Advertisement

Tracing the origin of the panda’s thumb

Abstract

We investigate the relative development of the carnivoran radial sesamoids to untangle the evolution of this iconic structure. In the pandas (both giant and red), this ‘false thumb’ is known to perform a grasping role during bamboo feeding in both the red and giant pandas. An original locomotor role has been inferred for ailurids, but this remains to be ascertained for ursids. A large sample of radial sesamoids of Indarctos arctoides from the Miocene of Batallones-3 (Spain) indicates that this early ailuropodine bear displayed a relatively hypertrophied radial sesamoid, with a configuration more similar to that of the red panda and other carnivorans than to that of giant pandas. This false thumb is the first evidence of this feature in the Ursidae, which can be linked to a more herbivorous diet. Moreover, in the two extant pandas, the false thumb should not be interpreted as an anatomical convergence, but as an exaptive convergence regarding its use during the bamboo feeding, which changes the evolutionary view of this singular structure.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Abella J (2011) Indarctos arctoides Depéret, 1895 (Carnivora, Mammalia) del yacimiento vallesiense de Batallones 3 (cuenca de Madrid). PhD. dissertation, Universidad Autónoma de Madrid / Museo Nacional de Ciencias Naturales

  2. Abella J, Montoya P, Morales J (2011) New species of Agriarctos (Ailuropodinae, Ursidae, Carnivora) in the locality of Nombrevilla 2 (Zaragoza, Spain). Estud Geol 67:187–191

  3. Abella J, Alba DV, Robles JM, Valenciano A, Rotgers C, Carmona R, Montoya P, Morales J (2012) Kretzoiarctos gen. nov., the oldest member of the giant panda clade. PLoS One 7:e48985

  4. Abella J, Valenciano A, Pérez-Ramos A, Montoya P, Morales J (2013a) The radial sesamoid of Indarctos arctoides, the first evidence of a feeding related false thumb [abstract]. Anat Rec 296:271–272, Special Feature – 1

  5. Abella J, Valenciano A, Pérez-Ramos A, Montoya P, Morales J (2013b) On the socio-sexual behaviour of the extinct ursid Indarctos arctoides: an approach based on its baculum size and morphology. PLoS One 8:e77711

  6. Abella J, Montoya P, Morales J (2014) Paleodiversity of the superfamily Ursoidea (Carnivora, Mammalia) in the Spanish Neogene, related to environmental changes. J Iberian Geol 40:11–18

  7. Antón M, Salesa MJ, Pastor JF, Peigné S, Morales J (2006) Implications of the functional anatomy of the hand and forearm of Ailurus fulgens (Carnivora, Ailuridae) for the evolution of the ‘false-thumb’ in pandas. J Anat 209:757–764

  8. Barone R (2000) Anatomie Comparée des mammifères domestiques. Tome 1 and 2. Paris: Éditions Vigot

  9. Calvo JP, Pozo M, Silva PG, Morales J (2013) Pattern of sedimentary infilling of fossil mammal traps formed in pseudokarst at Cerro de los Batallones, Madrid Basin, Central Spain. Sedimentology 60:1681–1708

  10. Chorn J, Hoffmann RS (1978) Ailuropoda melanoleuca. Mamm Species 110:1–6

  11. Cirot E (1992) Étude phylogénétique de quelques genres d’Arctoidea de l’Oligocène eurasiatique. Comparaison des données morphologiques et moléculaires. Dissertation, University of Poitiers

  12. Davis DD (1964) The giant panda. A morphological study of evolutionary mechanisms. Fieldiana: Zool Me 3:1–339

  13. Delfino M, Abella J, Sánchez IM, Alba D (2013) A nearly complete Varanus specimen from the Late Miocene of Cerro de los Batallones (Madrid Basin). Volume: 11th EAVP Meeting. Villers-sur-Mer, France, p 33

  14. Domingo MS, Alberdi MT, Azanza B, Silva PG, Morales J (2013) Origin of an assemblage massively dominated by carnivorans from the Miocene of Spain. PLoS One 8:e63046

  15. Endo H, Sasaki N, Yamagiwa D, Uetake Y, Kurohmaru M, Hayashi Y (1996) Functional anatomy of the radial sesamoid bone in the giant panda (Ailuropoda melanoleuca). J Anat 189:587–592

  16. Endo H, Yamagiwa D, Hayasahi Y, Koie H, Yamaya Y, Kimura J (1999a) Role of the giant panda’s ‘pseudo-thumb’. Nature 397:309–310

  17. Endo H, Hayashi Y, Yamagiwa D, Kurohmaru M, Koie H, Yamaya Y, Kimura J (1999b) CT examination of the manipulation system in the giant panda (Ailuropoda melanoleuca). J Anat 195:295–300

  18. Endo H, Makita T, Sasaki M, Arishima K, Yamamoto M, Hayashi Y (1999c) Comparative anatomy of the radial sesamoid bone in the polar bear (Ursus maritimus), the brown bear (Ursus arctos) and the giant panda (Ailuropoda melanoleuca). J Vet Med Sci 61:903–907

  19. Endo H, Sasaki M, Hayashi Y, Koie H, Yamaya Y, Kimura J (2001a) Carpal bone movements in gripping action of the giant panda (Ailuropoda melanoleuca). J Anat 198:243–246

  20. Endo H, Sasaki M, Kogiku H, Yamamoto M, Arishima K (2001b) Radial sesamoid bone as a part of the manipulation system in the lesser panda (Ailurus fulgens). Ann Anat 183:181–184

  21. Endo H, Hama N, Niizawa N, Kimura J, Itou T, Koie H, Sakai T (2007) Three-dimensional reconstruction of the manipulation system in the lesser panda. Mamm Study 32:99–103

  22. Endo H, Hama N, Niizawa N, Kimura J, Itou T, Koie H, Sakai T (2008) Three-dimensional imaging of the manipulating apparatus in the lesser panda and the giant panda. In: Endo H, Frey R (eds) Anatomical imaging: towards a new morphology (eds H.). Springer, Japan, pp 61–66

  23. Ewer RF (1998) The carnivores. Cornell University Press, Ithaca, New York

  24. Fisher RE, Adrian B, Barton M, Holmgren J, Tang SY (2009) The phylogeny of the red panda (Ailurus fulgens): evidence from the forelimb. J Anat 215:611–635

  25. Gould SJ (1978) The panda’s peculiar thumb. Nat Hist 87:20–30

  26. Gould SJ (1980) The panda’s thumb: more reflections in natural history. Norton, New York

  27. Gould SJ (2002) The Structure of evolutionary theory. The Belknap Press of Harvard University Press

  28. Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15

  29. Gray H (1977) Anatomy, descriptive and surgical. Bounty Books, New York

  30. Heinrich RE, Houde P (2006) Postcranial anatomy of Viverravus (Mammalia, Carnivora) and implications for substrate use in basal Carnivora. J Vert Paleontol 26:422–435

  31. Hutchinson JR, Delmer C, Miller CE, Hildebrandt T, Pitsillides A, Boyde A (2011) From flat foot to fat foot: structure, ontogeny, function, and evolution of elephant “sixth toes”. Science 334:1699–1703

  32. Jennings AP, Veron G (2009) Family Viverridae (civets, genets and oyans). In: Wilson DE, Mittermeier RA (eds) Handbook of mammals of the world. 1. Carnivores. Lynx Editions, Barcelona, pp 174–233

  33. Krause WD, Jenkins FA (1983) The postcranial skeleton of North American multituberculates. Bull Mus Comp Zool 150:199–246

  34. Lankester ER, Lydekker R (1901) On the affinities of Aeluropus melanoleucus, A. Milne-Edwards. Trans. Linn Soc Lon Zool 8:163–172

  35. Larivière S, Jennings AP (2009) Family Mustelidae (weasels and relatives). In: Wilson DE, Mittermeier RA (eds) Handbook of mammals of the world. 1. Carnivores. Lynx Editions, Barcelona, pp 564–656

  36. Le Minor JM (1994) The sesamoid bone of musculus abductor pollicis longus (os radiale externum or prepollex) in primates. Acta Anat 150:227–231

  37. Legreneur P, Laurin M, Monteil KM, Bels V (2011) Convergent exaptation of leap up for escape in distantly related arboreal amniotes. Adapt Behav 20:61–77

  38. López-Antoñanzas R, Peláez-Campomanes P, Álvarez-Sierra MA, García-Paredes I (2010) New species of Hispanomys (Rodentia, Cricetodontinae) from the Upper Miocene of Batallones (Madrid, Spain). Zool J Linn Soc 160:725–747

  39. Mangas JG, Carrobles M, Alcázar LH, Bellón D, Virgós E (2007) Aproximación al estudio de la ecología espacial de especies simpátricas: la garduña (Martes foina) y la gineta (Genetta genetta). Galemys, 19 (Número especial):61–71

  40. McLearn D (1992) Locomotion, posture, and feeding behavior of kinkajous, coatis and raccons. J Mammal 73:245–261

  41. Mondolfi E (1989) Notes on the distribution, habitat, food habits, status and conservation of the spectacled bear (Tremarctos ornatus) in Venezuela. Mammalia 53:525–544

  42. Monescillo MFG, Salesa MJ, Antón M, Siliceo G, Morales J (2014) Machairodus aphanistus (Felidae, Machairodontinae, Homotherini) from the Late Miocene (Vallesian, MN10) site of Batallones-3 (Torrejón de Velasco, Madrid, Spain). J Vert Paleontol 34:699–709

  43. Morales J et al (2008) El sistema de yacimientos de mamíferos miocenos del Cerro de los Batallones, Cuenca de Madrid: Estado actual y perspectivas Paleontologica Nova SEPAZ 8:41–117

  44. Nowak RM (1999) Walker’s mammals of the world, vol I, 6th edn. The Johns Hopkins University Press, Baltimore Maryland

  45. Peyton B (1980) Ecology, distribution, and food habits of spectacled bears, Tremarctos ornatus, in Peru. J Mammal 61:639–652

  46. Poe S, Goheen JR, Hulebak EP (2007) Convergent exaptation and adaptation in solitary island lizards. Proc R Soc B 274:2231–2237

  47. Ríos-Uzeda B, Gómez H, Wallace RB (2006) Habitat preference of the Andean bear (Tremarctos ornatus) in the Bolivian Andes. J Zool 268:271–278

  48. Roberts MS, Gittleman JL (1984) Ailurus fulgens. Mamm Species 222:1–8

  49. Roussiakis SJ (2001) Postcranial remains of Indarctos (Ursidae, Mammalia) from the classical locality of Pikermi (Attica, Greece), with a description of the front limb. Senckenb Lethaea 81:347–358

  50. Salesa MJ, Siliceo G, Antón M, Abella J, Montoya P, Morales J (2006a) Anatomy of the “false thumb” of Tremarctos ornatus (Carnivora, Ursidae, Tremarctinae): phylogenetic and functional implications. Estud Geol 62:389–394

  51. Salesa MJ, Antón M, Peigné S, Morales J (2006b) Evidence of a false thumb in a fossil carnivore clarifies the evolution of pandas. Proc Natl Acad Sci U S A 103:379–382

  52. Salesa MJ, Antón M, Peigné S, Morales J (2008) Functional anatomy and biomechanics of the postcranial skeleton of Simocyon batalleri (Viret, 1929) (Carnivora, Ailuridae) from the Late Miocene of Spain. Zool J Linn Soc 152:593–621

  53. Salesa MJ, Antón M, Morales J, Peigné S (2012) Systematics and phylogeny of the small felines (Carnivora, Felidae) from the Late Miocene of Europe: a new species of Felinae from the Vallesian of Batallones (MN 10, Madrid, Spain). J Syst Palaeonto 10:87–102

  54. Salton JA, Sargis EJ (2008) Evolutionary morphology of the Tenrecoidea (Mammalia) carpal complex. Biol J Linn Soc 93:267–288

  55. Sánchez-Villagra MR, Menke PR (2005) The mole’s thumb—evolution of the hand skeleton in talpids (Mammalia). Zool 108:3–12

  56. Sasaki M, Endo H, Wiig O, Derocher AE, Tsubota T, Taru H, Yamamoto M, Arishima K, Hayashi Y, Kitamura N, Yamada J (2005) Adaptation of the hindlimbs for climbing in bears. Ann Anat 187:153–160

  57. Sato JJ, Wolsan M, Minami S, Hosoda T, Sinaga MH, Hiyama K, Yamaguchi Y, Suzuki H (2009) Deciphering and dating the red panda’s ancestry and early adaptive radiation of Musteloidea. Mol Phylogenet Evol 53:907–922

  58. Sato JJ, Wolsan M, Minami S, Prevosti FJ, D’Elía G, Begg C, Begg K, Hosoda T, Campbell KL, Suzuki H (2012) Evolutionary and biogeographic history of weasel-like carnivorans (Musteloidea). Mol Phylogenet Evol 63:745–757

  59. Siliceo G, Salesa MJ, Antón M, Monescillo MFG, Morales J (2014) Promegantereon ogygia (Felidae, Machairodontinae, Smilodontini) from the Vallesian (Late Miocene, MN10) of Spain: morphological and functional differences in two noncontemporary populations. J Vert Paleontol 34:407–418

  60. Spaulding M, Flynn JF (2009) Anatomy of the postcranial skeleton of “Miacisuintensis (Mammalia: Carnivoramorpha). J Vert Paleontol 29:1212–1223

  61. Szalay FS (1994) Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge University Press, London

  62. Taylor ME (1974) The functional anatomy of the forelimb of some African Viverridae (Carnivora). J Morphol 143:307–336

  63. Valenciano A, Abella J, Sanisidro O, Hartstone-Roses A, Álvarez-Sierra MA, Morales J (2015) Complete description of the skull and mandible of the giant mustelid Eomellivora piveteaui Ozansoy, 1965 (Mammalia, Carnivora, Mustelidae) from Batallones (MN10), Late Miocene (Madrid, Spain). J Vert Paleontol. doi:10.1080/02724634.2014.934570

  64. Wallace SC (2011) Advanced members of the Ailuridae (lesser or red pandas—subfamily Ailurinae). In: Glatston AR (ed) Red panda. Biology and conservation of the first panda. Academic, San Diego, pp 43–60

  65. Wood-Jones F (1939a) The ‘thumb’ of the giant panda. Nature 143:157

  66. Wood-Jones F (1939b) The forearm and manus of the giant panda, Ailuropoda melanoleuca, M.-Edw. With an account of the mechanism of its grasp. Proc Zool Soc B 109:113–129

Download references

Acknowledgments

This study was supported by the Spanish Ministerio de Economía y Competitividad (CGL2011-25754, CGL2011-28681 and RYC–2009–04533 to D.M.A.), the Universidad Complutense de Madrid (BSCH-UCM910607) and the Generalitat de Catalunya (2009 SGR 754 GRC and 2014 SGR 416 GRC). J.A. thanks the ‘Proyecto Prometeo’ of the ‘Secretaria de Educación Superior, Ciencia Tecnología e Innovación’, Republic of Ecuador. A.V. is a researcher in formation in the CSIC program JAE-PRE_CP2011 (CSIC program ‘Junta para la ampliación de estudios’), co-funded by the European Social Fund and has received funding from the European Union’s Seventh Framework Programme (FP7/2007–2013) under grant agreement no. 226506 (SYNTHESYS; SE-TAF-3637), the USC School of Medicine (Columbia, South Carolina, USA) and the AMNH (Collection Study Grant Programme 2014). M.D.E. thanks the MACN for a PhD student grant. We are indebted to S. Roussiakis for photographs of the radial sesamoid of I. punjabiensis from Pikermi; to S. Wallace, M.A. Nieto Cambra, R. Portela Miguez, E. Westwig, D. Lunde, E. López Errasquin, D. Kalthoff, P. Moreno, F. Pastor, D. Flores and S. Lucero and D. Verzi and I. Olivares for the access to comparative material under their care; to M. Bastir (Paleoanthropology Group, MNCN, Spain) for the scans of the radius and ulna of I. arctoides; to Louis de Bonis for his recommendations on the manuscript; to Ó. Sanisidro for Fig. 1; and to the editors and the many reviewers who helped us to improve this manuscript.

Authors’ contribution

J.A., P.M. and J.M. conceived and designed the experiments. J.A., A.P.R. and A.V. performed the experiments. J.A., M.D.E. and A.V. analysed the data. J.A., A.V., A.P.R. and D.H. contributed reagents/materials/analysis tools. J.A., D.M.A. and J.M. wrote the paper.

Author information

Correspondence to Juan Abella.

Additional information

Communicated by: Sven Thatje

Electronic supplementary material

Below is the link to the electronic supplementary material.

Video showing the grasping action of the right forepaw, based on the fossil remains of Indarctos arctoides from Batallones 3. This video only shows the last phase of the movement, since supination of the forepaw and flexion of carpals and metacarpals occur prior to the digit flexion shown here. (AVI 2443 kb)

Supporting Information Table 1 (SIT 1)

List of taxa included in the comparative sample, which includes skeletons of extant and extinct carnivorans, showing sample size (N), species name, housing institution and catalogue number. (DOCX 153 kb)

Supporting information Video 1 (SIV1)

Video showing the grasping action of the right forepaw, based on the fossil remains of Indarctos arctoides from Batallones 3. This video only shows the last phase of the movement, since supination of the forepaw and flexion of carpals and metacarpals occur prior to the digit flexion shown here. (AVI 2443 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abella, J., Pérez-Ramos, A., Valenciano, A. et al. Tracing the origin of the panda’s thumb. Sci Nat 102, 35 (2015). https://doi.org/10.1007/s00114-015-1286-3

Download citation

Keywords

  • Cerro de los Batallones
  • Late Miocene
  • Radial sesamoid
  • Carnivora
  • Ursidae