Placentation in the anteaters Myrmecophaga tridactyla and Tamandua tetradactyla (Eutheria, Xenarthra)

Reproductive Biology and Endocrinology

Maria A Miglino⁵  Estela Bevilacqua¹  Carlos E Ambrósio⁴  Rosangela F Rodrigues⁵  Allan PF Melo⁵  Christine Osmann³  Christiane Pfarrer²  Phelipe O Favaron⁵  Andrea M Mess⁵ 

[1] Institute of Biomedical Sciences, University of Sao Paulo, Av. Prof. Lineu Prestes, 1524, Cidade Universitária, São Paulo, SP, CEP 05508-900, Brazil;Institute of Anatomy, University of Veterinary Medicine Hannover, Bischofsholer Damm 15, 30173, Hannover, Germany;Zoo Dortmund, Mergelteichstr. 80, 44225, Dortmund, Germany;Department of Basic Science, Faculty of Animal Sciences and Food Engineering, University of Sao Paulo, Av. Duque de Caxias Norte, 225, ZAB, Pirassununga, CEP 13635-900, Brazil;Department of Surgery, Faculty of Veterinary Medicine and Animal Science, University of Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, Cidade Universitária, São Paulo, SP, CEP 05508-270, Brazil

关键词: Villous placenta;    Interhaemal barrier;    Trophoblast;    Vermilingua;    Evolution;   

Others  :  1149712
DOI  :  10.1186/1477-7827-10-102

 received in 2012-09-05, accepted in 2012-11-16,  发布年份 2012

【 摘 要 】

Background

Since Xenarthra are serious candidates for being basal to Eutheria, their characteristics, e.g. the placental system, influence perceptions of evolution. However, in the subgroup containing the anteaters, data are very limited. The present study aims to elucidate the nature of the feto-maternal interface in the anteater placenta and to interpret these data within an evolutionary context.

Methods

Placentas of two species were investigated with histology, immunohistochemistry and transmission electron microscopy.

Results

Remnants of the maternal vessel endothelium were absent, resulting in a fully haemochorial barrier throughout the placenta. Two structurally different parts, the villous and trabecular areas were complex and intermingled. In particular, the trabeculae which consisted of cellular, proliferative trophoblast, associated with connective tissue, were attached to the decidua. The villi contained fetal capillaries and hypertrophied mesenchymal cells that occured near the surface near the end of gestation. The surface of the villi consisted of flat, syncytial trophoblast, interspersed with proliferative trophoblast cells.

Conclusions

Based on fundamental differences between anteaters and armadillos, we inferred that placental evolution was more complex than previously thought. The haemochorial pattern of anteaters was likely an ancient condition of xenarthrans. Consequently, villous placentation may be attributed, at least in part, by convergent evolution, but was also characterized by some features that were widespread among xenarthrans.

【 授权许可】

   
2012 Mess et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Delsuc F, Douzery EJP: Recent advances and future prospects in xenarthran molecular genetics. In The biology of the xenarthra. Edited by Vizcaíno SFL, Loughry WJ. Gainesville: University Press of Florida; 2008:11-23.
• [2]Gaudin TJ, McDonald HG: Morphology-based investigations of the phylogenetic relationships among extant and fossil xenarthrans. In The biology of the xenarthra. Edited by Vizcaíno SFL, Loughry WJ. Gainesville: University Press of Florida; 2008:24-36.
• [3]Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ: Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 2011, 334:521-524.
• [4]Montgomery GG: The evoluion and ecology of armadillos, sloths, and vermilinguas. Washington: Smithsonian Institution; 1985.
• [5]Osmann C: Ordnung nebengelenktiere. In Zootierhaltung. Edited by Puschmann W. Frankfurt a.M: Verlag Harri Deutsch; 2004:253-265.
• [6]Wilson DE, Reeder DM: Mammal species of the world. Baltimore: Johns Hopkins University Press; 2005.
• [7]Redford KH, Eisenberg JF: Mammals of the neotropics. The southern cone. Chile, argentinia, uruguay, paraguay. Illinois: University of Chicago Press; 1992.
• [8]Eisenberg JF, Redford KH: Mammals of the neotropics: the central neotropics. Ecuador, Peru, Bolivia, brazil. Chicago: University of Chicago Press; 1999.
• [9]Redford KH: The edentates of the cerrado. Edentata 1994, 1:4-10.
• [10]Emmons LH, Feer F: Neotropical rainforest mammals: A field guide. Chicago: The University of Chicago Press; 1990.
• [11]Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ: Molecular phylogenetics and the origins of placental mammals. Nature 2001, 409:614-618.
• [12]Springer MS, Stanhope MJ, Madsen O, Jong WW: Molecules consolidate the placental mammal tree. Trends Ecol Evol 2004, 19:430-438.
• [13]Springer MS, Murphy WJ: Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev 2007, 82:375-392.
• [14]Delsuc F, Scally M, Madsen O, Stanhope MJ, Jong WW, Catzeflis FM, Springer MS, Douzery EJP: Molecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Mol Biol Evol 2002, 19:1656-1671.
• [15]Mess A, Carter AM: Evolutionary transformations of fetal membrane characters in eutheria with special reference to afrotheria. J Exp Zool B Mol Dev Evol 2006, 306:140-163.
• [16]Mess A, Carter AM: Evolution of the placenta during the early radiation of placental mammals. Comp Biochem Physiol A Comp Physiol 2007, 148:769-779.
• [17]Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R: Evolution of the mammalian placenta revealed by phylogenetic analysis. PNAS 2006, 103:3203-3208.
• [18]Elliot MG, Crespi BJ: Phylogenetic evidence for early hemochorial placentation in eutheria. Placenta 2009, 30:49-67.
• [19]Capellini I: The evolutionary significance of placental interdigitation in mammalian reproduction: contributions from comparative studies. Placenta 2012, 33:763-768.
• [20]Strahl VH: Über den Bau der placenta von dasypus novemcinctus. Anat Anz 1913, 44:440-447.
• [21]Fernández M: Zur anordnung der embryonen und form der placenta bei Tatusia novemcincta. Anat Anz 1914, 46:253-258.
• [22]Enders AC: Development and structure of the villous haemochorial placenta of the nine-banded armadillo (dasypus novemcinctus). J Anat 1960, 94:34-45.
• [23]Enders AC: Electron microscopic observations on the villous haemochorial placenta of the nine-banded armadillo (dasypus novemcinctus). J Anat 1960, 94:205-215.
• [24]Adamoli VC, Cetica PD, Merani MS, Solari AJ: Comparative morphologic placental types in dasypodidae (chaetophractus villosus, cabassous chacoensis, Tolypeutes matacus and dasypus hybridus). Biocell 2001, 25:17-22.
• [25]Enders AC: Placentation in armadillos, with emphasis on development of the placenta in polyembryonic species. In The biology of the xenarthra. Edited by Vizcaíno SFL, Loughry WJ. Gainesville: University Press of Florida; 2008:172-180.
• [26]Rezende LC, Barbeito CG, Mess A, Favaron PO, Miglino MA: The fetomaternal interface in the placenta of three species of armadillos (eutheria, xenrthra, dasypodidae). Reprod Biol Endocrinol 2012, 10:38. BioMed Central Full Text
• [27]Enders AC, Carter AM: The evolving placenta: different developmental paths to a hemochorial relationship. Placenta 2012, 33:S92-S98.
• [28]Turner W: The placenta in the sloth. J Anat Physiol 1879, 14:147-148.
• [29]King BF, Pinheiro PB, Hunter RL: The fine structure of the placental labyrinth in the sloth, bradypus tridactylus. Anat Rec 1982, 202:15-22.
• [30]Enders AC, Carter AM: The evolving placenta: convergent evolution of variations in the endotheliochorial relationship. Placenta 2012, 33:319-326.
• [31]Carter AM, Mess AM: Conservation of placentation during the tertiary radiation of mammals in south America. J MorpholIn press
• [32]Walls EW: Myrmecophaga jubata: an embryo with placenta. J Anat 1939, 73:311-317.
• [33]Benirschke K: [http://placentation.ucsd.edu] webciteGiant anteater. 2007. [Myrmecophaga tridactyla]
• [34]Wislocki GB: On the placentation of the two-toed anteater (Cyclopes didactylus). Anat Rec 1928, 39:69-79.
• [35]Becher H: Placenta und uterusschleimhaut von Tamandua tetradactya (Myrmecophaga). Gegenbaurs Morphol Jahrb 1931, 67:381-458.
• [36]Schauerte N: Untersuchungen zur zyklus- und graviditätsdiagnostik beim großen ameisenbären (myrmecophaga tridactyla). Gießen: Justus-Liebig-Universität, PhD Thesis; 2005.
• [37]Schauerte N, Osmann C: Reproducao de tamanduas em cativeiro. In Manutencao de tamanduas em cativeiro Edited by Miranda F. 2012, 134-145.
• [38]Oliveira MF, Favaron PO, Ambrosio CE, Miglino MA, Mess A: Chorioallantoic and yolk sac placentation in thrichomys laurentinus (echimyidae) and the evolution of hystricognath rodents. J Exp Zool B Mol Dev Evol 2012, 318:13-25.