Primiparous and multiparous females differ in mammary gland alveolar development: Implications for milk production

Journal of Experimental Biology

Volumn 215, Issue 16, 2012, Pages 2904-2911

  Lang, Shelley L C ^a   Iverson, Sara J ^a   Bowen, W Don ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b BEDFORD INSTITUTE OF OCEANOGRAPHY   (Canada)

Author keywords

Alveolar density; Alveolar size; Cell density; Grey seal; Halichoerus grypus; Lactation; Mammary gland development; Multiparous; Primiparous; Reproductive experience

Indexed keywords

ANIMAL; ARTICLE; BODY WEIGHT; CANADA; CELL COUNT; CYTOLOGY; FEMALE; GROWTH, DEVELOPMENT AND AGING; LACTATION; METABOLISM; MILK; PARITY; PHOCA; PHYSIOLOGY; PREGNANCY; STAINING; UDDER;

ANIMALS; BODY WEIGHT; CELL COUNT; FEMALE; LACTATION; MAMMARY GLANDS, ANIMAL; MILK; NOVA SCOTIA; PARITY; PREGNANCY; SEALS, EARLESS; STAINING AND LABELING;

HALICHOERUS GRYPUS;

EID: 84864342663     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.067058     Document Type: Article

References (52)

1. Akers, R. M. (2002). Lactation and the Mammary Gland. Ames, IA: Iowa State Press.
2. Allen, P. J., Amos, W., Pomeroy, P. P. and Twiss, S. D. (1995). Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol. Ecol. 4, 653-662. (Pubitemid 3012619)
3. Anderson, R. R. and Sheffield, L. G. (1983). Growth of guinea pig mammary glands through their first six lactations. J. Dairy Sci. 66, 29-34.
4. AOAC (2000a). AOAC official method 991.20 for nitrogen (total) in milk, Kjeldahl methods. In Official Methods of Analysis (ed. W. Horwitz), pp. 10. Gaithersburg, MD: AOAC International.
5. AOAC (2000b). AOAC official method 905.02 for fat in milk, Roese-Gottlieb method. In Official Methods of Analysis (ed. W. Horwitz), pp. 18. Gaithersburg, MD: AOAC International.
6. Belov, L. N. (1971). Histological organisation of the mammary gland in the seals Pagophilus groenlandicus and Crystophora cristata. J. Evol. Biochem. Physiol. 7, 585-589.
7. Blaxter, K. (1989). Energy Metabolism in Animals and Man. Cambridge, UK: Cambridge University Press.
8. Bowen, W. D., Stobo, W. T. and Smith, S. J. (1992). Mass changes of grey seal (Halichoerus grypus) pups on Sable Island: differential maternal investment reconsidered. J. Zool. 227, 607-622. (Pubitemid 23397953)
9. Bowen, W. D., Iverson, S. J., McMillan, J. I. and Boness, D. J. (2006). Reproductive performance in grey seals: age-related improvement and senescence in a capital breeder. J. Anim. Ecol. 75, 1340-1351. (Pubitemid 44556455)
10. Bowen, W. D., McMillan, J. I. and Blanchard, W. (2007). Reduced population growth of gray seals at Sable Island: evidence from pup production and age of primiparity. Mar. Mamm. Sci. 23, 48-64. (Pubitemid 46066554)
11. Cowie, A. T., Forsyth, I. A. and Hart, I. C. (1980). Hormonal Control of Lactation. New York, NY: Springer-Verlag.
12. Farr, V. C., Stelwagen, K., Cate, L. R., Molenaar, A. J., McFadden, T. B. and Davis, S. R. (1996). An improved method for the routine biopsy of bovine mammary tissue. J. Dairy Sci. 79, 543-549. (Pubitemid 126429082)
13. Festa-Bianchet, M., Jorgenson, J. T. and Reale, D. (2000). Early development, adult mass and reproductive success in bighorn sheep. Behav. Ecol. 11, 633-639. (Pubitemid 34134647)
14. Fowler, P. A., Knight, C. H., Cameron, G. G. and Foster, M. A. (1990). In-vivo studies of mammary development in the goat using magnetic resonance imaging (MRI). J. Reprod. Fertil. 89, 367-375. (Pubitemid 20156239)
15. Gittleman, J. L. and Thompson, S. D. (1988). Energy allocation in mammalian reproduction. Am. Zool. 28, 863-875.
16. Hall, A. J., McConnell, B. J. and Barker, R. J. (2001). Factors affecting first-year survival in grey seals and their implications for life history strategy. J. Anim. Ecol. 70, 138-149. (Pubitemid 32232370)
17. Heald, C. W. (1974). Hormonal effects on mammary cytology. J. Dairy Sci. 57, 917-925.
18. Hennighausen, L. and Robinson, G. W. (1998). Think globally, act locally: the making of a mouse mammary gland. Genes Dev. 12, 449-455. (Pubitemid 28101007)
19. Hillerton, J. E., Knight, C. H., Turvey, A., Wheatley, S. D. and Wilde, C. J. (1990). Milk yield and mammary function in dairy cows milked four times daily. J. Dairy Res. 57, 285-294.
20. Iverson, S. J., Bowen, W. D., Boness, D. J. and Oftedal, O. T. (1993). The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol. Zool. 66, 61-88. (Pubitemid 24408005)
21. Knight, C. H. (2000). The importance of cell division in udder development and lactation. Livest. Prod. Sci. 66, 169-176.
22. Knight, C. H. and Peaker, M. (1982). Development of the mammary gland. J. Reprod. Fertil. 65, 521-536. (Pubitemid 12013247)
23. Knight, C. H. and Peaker, M. (1984). Mammary development and regression during lactation in goats in relation to milk secretion. Q. J. Exp. Physiol. 69, 331-338. (Pubitemid 14138561)
24. Lang, S. L. C., Iverson, S. J. and Bowen, W. D. (2009). Repeatability in lactation performance and the consequences for maternal reproductive success in gray seals. Ecology 90, 2513-2523.
25. Lang, S. L. C., Iverson, S. J. and Bowen, W. D. (2011a). The influence of reproductive experience on milk energy output and lactation performance in the grey seal (Halichoerus grypus). PLoS ONE 6, e19487
26. Lang, S. L. C., Boness, D. J., Bowen, W. D. and Iverson, S. J. (2011b). Primiparous females do not exhibit reduced maternal care in gray seals (Halichoerus grypus). Mar. Mamm. Sci. 27, E153-E164.
27. Masso-Welch, P. A., Darcy, K. M., Stangle-Castor, N. C. and Ip, M. M. (2000). A developmental atlas of rat mammary gland histology. J. Mammary Gland Biol. Neoplasia 5, 165-185. (Pubitemid 32045694)
28. Mazerolle, M. J. (2011). AICcmodavg: Model Selection and Multimodel Inference Based on (Q)AIC(c). R package version 1.17. http://CRAN.R-project.org.
29. Mellish, J. E. (1999). Physiology of Milk Fat Secretion and Neonatal Fat Deposition During Lactation in Phocid Seals. PhD dissertation, Dalhousie University, Halifax, Canada.
30. Mellish, J. E., Iverson, S. J. and Bowen, W. D. (1999a). Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol. Biochem. Zool. 72, 677-690. (Pubitemid 30156938)
31. Mellish, J. E., Iverson, S. J., Bowen, W. D. and Hammill, M. O. (1999b). Fat transfer and energetics during lactation in the hooded seal: the roles of tissue lipoproteinlipase in milk fat secretion and pup blubber deposition. J. Comp. Physiol. B 169, 377-390. (Pubitemid 29478284)
32. Miller, N., Delbecchi, L., Petitclerc, D., Wagner, G. F., Talbot, B. G. and Lacasse, P. (2006). Effect of stage of lactation and parity on mammary gland cell renewal. J. Dairy Sci. 89, 4669-4677. (Pubitemid 46118368)
33. Neville, M. C., McFadden, T. B. and Forsyth, I. (2002). Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 7, 49-66. (Pubitemid 38420781)
34. Nielsen, O. L., Pedersen, A. R. and Sorensen, M. T. (2001). Relationships between piglet growth rate and mammary gland size of the sow. Livest. Prod. Sci. 67, 273-279. (Pubitemid 32143146)
35. Noren, S. R., Boness, D. J., Iverson, S. J., McMillan, J. and Bowen, W. D. (2008). Body condition at weaning affects the duration of the postweaning fast in gray seal pups (Halichoerus grypus). Physiol. Biochem. Zool. 81, 269-277. (Pubitemid 351601419)
36. Oftedal, O. T. and Iverson, S. J. (1995). Phylogenetic variation in the gross composition of mammalian milks. In The Handbook of Milk Composition (ed. R. G.Jensen and M. Thompson), pp. 790-827. San Diego, CA: Academic Press.
37. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and R Development Core Team (2011). Nlme: Linear and Nonlinear Mixed Effects Models. R Package Ver. 3. pp. 1-100.
38. Pitelka, D. R. (1998). The mammary gland. In Cell and Tissue Biology (ed. L. Weiss), pp. 880-898. Baltimore: Urban and Schwarzenberg.
39. Pomeroy, P. P., Twiss, S. D. and Redman, P. (2000). Philopatry, site fidelity and local kin associations within grey seal breeding colonies. Ethology 106, 899-919.
40. Reginato, M. J. and Muthuswamy, S. K. (2006). Illuminating the center: mechanisms regulating lumen formation and maintenance in mammary morphogenesis. J. Mammary Gland Biol. Neoplasia 11, 205-211. (Pubitemid 44869916)
41. Richert, M. M., Schwertfeger, K. L., Ryder, J. W. and Anderson, S. M. (2000). An atlas of mouse mammary gland development. J. Mammary Gland Biol. Neoplasia 5, 227-241. (Pubitemid 32045698)
42. Shipman, L. J., Docherty, A. H., Knight, C. H. and Wilde, C. J. (1987). Metabolic adaptations in mouse mammary gland during a normal lactation cycle and in extended lactation. Q. J. Exp. Physiol. 72, 303-311.
43. Tedman, R. A. (1983). Ultrastructural distribution of morphology of the mammary gland with observations on the size fat droplets in milk of the Weddell seal Leptonychotes weddelli (Pinnipedia). J. Zool. 200, 131-141.
44. Tedman, R. A. (1985). The weddell seal, Leptonychotes weddelli, at McMurdo Sound,Antarctica: milk production in relation to pup growth. In Studies of Sea Mammals in South Latitudes (ed. J. K. Ling and M. M. Bryden), pp. 41-52. Adelaide, Australia: South Australian Museum.
45. Tedman, R. A. and Bryden, M. M. (1981). The mammary gland of the Weddell seal, Leptonychotes weddelli (Pinnipedia). I. Gross and microscopic anatomy. Anat. Rec. 199, 519-529. (Pubitemid 11098468)
46. Tucker, H. A. (1981). Physiological control of mammary growth, lactogenesis, and lactation. J. Dairy Sci. 64, 1403-1421.
47. Vonderhaar, B. K., Smith, G. H., Pauley, R. J., Rosen, J. M. and Topper, Y. J. (1978). Difference between mammary epithelial cells from mature virgin and primiparous mice. Cancer Res. 38, 4059-4065. (Pubitemid 9060141)
48. Wada, H. and Turner, C. W. (1959). Effect of recurring pregnancy on mammary gland growth in mice. J. Dairy Sci. 42, 1198-1202.
49. Wagner, K.-U. and Smith, G. H. (2005). Pregnancy and stem cell behavior. J. Mammary Gland Biol. Neoplasia 10, 25-36. (Pubitemid 40724020)
50. Wagner, K. U., Boulanger, C. A., Henry, M. D., Sgagias, M., Hennighausen, L. and Smith, G. H. (2002). An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 129, 1377-1386. (Pubitemid 34874159)
51. Wauters, L., Bijnens, L. and Dhondt, A. A. (1993). Body mass at weaning and juvenile recruitment in the red squirrel. J. Anim. Ecol. 62, 280-286.
52. Yang, H., Eastham, P. R., Phillips, P. and Whittemore, C. T. (1989). Reproductive performance, body weight and body condition of breeding sows with differing body fatness at parturition, differing nutrition during lactation, and differing litter size. Anim. Prod. 48, 181-201.