Skip to main content

Advertisement

SpringerLink
Log in

Evo-Devo of the Mammary Gland

  • Published:
Journal of Mammary Gland Biology and Neoplasia Aims and scope Submit manuscript

Abstract

We propose a new scenario for mammary evolution based on comparative review of early mammary development among mammals. Mammary development proceeds through homologous phases across taxa, but evolutionary modifications in early development produce different final morphologies. In monotremes, the mammary placode spreads out to form a plate-like mammary bulb from which more than 100 primary sprouts descend into mesenchyme. At their distal ends, secondary sprouts develop, including pilosebaceous anlagen, resulting in a mature structure in which mammary lobules and sebaceous glands empty into the infundibula of hair follicles; these structural triads (mammolobular-pilo-sebaceous units or MPSUs) represent an ancestral condition. In marsupials a flask-like mammary bulb elongates as a sprout, but then hollows out; its secondary sprouts include hair and sebaceous anlagen (MPSUs), but the hairs are shed during nipple formation. In some eutherians (cat, horse, human) MPSUs form at the distal ends of primary sprouts; pilosebaceous components either regress or develop into mature structures. We propose that a preexisting structural triad (the apocrine-pilo-sebaceous unit) was incorporated into the evolving mammary structure, and coupled to additional developmental processes that form the mammary line, placode, bulb and primary sprout. In this scenario only mammary ductal trees and secretory tissue derive from ancestral apocrine-like glands. The mammary gland appears to have coopted signaling pathways and genes for secretory products from even earlier integumentary structures, such as odontode (tooth-like) or odontode-derived structures. We speculate that modifications in signal use (such as PTHrP and BMP4) may contribute to taxonomic differences in MPSU development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

APSU:

Apo-pilo-sebaceous unit

BMP:

Bone morphogenic protein

CRL:

Crown-rump length

EDA:

Ectodysplasin

FGF:

Fibroblast growth factor

Ihh:

Indian hedgehog

MB:

Mammary bulb

MG:

Mammary gland

ML:

Mammary line

MP:

Mammary placode

MPSU:

Mammolobular-pilo-sebaceous unit

mya:

Million years ago

PS:

Primary sprout

PTHrP:

Parathyroid hormone-related protein

SG:

Sebaceous gland

Shh:

Sonic hedgehog

SS:

Secondary sprout

References

  1. Oftedal OT. The evolution of milk secretion and its ancient origins. Animal. 2012;6:355–68.

    Article  CAS  PubMed  Google Scholar 

  2. Oftedal OT. Origin and evolution of the major constituents of milk. In: McSweeney PLH, Fox PF, editors. Advanced dairy chemistry: volume 1A: proteins. Basic aspects. Boston: Springer US; 2013. p. 1–42.

    Google Scholar 

  3. Benton MJ. Vertebrate paleontology. 3rd ed. Malden: Blackwell Publishing; 2005.

    Google Scholar 

  4. Kemp TS. The origin and evolution of mammals. New York: Oxford University Press; 2005.

    Google Scholar 

  5. Luo Z-X, Yuan CX, Meng Q-J, Ji Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature. 2011;476:442–5.

    Article  CAS  PubMed  Google Scholar 

  6. Clack JA. Gaining ground. The origin and evolution of tetrapods. 2nd ed. Bloomington: Indiana University Press; 2012.

    Google Scholar 

  7. Wells KD. The ecology and behavior of amphibians. Chicago: University of Chicago Press; 2007.

    Book  Google Scholar 

  8. Oftedal OT. The origin of lactation as a water source for parchment-shelled eggs. J Mammary Gland Biol Neoplasia. 2002;7(3):253–66.

    Article  PubMed  Google Scholar 

  9. Oftedal OT. The mammary gland and its origin during synapsid evolution. J Mammary Gland Biol Neoplasia. 2002;7(3):225–52.

    Article  PubMed  Google Scholar 

  10. Dhouailly D. A new scenario for the evolutionary origin of hair, feather, and avian scales. J Anat. 2009;214(4):587–606.

    Article  PubMed  Google Scholar 

  11. Lemay DG, Lynn DJ, Martin WF, Neville MC, Casey TM, Rincon G, et al. The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biol. 2009;10(4):R43. doi:10.1186/gb-2009-10-4-r43.

    Article  PubMed  CAS  Google Scholar 

  12. Chapman RE. Hair, wool, quill, nail, claw, hoof, and horn. In: Bereiter-Hahn J, Matolstoy AG, Richards KS, editors. Biology of the integument. 2. Vertebrates. Berlin: Springer Verlag; 1986. p. 293–317.

    Chapter  Google Scholar 

  13. Craigmyle MBL. The apocrine glands and the breast. New York: John Wiley and Sons; 1984.

    Google Scholar 

  14. Veltmaat JM, Mailleux AA, Thiery JP, Bellusci S. Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation. 2003;71:1–17.

    Article  CAS  PubMed  Google Scholar 

  15. Vorherr H. The breast. Morphology, physiology and lactation. New York: Academic; 1974.

    Google Scholar 

  16. Anderson R. Embryonic and fetal development of the mammary apparatus. In: Larson B, editor. Lactation: a comprehensive treatise. Volume IV. The mammary gland/ human lactation/ milk synthesis. New York: Academic; 1978. p. 3–40.

    Google Scholar 

  17. Griffiths M. Biology of the monotremes. New York: Academic; 1978.

    Google Scholar 

  18. Bresslau E. Die Entwickelung des Mammarapparates der Monotremen, Marsupialier und einiger Placentalier. Ein Beitrag zur Phylogenie der Saugethiere. I. Entwickelung und Ursprung des Mammarapparates von Echidna. Denskschr Med-Naturwiss Gesellsch Jena. 1907;7(5):455–518. plates 28–30.

    Google Scholar 

  19. Griffiths M, Elliott MA, Leckie RMC, Schoefl GI. Observations of the comparative anatomy and ultrastructure of mammary glands and on the fatty acids of the triglycerides in platypus and echidna milk fats. J Zool. 1973;169:255–79.

    Article  CAS  Google Scholar 

  20. Nilsson M, Churakov G, Sommer M, Tran N, Zemann A, Brosius J, et al. Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol. 2010;8:e1000436. doi:10.1371/journal.pbio.1000436.

    Article  PubMed  CAS  Google Scholar 

  21. Hughes R, Hall L. Structural adaptations of the newborn marsupial. In: Tyndale-Biscoe CH, Janssens P, editors. The developing marsupial. Models for biomedical research. Berlin: Springer Verlag; 1988. p. 8–27.

    Chapter  Google Scholar 

  22. Bresslau E. Die Entwickelung des Mammarapparates der Monotremen, Marsupialier und einiger Placentalier. III. Entwickelung des Mammarapparates der Marsupialier, Insectivoren, Nagathiere, Carnivoren und Wiederkäuer. Denskschr Med-Naturwiss Gesellsch Jena. 1912;7(5):647–874. plates 37–46.

    Google Scholar 

  23. Tyndale-Biscoe H, Renfree M. Reproductive physiology of marsupials. Cambridge: Cambridge University Press; 1987.

    Book  Google Scholar 

  24. Green B, Merchant J. The composition of marsupial milk. In: Tyndale-Biscoe CH, Janssens PA, editors. The developing marsupial. Models for biomedical research. Berlin: Springer Verlag; 1988. p. 41–54.

    Chapter  Google Scholar 

  25. Bresslau E. Beiträge zur Entwicklungsgeschichte der Mammarorgane bei den Beutelthieren. Z Morphol Anthropol. 1902;4:261–317.

    Google Scholar 

  26. Griffiths M, McIntosh D, Leckie RMC. The mammary glands of the red kangaroo with observations on the fatty acid components of the milk triglycerides. J Zool. 1972;166:265–75.

    Article  CAS  Google Scholar 

  27. Cowin P, Wysolmerski J. Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb Perspect Biol. 2011;2:a003251. doi:10.1101/cshperspect.a003251.

    Article  CAS  Google Scholar 

  28. Turner CW. The mammary gland. I. The anatomy of the udder of cattle and domestic animals. Columbia: Lucas Brothers; 1952.

    Google Scholar 

  29. Raynaud A. Morphogenesis of the mammary gland. In: Kon S, Cowie A, editors. Milk: the mammary gland and its secretion. New York: Academic; 1961. p. 3–46.

    Google Scholar 

  30. Rowson AR, Daniels KM, Ellis SE, Hovey RC. Growth and development of the mammary glands of livestock: a veritable barnyard of opportunities. Semin Cell Dev Biol. 2012;23:557–66.

    Article  PubMed  Google Scholar 

  31. Uehlinger P. Studien zur Entwicklung der Milchdrüse des Pferdes. 11. Beitrag zum Bau und zur Entwicklung von Hautorganen bei Saugetieren. Inaugural-Dissertation zur Erlangung der Doctor-Würde. Zurich: University of Zurich; 1922.

  32. Profé O. Beiträge zur Ontogenie und Phylogenie der Mammarorgane. Anat Hefte. 1899;11:245–86.

    Google Scholar 

  33. Rein G. Untersuchungen über die embryonale Enwicklungsgeschichte der Milchdrüse. II. Vergleichend-anatomische Ergebnisse und Schlussresultate. Arch Mikrosk Anat. 1882;21:678–94. plate 30.

    Article  Google Scholar 

  34. Hamburger C. Studien zur Entwickelung der Mammarorgane. I. Die Zitze von Pferd und Esel. Anat Anz. 1900;18:16–26.

    Google Scholar 

  35. Brouha M. Recherches sur les diverses phases du développement et de l’activité de la mamelle. Arch Biol. 1905;21:459–603. plates 18–20.

    Google Scholar 

  36. Dabelow A. Die Milchdrüse. In: von Möllendorff W, Bargmann W, editors. Handbuch der mikroskopischen Anatomie des Menschen. Dritter Band, Haut und Sinnesorgane. Dritter Teil, die Haut die Milchdrüse. Berlin: Springer Verlag; 1957. p. 277–485.

    Google Scholar 

  37. Jolicoeur F. Intrauterine breast development and the mammary myoepithelial lineage. J Mammary Gland Biol Neoplasia. 2005;10:199–210.

    Article  PubMed  Google Scholar 

  38. Ba G, Stein T. Human breast development. Semin Cell Dev Biol. 2012;23:567–73.

    Article  Google Scholar 

  39. Howard BA, Gusterson BA. Human breast development. J Mammary Gland Biol Neoplasia. 2000;5:119–37.

    Article  CAS  PubMed  Google Scholar 

  40. Russo J, Russo IH. Development of the human mammary gland. In: Neville MC, Daniel CW, editors. The mammary gland. Development, regulation and function. New York: Plenum Press; 1987. p. 67–93.

    Google Scholar 

  41. Hassiotou F, Geddes D. Anatomy of the human mammary gland: current status of knowledge. Clin Anat. 2013;26:29–48.

    Article  PubMed  Google Scholar 

  42. Hughes ESR. Development of the mammary gland. Ann R Coll Surg Engl. 1950;6:99–119.

    CAS  PubMed  Google Scholar 

  43. Broman I. Normale und abnorme Entwicklung des Menschen. Wiesbaden: Verlag von JF Bergmann; 1911.

    Google Scholar 

  44. Cooper AP. On the anatomy of the breast. London: Longman, Orme, Green, Brown and Longmans; 1840.

    Google Scholar 

  45. Love SM, Barsky SH. Anatomy of the nipple and breast ducts revisited. Cancer. 2004;101:1947–57.

    Article  PubMed  Google Scholar 

  46. Rusby J, Brachtel E, Michaelson J, Koerner F, Smith B. Breast duct anatomy in the human nipple: three-dimensional patterns and clinical implications. Breast Cancer Res Treat. 2007;106:171–9.

    Article  PubMed  Google Scholar 

  47. Going JJ. Lobar anatomy of human breast and its importance for breast cancer. In: Tot T, editor. Breast cancer. London: Springer London; 2011. p. 19–38.

    Google Scholar 

  48. Eggeling H. Über ein wichtiges Stadium in der Entwicklung der menschlichen Milchdrüse. Anat Anz. 1904;24:595–605.

    Google Scholar 

  49. Renfree MB, Papenfuss AT, Deakin JE, Lindsay J, Heider T, Belov K, et al. Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol. 2011;12:R81. doi:10.1186/gb-2011-12-8-r81.

    Article  PubMed  Google Scholar 

  50. Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S. Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn. 2004;229:349–56.

    Article  CAS  PubMed  Google Scholar 

  51. Rein G. Untersuchungen über die embryonale Entwicklungsgeschichte der Milchdrüse I. Arch Mikrosk Anat. 1882;20:431–501. plates 28–29.

    Article  Google Scholar 

  52. Gosling L. The duration of lactation in feral coypus (Myocastor coypus). J Zool. 1980;191:461–74.

    Article  Google Scholar 

  53. Koyama S, Wu H-J, Easwaran T, Thopady S, Foley F. The nipple: a simple intersection of mammary gland and integument, but focal point of organ function. J Mammary Gland Biol Neoplasia. 2013;18. doi:10.1007/s10911-013-9289-1.

  54. Pearl R. On the correlation between the number of mammá of the dam and size of litter in mammals. I. Interracial correlation. Exp Biol Med. 1913;11:27–30.

    Article  Google Scholar 

  55. Gilbert AN. Mammary number and litter size in Rodentia: the “one-half rule”. Proc Natl Acad Sci U S A. 1986;83:4828–30.

    Article  CAS  PubMed  Google Scholar 

  56. Sherman PW, Braude S, Jarvis JUM. Littter sizes and mammary numbers of naked mole-rats: breaking the one-half rule. J Mammal. 1999;80:720–33.

    Article  Google Scholar 

  57. Derocher AW. Supernumerary mammae and nipples in the polar bear (Ursus maritimus). J Mammal. 1990;71:236–7.

    Article  Google Scholar 

  58. Hsu MJ, Moore J, Lin JF, Agoramoorthy G. High incidence of supernumerary nipples and twins in Formosan macaques (Macaca cyclopis) at Mt. Longevity, Taiwan. Am J Primatol. 2000;52:199–205.

    Article  CAS  PubMed  Google Scholar 

  59. Bell AG. Saving the six-nippled breed. Dr Bell’s last contribution to science. J Hered. 1923;14:99–111.

    Google Scholar 

  60. Castle WE. The genetics of multi-nippled sheep. An analysis of the sheep breeding experiments of Dr. and Mrs. Alexander Graham Bell at Beinn Bhreagh, N.S. J Hered. 1924;15:75–85.

    Google Scholar 

  61. Morrow GE, Nicol SC. Maternal care in the Tasmanian echidna (Tachyglossus aculeatus setosus ). Aust J Zool. 2013. doi:10.1071/ZO12066.

    Google Scholar 

  62. Pires-daSilva A, Sommer RJ. The evolution of signalling pathways in animal development. Nat Rev Genet. 2003;4:39–49.

    Article  CAS  PubMed  Google Scholar 

  63. Widelitz R, Chuong C-M. Early events in skin appendage formation: induction of epithelial placodes and condensation of dermal mesenchyme. J Invest Dermatol Symp Proc. 1999;4:302–6.

    Article  CAS  Google Scholar 

  64. Olivera-Martinez I, Viallet J, Michon F, Pearton DJ, Dhouailly D. The different steps of skin formation in vertebrates. Int J Dev Biol. 2004;48:107–15.

    Article  CAS  PubMed  Google Scholar 

  65. McClellan HL, Miller SJ, Hartmann PE. Evolution of lactation: nutrition v. protection with special reference to five mammalian species. Nutr Res Rev. 2008;21:97–116.

    Article  CAS  PubMed  Google Scholar 

  66. Vorbach C, Capecchi MR, Penninger JM. Evolution of the mammary gland from the innate immune system? Bioessays. 2006;28:606–16.

    Article  CAS  PubMed  Google Scholar 

  67. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA. Phylogenetic perspectives in innate immunity. Science. 1999;284:1313–8.

    Article  CAS  PubMed  Google Scholar 

  68. Fliniaux I, Viallet J, Dhouailly D. Signaling dynamics of feather tract formation from the chick somatopleure. Development. 2004;131:3955–66.

    Article  CAS  PubMed  Google Scholar 

  69. Fliniaux I, Viallet J, Dhouailly D, Jahoda C. Transformation of amnion epithelium into skin and hair follicles. Int Soc Diff. 2004;72:558–65.

    CAS  Google Scholar 

  70. Prin F, Dhouailly D. How and when the regional competence of chick epidermis is established: feathers vs. scutate and reticulate scales, a problem en route to a solution. Int J Dev Biol. 2004;48:137–48.

    Article  CAS  PubMed  Google Scholar 

  71. Collomb E, Yang Y, Foriel S, Cadau S, Pearton DJ, Dhouailly D. The corneal epithelium and lens develop independently from a common pool of precursors. Dev Dyn. 2013. doi:10.1002/dvdy.23925.

    PubMed  Google Scholar 

  72. Jussila M, Thesleff I. Signaling networks regulating tooth organogenesis and regeneration, and the specification of dental mesenchymal and epithelial cell lineages. Cold Spring Harb Perspect Biol. 2012; 4(4). doi:10.1101/cshperspect.a008425.

  73. Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, et al. Gli3-mediated somitic FGF10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development. 2006;133:2325–35.

    Article  CAS  PubMed  Google Scholar 

  74. Huh SH, Närhi K, Lindfors PH, Häärä O, Yang L, Ornitz DM, et al. Fgf20 governs formation of primary and secondary dermal condensations in developing hair follicles. Genes Dev. 2013;27(4):450–8.

    Article  CAS  PubMed  Google Scholar 

  75. Hens JR, Dann P, Zhang J, Harris S, Robinson G, Wysolmerski J. BMP4 and PTHrP interact to stimulate ductal outgrowth during embryonic mammary development and to inhibit hair follicle induction. Development. 2007;134:1221–30.

    Article  CAS  PubMed  Google Scholar 

  76. Propper AY. Relations epidermo-mesodermiques dans la differenciation de l’ebauche mammaire d’embryon de lapin. Ann Embryol Morphogen. 1968;2:151–60.

    Google Scholar 

  77. Kratochwil K. Organ specificity in mesenchymal induction demonstrated in the embryonic development of the mammary gland of the mouse. Dev Biol. 1969;20:46–71.

    Article  CAS  PubMed  Google Scholar 

  78. Dhouailly D. [Dermo-epidermal interactions between birds and mammals: differentiation of cutaneous appendages]. J Embryol Exp Morphol. 1973;30:587–603.

    CAS  PubMed  Google Scholar 

  79. Dhouailly D. Formation of cutaneous appendages in dermo-epidermal recombinations between reptiles, birds and mammals. Wilhelm Roux's Arch Dev Biol. 1975;177:323–40.

    Article  Google Scholar 

  80. Dhouailly D. Dermo-epidermal interactions during morphogenesis of cutaneous appendages in amniotes. Front Matrix Biol. 1977;4:86–121.

    CAS  Google Scholar 

  81. Sick S, Reinker S, Timmer J, Schlake T. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science. 2006;314(5804):1447–50.

    Article  CAS  PubMed  Google Scholar 

  82. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development. 2004;131:4819–29.

    Article  CAS  PubMed  Google Scholar 

  83. Mikkola ML, Thesleff I. Ectodysplasin signaling in development. Cytokine Growth Factor Rev. 2003;14:211–24.

    Article  CAS  PubMed  Google Scholar 

  84. Harris M, Rohner N, Schwartz H, Perathoner H, Konstantinidis P, Nusslein-Volhard C. Zebrafish eda and edar mutants reveal conserved and ancestral roles of Ectodysplasin signaling in vertebrates. PLoS Genet. 2008;4. doi:10.1371/journal.pgen.1000206.

  85. Huh S, Närhi K, Lindfors P, Häärä O, Yang L, Ornitz DM, et al. Fgf20 governs formation of primary and secondary dermal condensations in developing hair follicles. Gene Dev. 2013;27:450–8.

    Article  CAS  PubMed  Google Scholar 

  86. St-Jacques B, Dassule HR, Karavanova I, Botchkarev VA, Li J, Danielian PS, et al. Sonic hedgehog signaling is essential for hair development. Curr Biol. 1998;8:1058–68.

    Article  CAS  PubMed  Google Scholar 

  87. Pispa J, Pummila M, Barker PA, Thesleff I, Mikkola ML. Edar and Troy signalling pathways act redundantly to regulate initiation of hair follicle development. Hum Mol Genet. 2008;17:3380–91.

    Article  CAS  PubMed  Google Scholar 

  88. Lewis MT, Veltmaat JM. Next stop, the twilight zone: hedgehog network regulation of mammary gland development. J Mammary Gland Biol Neoplasia. 2004;9:165–81.

    Article  PubMed  Google Scholar 

  89. Gallego M, Beachy P, Hennighausen L, Robinson G. Differential requirements for Shh in mammary tissue and hair follicle morphogenesis. Dev Biol. 2002;249:131–9.

    Article  CAS  PubMed  Google Scholar 

  90. Michno K, Boras-Granic K, Mill P, Hui CC, Hamel PA. Shh expression is required for embryonic hair follicle but not mammary gland development. Dev Biol. 2003;264:153–65.

    Article  CAS  PubMed  Google Scholar 

  91. Hatsell SJ, Cowin P. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development. 2006;133:3661–70.

    Article  CAS  PubMed  Google Scholar 

  92. Gritli-Linde A, Hallberg K, Harfe BD, Reyahi A, Kannius-Janson M, Nilsson J, et al. Abnormal hair development and apparent follicular transformation to mammary gland in the absence of hedgehog signaling. Dev Cell. 2007;12(1):99–112.

    Article  CAS  PubMed  Google Scholar 

  93. Chiang C, Swan R, Grachtchouk M, Bolinger M, Litingtung Y, Robertson E, et al. Essential role for Sonic hedgehog during hair follicle morphogenesis. Dev Biol. 1999;205:1–9.

    Article  CAS  PubMed  Google Scholar 

  94. Niemann C, Unden A, Lyle S, Zaouboulis C, Toftgård R, Watt F. Indian hedgehog and β-catenin signaling: role in the sebaceous lineage of normal and neoplastic mammalian epidermis. Proc Natl Acad Sci U S A. 2003;30(Supplement 1):11873–80.

    Article  CAS  Google Scholar 

  95. Hardy M. Glandular metaplasia of hair follicles and other responses to vitamin A excess in cultures of rodent skin. J Embryol Exp Morphol. 1968;19:157–80.

    CAS  PubMed  Google Scholar 

  96. Viallet J, Dhouailly D. Retinoic acid and mouse skin morphogenesis. II. Role of epidermal competence in hair glandular metaplasia. Dev Biol. 1994;166:277–88.

    Article  CAS  PubMed  Google Scholar 

  97. Cho K, Kwon H, Shin J, Lee J, Cho S. Retinoic acid signaling and the initiation of mammary gland development. Dev Biol. 2012;365:259–66.

    Article  CAS  PubMed  Google Scholar 

  98. Parsa S, Ramasamy SK, De Langhe S, Gupte VV, Haigh JJ, Medina D, et al. Terminal end bud maintenance in mammary gland is dependent upon FGFR2b signaling. Dev Biol. 2008;317:121–31.

    Article  CAS  PubMed  Google Scholar 

  99. Unbekandt M, del Moral P, Sala FG, Bellusci S, Warburton D, Fleury V. Tracheal occlusion increases the rate of epithelial branching of embryonic mouse lung via the FGF10-FGFR2b-Sprouty2 pathway. Mech Dev. 2008;125:314–24.

    Article  CAS  PubMed  Google Scholar 

  100. Lo T, Yusoff P, Fong C, Guo K, McCaw B, Phillips W, et al. The ras/mitogen-activated protein kinase pathway inhibitor and likely tumor suppressor proteins, Sprouty 1 and Sprouty 2 are deregulated in breast cancer. Cancer Res. 2004;64:6127–36.

    Article  CAS  PubMed  Google Scholar 

  101. Kramer S, Okabe M, Hacohen N, Krasnow M, Hiromi Y. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development. 1999;126:2515–25.

    CAS  PubMed  Google Scholar 

  102. Yue Z, Jiang T, Wu P, Widelitz R, Chuong C-M. Sprouty/FGF signaling regulates the proximal-distal feather morphology and the size of dermal papillae. Dev Biol. 2012;372:45–54.

    Article  CAS  PubMed  Google Scholar 

  103. Foley J, Dann P, Hong J, Cosgrove J, Dreyer B, Rimm D, et al. Parathyroid hormone-related protein maintains mammary epithelial fate and triggers nipple skin differentiation during embryonic breast development. Development. 2001;128:513–25.

    CAS  PubMed  Google Scholar 

  104. Wysolmerski JJ, Cormier S, Philbrick WM, Dann P, Zhang JP, Roume J, et al. Absence of functional type 1 parathyroid hormone (PTH)/PTH-related protein receptors in humans is associated with abnormal breast development and tooth impaction. J Clin Endocrinol Metab. 2001;86(4):1788–94.

    Article  CAS  PubMed  Google Scholar 

  105. Mayer JA, Foley J, De La Cruz D, Chuong C-M, Widelitz R. Conversion of the nipple to hair-bearing epithelia by lowering bone morphogenetic protein pathway activity at the dermal-epidermal interface. Am J Pathol. 2008;173:1339–48.

    Article  CAS  PubMed  Google Scholar 

  106. Wysolmerski JJ. Parathyroid hormone-related protein: an update. J Clin Endocrinol Metab. 2012;97:2947–56.

    Article  CAS  PubMed  Google Scholar 

  107. Debiais-Thibaud M, Oulion S, Bourrat F, Laurenti P, Casane D, Borday-Birraux V. The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula. BMC Evol Biol. 2011;11:307. doi:10.1186/1471-2148-11-307.

    Article  CAS  PubMed  Google Scholar 

  108. Kawasaki K, Lafont A, Sire J. The evolution of milk casein genes from tooth genes before the origin of mammals. Mol Biol Evol. 2011;28:2053–61.

    Article  CAS  PubMed  Google Scholar 

  109. Witzmann F, Scholz H, Mueller J, Kardjilov N. Sculpture and vascularization of dermal bones and implications for the physiology of basal tetrapods. Zool J Linnean Soc. 2010;160:302–40.

    Article  Google Scholar 

  110. Wu P, Hou L, Plikus M, Hughes M, Scehnet J, Suksaweang S, et al. Evo-Devo of amniote integuments and appendages. Int J Dev Biol. 2004;48:249–70.

    Article  CAS  PubMed  Google Scholar 

  111. Alibardi L. Perspectives on hair evolution based on some comparative studies on vertebrate cornification. J Exp Zool Part B. 2012;318:325–43.

    Article  CAS  Google Scholar 

  112. Lefèvre C, Sharp J, Nicholas K. Evolution of lactation: ancient origin and extreme adaptations of the lactation system. Annu Rev Genomics Hum Genet. 2010;11:219–38.

    Article  PubMed  CAS  Google Scholar 

  113. Widelitz RB, Veltmaat JM, Mayer JA, Foley J, Chuong CM. Mammary glands and feathers: comparing two skin appendages which help define novel classes during vertebrate evolution. Semin Cell Dev Biol. 2007;18(2):255–66.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. R. Eisert, F. Caraguel and Mrs. B. Peyrusse for assistance in figure preparation, and staff at the Smithsonian Institution Libraries and the History of Medicine Division of the US National Library of Medicine for locating obscure publications. We particularly acknowledge the Biodiversity Heritage Library for online access (www.biodiversitylibrary.org) to scans of old embryological publications. We are grateful to J. Veltmaat and B. Howard for many helpful comments on earlier versions of this paper.

Author information

Authors and Affiliations

  1. Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA

    Olav T. Oftedal

  2. FRE 3405 CNRS/UJF/EPHE Université Joseph Fourier Site Santé, La Tronche, 38706, France

    Danielle Dhouailly

Authors
  1. Olav T. Oftedal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danielle Dhouailly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olav T. Oftedal.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplemental Table 1

(DOCX 31.1 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oftedal, O.T., Dhouailly, D. Evo-Devo of the Mammary Gland. J Mammary Gland Biol Neoplasia 18, 105–120 (2013). https://doi.org/10.1007/s10911-013-9290-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10911-013-9290-8

Keywords

Search

Navigation