1096-3642.2003.00100.x)
52. Nyakatura, J. A. In press. The convergent evolution of suspensory posture and locomotion in tree sloths. J. Mamm. Evol. (doi:10.1007/s10914-011-9174-x)
53. Pujos, F., Gaudin, T. J., De Iuliis, G. & Castelle, C. In press. Recent advances on variability, morphofunctional adaptations, dental terminology, and evolution of sloths. J. Mamm. Evol. (doi:10.1007/s10914-012-9189-y)
54. Jones, M. G. & Spells, K. E. 1963 A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc. R. Soc. Lond. B 157, 403-419. (doi:10.1098/rspb.1963.0019)
55. Muller, M. 1999 Size limitations in semicircular duct systems. J. Theor. Biol. 198, 405-437. (doi.org/10.1006/jtbi. 1999.0922)