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The status of the corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay

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Summary

Developmental delay is correlated with torpor in the temperate zone bent-winged bat, Miniopterus schreibersii (latitude 37° S) as a period of pre-implantation delay (delayed implantation) followed by a short post-implantation delay (delayed development). During this time, the number of steroidogenic organelles in luteal cytoplasm is greatly reduced compared with normal embryogenesis, and granular endoplasmic reticulum is prominent. Nidation, which occurs while the animals are hibernating, is not accompanied by marked changes in luteal ultrastructure, although the number of lipid droplets decreases somewhat. Progesterone rises slightly but not significantly; however, a pre-nidation decrease in high 17β-estradiol levels may play a role in implantation. Following implantation, the conceptus remains delayed at the blastocyst stage for several weeks. During this time the bats remain torpid and the only change in luteal cell ultrastructure is an increase in smooth endoplasmic reticulum as differentiation begins toward the trilaminar stage. At the end of developmental delay hypertrophy of the luteal cell begins and mitochondria and lipid droplets increase, markedly. By this time arousal from hibernation has occurred, placentation takes place, and normal development is underway. At placentation, smooth endoplasmic reticulum reaches its maximum in luteal cytoplasm; estrogen and progesterone levels peak about 6 weeks later. For the remaining 2 months of gestation, signs of luteolysis appear. These observations suggest that the corpus luteum of developmental delay, though suboptimally functional, is prolonged in its luteinization by the arrival of winter when the bats enter torpor. The capacity for maximal steroidogenesis is acquired at the end of winter, some weeks after implantation, when arousal occurs and normal development ensues.

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References

  • Aitken RJ (1981) Aspects of delayed implantation in the roe deer (Capreolus capreolus). J Reprod Fertil [Suppl] 29:83–95

    Google Scholar 

  • Anderson MB, Sherwood OD (1984) Ultrastructural localization of relaxin immunoreactivity in corpora lutea of pregnant rats. Endocrinology 114:1124–1127

    Google Scholar 

  • Bagwell JN (1977) Fine structure of the corpus luteum of pregnancy in the gerbil (Meriones unguiculatus). Cell Tissue Res 176:361–371

    Google Scholar 

  • Barry RE, Crapo JD (1985) Application of morphometric methods to study diffuse and focal injury in the lung caused by toxic agents. CRC Crit Rev Toxicol 14:1–32

    Google Scholar 

  • Belt WD, Cavazos LF, Anderson LL, Kraeling RR (1970) Fine structure and progesterone levels in the corpus luteum of the pig during pregnancy and after hysterectomy. Biol Reprod 2:98–113

    Google Scholar 

  • Berria M, Joseph MM, Mead RA (1988) Role of prolactin and luteinizing hormone in regulating timing of implantation in the spotted skunk. Biol Reprod 38 [Suppl] 1:184

    Google Scholar 

  • Bjersing L (1967) On the ultrastructure of granulosa lutein cells in the porcine corpus luteum. With special reference to endoplasmic reticulum and steroid hormone synthesis. Z Zellforsch 82:187–211

    Google Scholar 

  • Blanchette EJ (1966) Ovarian steroid cells. II. The lutein cell. J Cell Biol 31:517–542

    Google Scholar 

  • Bradshaw GVR (1961a) Le cycle de reproduction de Macrotus californicus (Chiroptera, Phyllostomatidae). Mammalia 25:117–119

    Google Scholar 

  • Bradshaw GVR (1961b) A life history study of the California leaf-nosed bat Macrotus californicus. PhD dissertation, University of Arizona

  • Branca A (1927) Recherches sur la placentation des cheiroptères. Arch Zool Exp Gén 66:291–450

    Google Scholar 

  • Burns JM, Easley RG (1977) Hormonal control of delayed development in the California leaf-nosed bat, Macrotus californicus. III. Changes in plasma progesterone during pregnancy. Gen Comp Endocrinol 32:163–166

    Google Scholar 

  • Burns JM, Wallace WE (1975) Hormonal control of delayed development in Macrotus waterhousii. II. Radioimmunoassay of plasma estrone and estradiol 17-β during pregnancy. Gen Comp Endocrinol 25:529–533

    Google Scholar 

  • Canivenc R (1965) A study of progestation in the European badger (Meles meles L.). In: Rowlands IW (ed) Comparative biology of reproduction in mammals. Academic Press, New York, pp 15–26

    Google Scholar 

  • Canivenc R, Bonnin-Leffargue M (1963) Inventory of problems raised by the delayed ovo implantation in the European badger (Meles meles). In: Enders AC (ed) Delayed implantation. University of Chicago Press, Chicago, pp 111–128

    Google Scholar 

  • Christensen AK, Gillim SW (1969) The correlation of fine structure and function in steroid-secreting cells, with emphasis on those of the gonads. In: McKerns KW (ed) The gonads. Appleton, Century, Crofts, New York, pp 415–488

    Google Scholar 

  • Courrier R (1927) Etude sur la déterminisme des caractères sexuel secondaries chez quelques mammifères à activité testiculaire périodique. Arch Biol (Paris) 37:173–334

    Google Scholar 

  • Crelin ES (1969) Interpubic ligament elasticity in pregnant freetailed bat. Science 164:81–82

    Google Scholar 

  • Crichton EG, Krutzsch PH (1985a) Comparative morphology of the corpus luteum of embryonic diapause in Chiroptera. J Anat 143:224

    Google Scholar 

  • Crichton EG, Krutzsch PH (1985b) Reproductive biology of the female leaf-nosed bat, Macrotus californicus, in southwestern United States. I. A morphometric analysis of the annual ovarian cycle. Am J Anat 173:69–87

    Google Scholar 

  • Crichton EG, Krutzsch PH (1987) Reproductive biology of the female little mastiff bat, Mormopterus planiceps (Chiroptera: Molossidae) in southeast Australia. Am J Anat 178:369–386

    Google Scholar 

  • Crisp TM, Dessouky DA, Denys FR (1970) The fine structure of the human corpus luteum of early pregnancy and during the progestational phase of the menstrual cycle. Am J Anat 127:37–70

    Google Scholar 

  • Crombie PR, Burton RD, Ackland N (1971) The ultrastructure of the corpus luteum of the guinea-pig. Z Zellforsch 115:473–493

    Google Scholar 

  • Daniel JC (1974) Circulating levels of oestradiol-17β during early pregnancy in the Alaskan fur seal showing an oestrogen surge preceding implantation. J Reprod Fertil 37:425–428

    Google Scholar 

  • Enders AC (1962) Observations on the fine structure of lutein cells. J Cell Biol 12:101–113

    Google Scholar 

  • Enders AC (1973) Cytology of the corpus luteum. Biol Reprod 8:158–182

    Google Scholar 

  • Farin CE, Moeller CL, Sawyer HR, Gamboni F, Niswender GD (1986) Morphometric analysis of cell types in the ovine corpus luteum throughout the estrous cycle. Biol Reprod 35:1299–1308

    Google Scholar 

  • Fonda E, Peyre A (1965) Localization de la 5–3 hydroxystéroidodéshydrogénase dans le placenta de Minioptère au cours de la gestation. C R Acad Sci Paris 261:2963–2969

    Google Scholar 

  • Foresman KR, Mead RA (1978) Luteal control of nidation in the ferret (Mustela putorius). Biol Reprod 18:490–496

    Google Scholar 

  • Hamre C, Meyer RK, Martin SJ (1928) Sex dimorphism of the symphysis pubis of the bat. Anat Rec 41:60–61

    Google Scholar 

  • Joseph MM, Mead RA (1987) Changes in the size distribution of luteal cells in pregnant ferrets. Biol Reprod 36:138

    Google Scholar 

  • Kayanja IB, Neaves WB (1973) The fine structure of the corpus luteum in Hyrax. Z Zellforsch 144:475–487

    Google Scholar 

  • Kimura K, Uchida TA (1983) Ultrastructural observations of delayed implantation in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. J Reprod Fertil 69:187–193

    Google Scholar 

  • Kimura K, Takeda A, Uchida TA (1987) Changes in progesterone concentrations in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. J Reprod Fertil 80:59–63

    Google Scholar 

  • Krutzsch PH, Crichton EG, Nagle RB (1982) Studies on prolonged spermatozoa survival in Chiroptera. A morphological examination of storage and clearance of intrauterine and cauda epididymal spermatozoa in the bats Myotis lucifugus and M. velifer. Am J Anat 165:421–434

    Google Scholar 

  • Leavitt WW, Basom CR, Blaha GC (1973) Structure and function of the hamster corpus luteum during the estrous cycle. Am J Anat 136:235–250

    Google Scholar 

  • Mead RA, Eik-Nes KB (1969) Oestrogen levels in peripheral blood of the spotted skunk. J Reprod Fertil 18:351–353

    Google Scholar 

  • Mead RA, Concannon PW, McRae M (1981) Effect of progestins on implantation in the western spotted skunk. Biol Reprod 25:128–133

    Google Scholar 

  • Mead RA, Joseph MM, Neirinckx S, Berria M (1988) Partial characterization of a luteal factor that induces implantation in the ferret. Biol Reprod 38:798–803

    Google Scholar 

  • Meyer GT, Bruce NW (1984) Quantitative ultrastructure of the luteal cell of the 16-day-pregnant rat and its relation to progesterone secretion. J Reprod Fertil 70:261–269

    Google Scholar 

  • Mikami S, Chiba S, Taniguchi K, Kubokawa K, Ishii S (1988) Immunocytochemical studies on the pituitary pars distalis of the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. Cell Tissue Res 251:291–299

    Google Scholar 

  • Møller OM (1973a) The fine structure of the lutein cells in the mink (Mustela vison) with special reference to the secretory activity during pregnancy. Z Zellforsch 138:523–544

    Google Scholar 

  • Møller OM (1973b) The progesterone concentration in peripheral plasma of the mink (Mustela vison) during pregnancy. J Endocrinol 56:121–132

    Google Scholar 

  • Mori H, Christensen AK (1980) Morphometric analysis of Leydig cells in the normal rat testis. J Cell Biol 84:340–354

    Google Scholar 

  • Murphy BD, Mead RA (1976) Effects of antibodies to oestrogens on implantation in ferrets. J Reprod Fertil 46:261–263

    Google Scholar 

  • O'Shea JD, Cran DG, Hay MF (1979) The small luteal cell of the sheep. J Anat 128:239–251

    Google Scholar 

  • Paavola LG (1977) The corpus luteum of the guinea pig. Fine structure at the time of maximum progesterone secretion and during regression. Am J Anat 150:565–604

    Google Scholar 

  • Parry DM, Willcox DL, Thorburn GD (1980) Ultrastructural and cytochemical study of the bovine corpus luteum. J Reprod Fertil 60:349–357

    Google Scholar 

  • Peyre A, Herlant M (1963a) Ovo-implantation différée et corrélations hypophysogénitales chez la femelle du Minioptère (Miniopterus schreibersii). C R Acad Sci Paris 257:524–526

    Google Scholar 

  • Peyre A, Herlant M (1963b) Corrélations hypophysogénitales chez la femelle du Minioptère (Miniopterus schreibersii B). Gen Comp Endocrinol 3:726

    Google Scholar 

  • Peyre A, Herlant M (1967) Ovo-implantation differée et déterminisme hormonal chez le Minioptère, Miniopterus schreibersii K (Chiroptère). C R Soc Biol (Paris) 162:1779–1182

    Google Scholar 

  • Peyre A, Malassine A (1969) L'équipement stéroidodeshydrogénasique et la fonction endocrine du placenta de Minioptère (Chiroptère). C R Soc Biol (Paris) 163:914–917

    Google Scholar 

  • Racey PA (1969) Diagnosis of pregnancy and experimental extension of gestation in the pipistrelle bat, Pipistrellus pipistrellus. J Reprod Fertil 19:465–474

    Google Scholar 

  • Racey PA (1973) Environmental factors affecting the length of gestation in heterothermic bats. J Reprod Fertil [Suppl] 19:175–189

    Google Scholar 

  • Racey PA, Swift SM (1981) Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. J Reprod Fertil 61:123–129

    Google Scholar 

  • Ravindra R, Mead RA (1984) Plasma estrogen levels during pregnancy in the western spotted skunk. Biol Reprod 30:1153–1159

    Google Scholar 

  • Renfree MB, Tyndale-Biscoe CH (1973) Intrauterine development after diapause in the marsupial Macropus eugenii. Dev Biol 32:28–40

    Google Scholar 

  • Rice GE, Jenkin G, Thorburn GD (1986) Comparison of particle-associated progesterone and oxytocin of the ovine corpus luteum. J Endocrinol 108:109–116

    Google Scholar 

  • Richardson BA (1979) The anterior pituitary and reproduction in bats. J Reprod Fertil 56:379–389

    Google Scholar 

  • Richardson BA (1981) Identification of prolactin and growth hormone cells in the pars distalis of the California leaf-nosed bat, Macrotus californicus. Am J Anat 161:427–440

    Google Scholar 

  • Richardson EG (1977) The biology and evolution of the reproductive cycle of Miniopterus schreibersii and M. australis (Chiroptera: Vespertilionidae). J Zool (Lond) 183:353–375

    Google Scholar 

  • Savard K (1973) The biochemistry of the corpus luteum. Biol Reprod 8:183–202

    Google Scholar 

  • Sempéré A (1977) Plasma progesterone levels in the roe deer Capreolus capreolus. J Reprod Fertil 50:365–366

    Google Scholar 

  • Shelden RM (1973) Failure of ovarian steroids to influence blastocysts of weasels (Mustela erminea) ovariectomized during delayed implantation. Endocrinology 92:638–641

    Google Scholar 

  • Siekevitz P (1963) Protoplasma; endoplasmic reticulum and microsomes and their properties. Annu Rev Physiol 25:15–40

    Google Scholar 

  • Sinha AA, Erickson AW (1972) Ultrastructure of the corpus luteum of Antarctic seals during pregnancy. Z Zellforsch 133:13–20

    Google Scholar 

  • Sinha AA, Mead RA (1975) Ultrastructural changes in granulosa lutein cells and progesterone levels during preimplantation, implantation, and early placentation in the western spotted skunk. Cell Tissue Res 164:179–192

    Google Scholar 

  • Sinha AA, Mead RA (1976) Morphological changes in the trophoblast, uterus and corpus luteum during delayed implantation in the western spotted skunk. Am J Anat 145:331–356

    Google Scholar 

  • Sinha AA, Seal US, Doe RP (1971) Ultrastructure of the corpus luteum of the white-tailed deer during pregnancy. Am J Anat 132:189–206

    Google Scholar 

  • Stone BA, Seamark RF (1985) Steroid hormones in uterine washings and in plasma of gilts between days 9 and 15 after oestrus and between days 9 and 15 after coitus. J Reprod Fertil 75:209–221

    Google Scholar 

  • Tyndale-Biscoe CH (1963) The role of the corpus luteum in the delayed implantation of marsupials. In: Enders AC (ed) Delayed implantation. University of Chicago Press, Chicago, pp 15–32

    Google Scholar 

  • Uchida TA, Inoue C, Kimura K (1984) Effects of elevated temperatures on the embryonic development and corpus luteum activity in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. J Reprod Fertil 71:439–444

    Google Scholar 

  • Van der Merwe M (1982) Histological study of implantation in the Natal clinging bat (Miniopterus schreibersii natalensis). J Reprod Fertil 65:319–323

    Google Scholar 

  • Wade-Smith J, Richmond ME, Mead RA, Taylor M (1980) Hormonal and gestational evidence for delayed implantation in the striped skunk, Mephitis mephitis. Gen Comp Endocrinol 42:509–515

    Google Scholar 

  • Wallace GI (1978) A histological study of the early stages of pregnancy in the bent-winged bat (Miniopterus schreibersii) in north-eastern New South Wales, Australia (30° 27′S). J Zool (Lond) 185:519–537

    Google Scholar 

  • Walker MT, Gemmell RT, Hughes RL (1983) Ultrastructure of the reactivated corpus luteum after embryonic diapause in the marsupial, Macropus rufogriseus banksianus. Cell Tissue Res 228:61–74

    Google Scholar 

  • Weibel ER (1979) Stereological methods. Vol 1. Practical methods for biological morphometry. Academic Press, London

    Google Scholar 

  • Weibel ER (1980) Stereological methods. Vol. 2. Theoretical foundations. Academic Press, New York

    Google Scholar 

  • Wimsatt WA (1963) Delayed implantation in the Ursidae with particular reference to the black bear (Ursus americanus Pallas). In: Enders AC (ed) Delayed implantation. University of Chicago Press, Chicago, pp 49–76

    Google Scholar 

  • Wright PL (1963) Variations in reproductive cycles in North American mustelids. In: Enders AC (ed) Delayed implantation. University of Chicago Press, Chicago, pp 77–97

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, University of Arizona, Tucson, Arizona, USA

    Elizabeth G. Crichton & Philip H. Krutzsch

  2. Department of Obstetrics and Gynecology, University of Adelaide, Adelaide, South Australia, Australia

    Robert F. Seamark

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  1. Elizabeth G. Crichton
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Crichton, E.G., Seamark, R.F. & Krutzsch, P.H. The status of the corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay. Cell Tissue Res. 258, 183–201 (1989). https://doi.org/10.1007/BF00223157

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