Skip to main content

Advertisement

Log in

An Overview of Xenarthran Developmental Studies with a Focus on the Development of the Xenarthrous Vertebrae

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The mammalian clade Xenarthra (armadillos, anteaters, and sloths) has a long history in comparative anatomy. Here, we review past developmental studies on Xenarthra and extend previous observations on the development of one of their most iconic anatomical features, the xenarthrous vertebral articulations. While xenarthrous vertebrae have been known to researchers since the first descriptions of xenarthrans, intermediate vertebral conditions remain unknown in the fossil record, and uncertainty remains regarding the development of the involved articulations. We used developmental and morphological techniques to provide a novel developmental perspective on the evolution of xenarthrous morphology. Our results highlight that within the xenarthrous articulation, the early-developing metapophysis is the major component, and the anapophysis is the supplementary component, which is an arrangement with both functional and historical implications. Our observations do not support the theory of sacralization as the evolutionary origin of xenarthrous articulations.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Adam PJ (1999) Choloepus didactylus. Mammal Species 621:1–8

  • Adamoli VC, Cetica PD, Merani MS, Solari AJ (2001) Comparative morphologic placental types in Dasypodidae (Chaetophractus villosus, Cabassous chacoensis, Tolypeutes matacus, and Dasypus hybridus). Biocell 25:17–22

    CAS  PubMed  Google Scholar 

  • Asher RJ, Bennett N, Lehmann T (2009) The new framework for understanding placental mammal evolution. Bioessays 31:853–864. https://doi.org/10.1002/bies.200900053

    Article  CAS  PubMed  Google Scholar 

  • Asher RJ, Lehmann T (2008) Dental eruption in afrotherian mammals. BMC Biol 6:14. https://doi.org/10.1186/1741-7007-6-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. J Evol Biol. https://doi.org/10.1111/j.1420-9101.2011.02240.x

    Article  CAS  PubMed  Google Scholar 

  • Bagatto B, Crossley D, Burggren WW (2000) Physiological variability in neonatal armadillo quadruplets: within- and between-litter differences. J Exp Biol 203:1733–1740

    CAS  PubMed  Google Scholar 

  • Ballowitz E (1892) Das Schmelzorgan der Edentaten, seine Ausbildung im Embryo und die Persistenz seines Keimrandes bei dem erwachsenen Thier. Arch mikrosk Anat 40:133–156

    Article  Google Scholar 

  • Baverstock H, Jeffery N, Cobb SN (2013) The morphology of the mouse masticatory musculature. J Anat 223:46–60

    Article  PubMed  PubMed Central  Google Scholar 

  • Becher H (1921) Zur Kenntnis der Placenta yon Bradypus tridactylus. Z Anat Entwicklungsgesch 61:114–136

    Article  Google Scholar 

  • Becher H (1931) Placenta und uterusschleimhaut von Tamandua tetradactyla (Myrmecophaga). Gegenbaurs Morphol Jahrb 67:381–458

    Google Scholar 

  • Benirschke K (2008) Reproductive parameters and placentation in anteaters and sloths. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 160–171

    Google Scholar 

  • Benirschke K, Kaufmann P, Baergen R (2006) Pathology of the Human Placenta. Springer, New York

    Google Scholar 

  • Billet G, Hautier L, Muizon C de, Valentin X (2011) Oldest cingulate skulls provide congruence between morphological and molecular scenarios of armadillo evolution. Proc R Soc B Biol Sci 278:2791–2797. https://doi.org/10.1098/rspb.2010.2443

    Article  PubMed  PubMed Central  Google Scholar 

  • Böker H (1932) Beobachtungen und Untersuchungen an Säugetieren (einschließlich südamerikanischer Edentaten) während einer biologisch-anatomischen Forschungsreise nach Brasilien. Gegenbaurs Morphol Jahrb 70:1–66

  • Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evol Dev 79:69–79. https://doi.org/10.1111/j.1525-142X.2008.00303.x

    Article  Google Scholar 

  • Burke AC, Nowicki JL (2003) A new view of patterning domains in the vertebrate mesoderm. Dev Cell 4:159–165

    Article  CAS  PubMed  Google Scholar 

  • Ciancio MR, Castro MC, Galliari FC, Carlini AA, Asher RJ (2012) Evolutionary implications of dental eruption in Dasypus (Xenarthra). J Mammal Evol 19:1–8. https://doi.org/10.1007/s10914-011-9177-7

    Article  Google Scholar 

  • Cooper ZK (1930) A histological study of the integument of the armadillo, Tatusia novemcincta. Am J Anat 45:1–37

    Article  Google Scholar 

  • Cox PG, Jeffery N (2011) Reviewing the jaw-closing musculature in squirrels, rats and guinea pigs with contrast-enhanced microCT. Anat Rec 294:915–928

    Article  Google Scholar 

  • De Lange D (1926) Quelques remarques sur la placentation de Bradypus. Comptes Rendus l’Association des Anat Liège 321–333

  • Emerling CA, Springer MS (2015) Genomic evidence for rod monochromacy in sloths and armadillos suggests early subterranean history for Xenarthra. Proc R Soc B 282:2014.2192

    Article  Google Scholar 

  • Enders AC (1960a) Development and structure of the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat 94:34–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enders AC (1960b) Electron microscopic observations on the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat 94:205–215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enders AC (2002) Implantation in the nine-banded armadillo: how does a single blastocyst form four embryos? Placenta 23:71–85. doi: https://doi.org/10.1053/plac.2001.0753

    Article  CAS  PubMed  Google Scholar 

  • Enders AC (2008) Placentation in armadillos, with emphasis on development of the placenta in polyembryonic species. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 172–180

    Google Scholar 

  • Enders AC, Carter AM (2012) The evolving placenta: convergent evolution of variations in the endotheliochorial relationship. Placenta 33:319–326. https://doi.org/10.1016/j.placenta.2012.02.008

    Article  CAS  PubMed  Google Scholar 

  • Fernández M (1914) Zur Anordnung der Embryonen und Form der Placenta bei Tatusia novemcincta. Anat Anz 46:253–258

    Google Scholar 

  • Fernández M (1922) Sobre la histogénesis y filogenia de la caparaza ósea de desdentados. In: Libro en honor de D. S. Ramón y Cajal Tomo II. Publicaciones de la Junta para el homenaje a Cajal, Madrid, pp 385–406

  • Flower WH (1885) An Introduction to the Osteology of the Mammalia. MacMillan and Company, London,

    Book  Google Scholar 

  • Frechkop S (1949) Explication biologique, fournie par les tatous, d’un des caractères distinctifs des xénarthres et d’un caractère adaptif analogue chez les pangolins. Bull l’Institut R des Sci Nat Belgique 25:1–12

    Google Scholar 

  • Galis F (1999) Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J Exp Zool 285:19–26

    Article  CAS  PubMed  Google Scholar 

  • Galliari FC, Carlini AA (2015) Ontogenetic criteria to distinguish vertebral types on the debated xenarthran synsacrum. J Morphol 276:494–502. https://doi.org/10.1002/jmor.20356

    Article  PubMed  Google Scholar 

  • Galliari FC, Carlini AA, Sánchez-Villagra MR (2010) Evolution of the axial skeleton in armadillos (Mammalia, Dasypodidae). Mammal Biol 75:326–333. doi: https://doi.org/10.1016/j.mambio.2009.03.014

    Article  Google Scholar 

  • Gaudin TJ (1999) The morphology of the xenarthrous vertebrae (Mammalia: Xenarthra). Fieldiana Geol 41:1–38

    Google Scholar 

  • Gaudin TJ, Biewener AA (1992) The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra). J Morphol 214:63–81

    Article  CAS  PubMed  Google Scholar 

  • Gaudin TJ, Croft DA (2015) Paleogene Xenarthra and the evolution of South American mammals. J Mammal 96:622–634. https://doi.org/10.1093/jmammal/gyv073

    Article  Google Scholar 

  • Gervais P (1869) Zoologie et Paléontologie générales: Nouvelles Recherches sur les animaux vertébrés vivants et fossiles. Arthus Ber, Paris

    Google Scholar 

  • Gervais P (1873) Remarque au sujet du système dentaire de l’aï. J Zool 437–437

  • Gibb GC, Condamine FL, Kuch M, Enk J, Moraes-Barros N, Superina M, Poinar HN, Delsuc F (2016) Shotgun mitogenomics provides a reference phylogenetic framework and timescale for living xenarthrans. Mol Biol Evol 33:621–642. https://doi.org/10.1093/molbev/msv250

    Article  CAS  PubMed  Google Scholar 

  • Goffart M (1971) Function and Form in the Sloth. Pergamon Press, Oxford

    Google Scholar 

  • Hallström BM, Janke A (2010) Mammalian evolution may not be strictly bifurcating. Mol Biol Evol 27:2804–2816. https://doi.org/10.1093/molbev/msq166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton HK, Levis WR, Martiniuk F, Cabrera A, Wolf J (2008) The role of the armadillo and sooty mangabey monkey in human leprosy. Internatl J Dermatol 47:545–550. https://doi.org/10.1111/j.1365-4632.2008.03722.x

    Article  Google Scholar 

  • Hautier L, Bennett NC, Viljoen H, Howard L, Milinkovitch MC, Tzika AC, Goswami A, Asher RJ (2013) Patterns of ossification in southern versus northern placental mammals. Evolution 67:1994–2010. https://doi.org/10.1111/evo.12071

    Article  PubMed  Google Scholar 

  • Hautier L, Charles C, Asher RJ, Gaunt SJ (2014) Ossification sequence and genetic patterning in the mouse axial skeleton. J Exp Zool Part B Mol Dev Evol. doi: https://doi.org/10.1002/jez.b.22590

    Article  Google Scholar 

  • Hautier L, Gomes Rodrigues H, Billet G, Asher RJ (2016) The hidden teeth of sloths: evolutionary vestiges and the development of a simplified dentition. Sci Rep 6:27763

  • Hautier L, Stansfield FJ, Allen WRT, Asher RJ (2012) Skeletal development in the African elephant and ossification timing in placental mammals. Proc R Soc B Biol Sci 279:2188–2195. https://doi.org/10.1098/rspb.2011.2481

    Article  PubMed  PubMed Central  Google Scholar 

  • Hautier L, Weisbecker V, Goswami A, Knight F, Kardjilov N, Asher RJ (2011) Skeletal ossification and sequence heterochrony in xenarthran evolution. Evol Dev 13:460–476. doi: https://doi.org/10.1111/j.1525-142X.2011.00503.x

    Article  Google Scholar 

  • Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Natl Acad Sci USA 107:18903–18908. https://doi.org/10.1073/pnas.1010335107

    Article  PubMed  PubMed Central  Google Scholar 

  • Hayssen V (2009) Bradypus tridactylus (Pilosa: Bradypodidae). Mammal Species 839:1–9. https://doi.org/10.1644/839.1.Key

    Article  Google Scholar 

  • Hayssen V (2010) Bradypus variegatus (Pilosa: Bradypodidae). Mammal Species 42:19–32. https://doi.org/10.1644/850.1.Key

    Article  Google Scholar 

  • Hayssen V (2011a) Tamandua tetradactyla (Pilosa: Myrmecophagidae). Mammal Species 43:64–74. https://doi.org/10.1644/875.1

    Article  Google Scholar 

  • Hayssen V (2011b) Choloepus hoffmanni (Pilosa: Megalonychidae). Mammal Species 43:37–55. https://doi.org/10.1644/873.1

    Article  Google Scholar 

  • Head JJ, Polly PD (2015) Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature 520:86–89. https://doi.org/10.1038/nature14042

    Article  CAS  PubMed  Google Scholar 

  • Hensel R (1872) Beiträge zur Kenntnis der Säugethiere Süd-Brasiliens. Abhandlungen der Königl Akademie der Wissenschaften, Berlin

    Book  Google Scholar 

  • Hill R V (2006) Comparative anatomy and histology of xenarthran osteoderms. J Morphol 1460:1441–1460. https://doi.org/10.1002/jmor

    Article  Google Scholar 

  • Jeffery NS, Stephenson R, Gallagher JA, Jarvis JC, Cox PG (2011) Micro-computed tomography with iodine staining reveals the arrangement of muscle fibres. J Biomech 44:189–192

    Article  PubMed  Google Scholar 

  • Jenkins FA Jr (1970) Anatomy and function of expanded ribs in certain edentates and primates. J Mammal 51:288–301

    Article  PubMed  Google Scholar 

  • Jones KE, Bielby J, Cardillo M, Fritz SA, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster C a., Price S a., Rigby E a., Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648–2648. https://doi.org/10.1890/08-1494.1

    Article  Google Scholar 

  • King BF, Pinheiro PBN, Hunter RL (1982) The fine structure of the placental labyrinth in the sloth, Bradypus tridactylus. Anat Rec 202:15–22. https://doi.org/10.1002/ar.1092020104

    Article  CAS  PubMed  Google Scholar 

  • Krmpotic CM, Galliari FC, Barbeito CG, Carlini AA (2012) Development of the integument of Dasypus hybridus and Chaetophractus vellerosus, and asynchronous events with respect to the postcranium. Mammal Biol 77:314–326. https://doi.org/10.1016/j.mambio.2012.02.008

    Article  Google Scholar 

  • Lebrun R (2014) ISE-MeshTools, a 3D interactive fossil reconstruction freeware. In: 12th Annual Meeting of EAVP, Torino

  • Leche W (1892) Studien über die Entwicklung des Zahnsystems bei den Saügethieren. Gegenbaurs Morphol Jahrb 19:502–547

  • Li J, Miller MA, Hutchins GD, Burr DB (2005) Imaging bone microdamage in vivo with positron emission tomography. Bone 37:819–824

    Article  PubMed  Google Scholar 

  • Limaye A (2006) Drishti - Volume Exploration and Presentation Tool. Poster presentation,Vis 2006, Baltimore 

  • Loughry WJ, McDonough CM (2013) The Nine-banded Armadillo: A Natural History. University of Oklahoma Press, Norman

    Google Scholar 

  • MacPhee RDE (1994) Morphology, adaptations, and relationships of Plesiorycteropus, and a diagnosis of a new order of eutherian mammals. Bull Am Mus Nat Hist 220:1–214

    Google Scholar 

  • Maroy R, Boisgard R, Comtat C, Frouin V, Cathier P, Duchesnay E, Dollé F, Nielsen PE, Trébossen R, Tavitian B (2008) Segmentation of rodent whole-body dynamic PET images: an unsupervised method based on voxel dynamics. IEEE Trans Med Imaging 27:342–354. https://doi.org/10.1109/TMI.2007.905106

    Article  PubMed  Google Scholar 

  • Martin BE (1916) Tooth development in Dasypus novemcinctus. J Morphol 27:647–691.

    Article  Google Scholar 

  • Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub N a, Springer MS, Murphy WJ (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334:521–524. https://doi.org/10.1126/science.1211028

    Article  CAS  PubMed  Google Scholar 

  • Mess AM, Favaron PO, Pfarrer C, Osmann C, Melo APF, Rodrigues RF, Ambrósio CE, Bevilacqua E, Miglino MA (2012) Placentation in the anteaters Myrmecophaga tridactyla and Tamandua tetradactyla (Eutheria, Xenarthra). Reprod Biol Endocrinol 10:102. https://doi.org/10.1186/1477-7827-10-102

    Article  PubMed  PubMed Central  Google Scholar 

  • Milinkovitch M, Tzika A (2007) Escaping the mouse trap; the selection of new evo-devo model species. J Exp Zool Part B Mol Dev Evol 308:337–346

    Article  Google Scholar 

  • Müller J, Scheyer TM, Head JJ, Barrett PM, Werneburg I, Ericson PGP (2010) Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc Natl Acad Sci USA 107:2118–2123. https://doi.org/10.1073/pnas.0912622107

    Article  Google Scholar 

  • Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 17:413–421. https://doi.org/10.1101/gr.5918807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narita Y, Kuratani S (2005) Evolution of the vertebral formulae in mammals: a perspective on developmental constraints. J Exp Zool Part B Mol Dev Evol 106:91–106. https://doi.org/10.1002/jez.b.21029

    Article  Google Scholar 

  • Navarrete D, Ortega J (2011) Tamandua mexicana (Pilosa: Myrmecophagidae). Mammal Species 43:56–63. https://doi.org/10.1644/874.1

    Article  Google Scholar 

  • Newman HH, Patterson JT (1910) The development of the nine-banded armadillo from the primitive streak stage to birth; with especial reference to the question of specific polyembryony. J Morphol 21:359–423

    Article  Google Scholar 

  • Nowak RM (1999) Walker’s Mammals of the World, Sixth edition. The Johns Hopkins University Press, Baltimore and London

    Google Scholar 

  • Oliver JD, Jones KE, Hautier L, Loughry WJ, Pierce SE (2016) Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus). J Exp Biol 219:2991–3002. https://doi.org/10.1242/jeb.142331

    Article  PubMed  Google Scholar 

  • Parker WK (1885) On the structure and development of the skull in Mammalia. Part II. Edentata. Phil Trans R Soc Lond 176:1–119

    Article  Google Scholar 

  • Pouchet G, Chabry L (1884) Contribution à l’odontologie des mammifères. J l’Anatomie la Physiol 20:149–192

    Google Scholar 

  • Prasad AB, Allard MW, Program NC sequencing, Green ED (2008) Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol Biol Evol 25:1795–1808. https://doi.org/10.1093/molbev/msn104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prodöhl PA, Loughry WJ, McDonough CM, Nelson WS, Avise JC (1996) Molecular documentation of polyembryony and the micro-spatial dispersion of clonal sibships in the nine-banded armadillo, Dasypus novemcinctus. Proc Biol Sci 263:1643–1649. https://doi.org/10.1098/rspb.1996.0240

    Article  PubMed  Google Scholar 

  • Redford KH, Eisenberg J (1992) Mammals of the Neotropics, Volume II. University of Chicago Press, Chicago

    Google Scholar 

  • Rezende LC, Barbeito CG, Favaron PO, Mess A, Miglino MA (2012) The fetomaternal interface in the placenta of three species of armadillos (Eutheria, Xenarthra, Dasypodidae). Reprod Biol Endocrinol 10:38. https://doi.org/10.1186/1477-7827-10-38

    Article  PubMed  PubMed Central  Google Scholar 

  • Röse C (1892) Beiträge zur Zahnentwickling der Edentaten. Anat Anz 7:495–512

    Google Scholar 

  • Rose KD, Emry RJ (1993) Relationships of Xenarthra, Pholidota, and fossil “edentates”: The morphological evidence. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny, Placentalia. Springer Verlag, New York pp 81–102

    Chapter  Google Scholar 

  • Russell RJ (1953) Description of a new armadillo (Dasypus novemcinctus) from Mexico with remarks on geographic variation of the species. Proc Biol Soc Washingt 66:21–26

    Google Scholar 

  • Simon L (1902) Beiträge Anatomie und Entwicklung der Bradypodiden. Arch fur Naturgesh 68:239–260

    Google Scholar 

  • Simpson GG (1948) The beginning of the age of mammals in South America. Part 1. Introduction. Systematics: Marsupialia, Edentata, Condylartha, Litopterna and Notioprogonia. Bull Am Mus Nat Hist 91:1–232

    Google Scholar 

  • Spurgin AM (1904) Enamel in the teeth of an embryo edentate (Dasypus novemcinctus Linn). Am J Anat 3:75–84

    Article  Google Scholar 

  • Stephenson RS, Boyett MR, Hart G, Nikolaidou T, Cai X, Corno AF, Alphonso N, Jeffery N, Jarvis JC (2012) Contrast enhanced micro-computed tomography resolves the 3-dimensional morphology of the cardiac conduction system in mammalian hearts. PLoS One 7:1–11. https://doi.org/10.1371/journal.pone.0035299

    Article  CAS  Google Scholar 

  • Storrs EE, Williams RJ (1968) A study of monozygous quadruplet armadillos in relation to mammalian inheritance. Proc Natl Acad Sci USA 60:910–914. https://doi.org/10.1073/pnas.60.3.910

    Article  CAS  Google Scholar 

  • Strahl H (1913) Ueber den Bau der Plazenta von D. novemcinctus. Anat Anz 44:440–447

    Google Scholar 

  • Superina M, Carreño N, Jahn GA (2009) Characterization of seasonal reproduction patterns in female pichis Zaedyus pichiy (Xenarthra: Dasypodidae) estimated by fecal sex steroid metabolites and ovarian histology. Anim Reprod Sci 116:358–369. https://doi.org/10.1016/j.anireprosci.2009.02.015

    Article  CAS  PubMed  Google Scholar 

  • Thomas O (1889) A milk dentition in Orycteropus. Proc R Soc Lond 47:246–248

    Article  Google Scholar 

  • Tomes CS (1874) On the existence of an enamel organ in an armadillo (Tatusia peba). Q J Microsc Sci 53:44–48

    Google Scholar 

  • Turner W (1873) On the placentation of the sloths. Trans R Soc Edinburgh 27:71–104.

    Article  Google Scholar 

  • Vaska P, Woody CL, Schlyer DJ, Shokouhi S, Stoll SP, Pratte JF, O’Connor P, Junnarkar SS, Rescia S, Yu B, Porschke M, Kandasamy A, Villanueva A, Kriplani A, Radeka V, Volkow N, Lecomte R, Fontaine R (2004) RatCAP: miniaturized head-mounted PET for conscious rodent brain imaging. IEEE Trans Nucl Sci 51:2718–2722. https://doi.org/10.1109/TNS.2004.835740

    Article  Google Scholar 

  • Vickaryous MK, Hall BK (2006) Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus. J Morphol 267:1273–1283. https://doi.org/10.1002/jmor

    Article  PubMed  Google Scholar 

  • Vizcaíno SF (2009) The teeth of the ‘toothless’: novelties and key innovations in the evolution of xenarthrans (Mammalia, Xenarthra). Paleobiology 35:343–366

    Article  Google Scholar 

  • Vizcaíno SF, Zárate M, Bargo MS, Dondas A (2001) Pleistocene burrows in the Mar del Plata area (Argentina) and their probable builders. Acta Palaeontol Pol 46:289–301

    Google Scholar 

  • Walls EW (1939) Myrmecophaga jubata: an embryo with placenta. J Anat 73:311–317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werneburg I, Tzika AC, Hautier L, Asher RJ, Milinkovitch MC, Sánchez-Villagra MR (2013) Development and embryonic staging in non-model organisms: the case of an afrotherian mammal. J Anat 222:2–18. https://doi.org/10.1111/j.1469-7580.2012.01509.x

    Article  PubMed  Google Scholar 

  • Wildman DE, Uddin M, Opazo JC, Liu G, Lefort V, Guindon S, Gascuel O, Grossman LI, Romero R, Goodman M (2007) Genomics, biogeography, and the diversification of placental mammals. Proc Natl Acad Sci USA 104:14395–14400. https://doi.org/10.1073/pnas.0704342104

    Article  CAS  Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore

  • Wislocki GB (1927) On the placentation of the tridactyl sloth (Bradypus griseus) with a description of the characters of the fetus. Contrib Embryol 19:211–227

    Google Scholar 

  • Wislocki GB (1928a) Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus griseus Gray and Choloepus hoffmanni Peters). J Morphol 46:317–397. https://doi.org/10.1002/jmor.1050460202

    Article  Google Scholar 

  • Wislocki GB (1928b) Further observations upon the minute structure of the labyrinth in the placenta of the sloths. Anat Rec 40:385–395

    Article  Google Scholar 

  • Wislocki GB (1928c) On the placentation of th two-toed anteater (Cyclopes didactylus). Anat Rec 39:69–83

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Peter Giere and Frieder Mayer (Museum für Naturkunde, Berlin), G. Verdon, M. Herbin, C. Bens, F. Renoult, C. Denys, and J. Cuisin (Museum National d’Histoire Naturelle, Paris), Roberto Portela Miguez and Louise Tomsett (Natural History Museum, London), Georges Lenglet (Institut Royal des Sciences Naturelles de Belgiques, Brussels), and their colleagues for access to comparative material. For access to material and facilities, we thank Richard Truman (LSU School of Veterinary Medicine, Baton Rouge, Louisiana), the Laboratory of Paleontology and the Institut des Sciences de l’Evolution de Montpellier. A. Heaver (University of Cambridge), Nikolai Kardjilov, and all the staff of the Helmholtz Zentrum (Berlin), R. Abel and R. Garwood (Natural History Museum, London), R. Lebrun (Institut des Sciences de l’Evolution de Montpellier), Ross MacPhee, Nicole Edmison, and James Thostenson (American Museum of Natural History, New York), Blake Dickson (Museum of Comparative Zoology, Cambridge), F. Landru, C. Morlier, G. Guillemain, and all the staff from Viscom SARL (St Ouen l’Aumône, France) provided generous help and advice with acquisition of CT scans. We also thank Sérgio Ferreira Cardoso for his help with the bibliography. LH warmly thanks Robert Asher (University of Cambridge, UK) for introducing him to the development of xenarthrans. We thank two anonymous reviewers and John Wible for their valuable comments on the manuscript. Access to the Helmholtz Zentrum Berlin was facilitated by the European Commission under the 7th Framework Programme through the “Research Infrastructures” action of the “Capacities” Programme, Contract No CP-CSA_INFRA-2008-1.1.1, number ZZ6507-NMI3. For support of the project as a whole, we acknowledge a research grant (F/09 364/I) from the Leverhulme Trust, UK. This work has benefited from an “Investissements d’Avenir’ grant managed by Agence Nationale de la Recherche, France (CEBA, ref. ANR-10-LABX-25-01). This research received support from the Synthesys Project http://synthesys3.myspecies.info/ which is financed by the European Community Research Infrastructure Action under the FP7. Some of the experiments were performed using the μ-CT facilities of the Montpellier Rio Imaging (MRI) platform and of the LabEx CeMEB. This publication is a contribution of the Institut des Sciences de l’Evolution de Montpellier (UMR 5554 – UM + CNRS + IRD + EPHE) No. ISEM 2017-181.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lionel Hautier.

Electronic supplementary material

Table S1

All examined and described specimens. Institutional abbreviations: BMNH, The Natural History Museum, London; IRSN, Institut Royal des Sciences Naturelles, Brussels; MNHN, Muséum National d’Histoire Naturelle, Paris; PMLER, Paul Mellon Laboratory of Equine Reproduction, Newmarket, UK; UCL, University College London, London; UMZC, University Museum of Zoology, Cambridge; UP, University of Pretoria; USNM, United States National Museum of Natural History, Smithsonian Institution, Washington, D.C.; ZMB, Museum für Naturkunde, Berlin. (DOCX 91 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hautier, L., Oliver, J.D. & Pierce, S.E. An Overview of Xenarthran Developmental Studies with a Focus on the Development of the Xenarthrous Vertebrae. J Mammal Evol 25, 507–523 (2018). https://doi.org/10.1007/s10914-017-9412-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-017-9412-y

Keywords

Navigation