The Pelvis of the Free-tailed Bat: Sexual Dimorphism and Pregnancy Changes E. S. CRELIN A N D E. V. NEWTON Department of Anatomy, Y a k University School of Medicine, New Haven, Connecticut ABSTRACT There are constant morphological differences between the bony pelves of adult males and females that constitute a sexual dimorphism. A convexity along the caudal border of the ischiopubic ramus and a bony projection bordering the pubic joint are present only in the male. The pubic joint in the male is a typical symphysis, whereas in the female it consists of an interpubic ligament interconnecting the coxal bones. The ligament contains an abundance of elastic fibers interspersed among collagenous fibers. The disparity between the size of the pelvic birth canal of the pregnant bat and the single full-term fetus is so great that during parturition the interpubic ligament stretches to more than 15 times its original length. The present experiment was designed to determine the features that constituted a bony pelvic sexual dimorphism and the pelvic changes occurring during pregnancy in the free-tailed bat. Weigert's resorcin-fuchsin elastic stain that stained elastic fibers blue-black to black, collagenous fibers pink to red, cell nuclei blue to black, and muscle yellow. MATERIALS AND METHODS There is no significant difference between the male and female in the size of the bony pelvis. The features constituting a bony pelvic sexual dimorphism are few. The caudal border of the ischiopubic ramus in the male has a distinct bony convexity that is lacking in the female (figs. 3, 5). The pubic joint of the male is a typical pubic symphysis (figs. 2, 11) . The ends of the coxal bones at the joint are less than 1 mm apart and capped with hypertrophic hyaline cartilage that is continuous with a compact lamina of fibro-elastic cartilage in the center of the joint. The dense articular capsule of the male pubic symphysis contains both collagenous and elastic fibers (fig. 11). A projection of coxal bone at the symphysis in the male is absent in the female (figs. 3, 5). Instead of a pubic symphysis in the adult female the ends of the coxal bones at the pubic joint are interconnected by an interpubic ligament (figs. 4, 6, 7, 9). The ligament is attached directly to an irregular surface of the coxal bones at the joint (figs. 5, 9). Its outer part is a mcdification of the articular capsule sur- A total of 43 free-tailed bats (Tadarida brasiliensis cynocephala, LeConte) were captured in their wild state. Five were adult males, six were nonpregnant adult females, and 32 were pregnant females in all stages of an 11 to 12 week pregnancy. Five of the latter were sacrificed shortly after parturition, whereas the others were sacrificed at different stages of the pregnancy period. At autopsy the pelves of all of the bats were exposed. If an interpubic ligament were present it was cleaned and measured in situ. The bony pelves were then excised and stripped of attached soft tissue. Quantitative and qualitative studies were made on each pelvis to determine the features that constituted a bony pelvic sexual dimorphism similar to those made on mouse and rat pelves (Crelin, '60; Bernstein and Crelin, '67). The pelves of two males, three nonpregnant females, five pregnant females, and two post partum females were prepared as dried whole mounts. The pubic joint portion of the coxal bones with its interconnecting cartilage or ligament was excised from the remaining bats and fixed, decalcified and embedded in paraffi?. The tissues were sectioned serially at 7 LI and stained with ANAT. REC., 164: 349-358. RESULTS Received Jan. 27, '69. Accepted Mar. 10,'69. 1 This investigation was supported in whole by Public Health Service Research p n t AM 09499-14 from the National Institute of Arthritis and Metabolic Diseases. 349 350 E. S. CRELIN AND E. V. NEWTON rounding the fibro-elastic cartilage of the male symphysis. In the female it is a long sheath of fibrous connective tissue containing an abundance of elastic fibers (figs. 10, 12, 13). The elastic fibers of the capsular portion blend with those of the stroma of the abdominal wall and pelvic musculature that attaches to the ligament. Deep to the capsular portion there is an intermingling of bundles of elastic and collagenous fibers (fig. 14). As the core of the ligament is approached the elastic fibers become fewer in number. The core consists almost entirely of collagenous fibers. Osteoclasts are present along the irregular surface of the coxal bones where the ligament attaches. The interpubic ligament was approximately the same length in the early pregnant bats as it was in the late pregnant ones. Its average length was 1.75 mm (range 1.10-2.35 mm) in all of the females, including the post partum females. The bony pelvic birth canal consists of the two coxal bones that articulate with the sacrum posteriorly and with each other anteriorly through the interpubic ligament (fig. 1 ). The widest diameter of the bony birth canal was in the transverse interacetabular plane in all of the females and averaged 3.35 mm (range 3.00-4.00 mm). Since the widest diameter of the five newborn bats was in their caudal truyk region and averaged 16.00 mm (range 15.5016.20 mm), it was calculated that the interpubic ligament had to increase in length Fig. 1 A diagram of the actual size of the bony birth canal of a nonpregnant free-tailed bat is shown in A. The increase in lenzth of the interpubic ligament necessary for the birth canal to accommodate a full-term fetus is shown in B. S, sacrum; C, coxal bone; L, interpubic ligament. during parturition by 15 times or more (figs. 1, 7, 8). DISCUSSION In the literature search nothing was found describing the presence of a bony pelvic sexual dimorphism in the free-tailed bat. Vaughn ('59) reported on the anatomy of three other species of bats (Eumops, Myotis, and Macrotus) in some detail, including illustrations, without describing a bony pelvic sexual dimorphism. Even so, such a dimorphism is probably universal in bats. The anatomy of the rat has been reported in great detail for many years and yet it wasn't until relatively recently that a bony pelvic dimorphism was described (Crelin and Brightman, '57). The dimorphic features of the bony pelvis of the bat presumably occur during development under hormonal influence. In the mouse and rat the chief causative factor of development is gonadal testostercne (Crelin, '60; Crelin and Blood, '61; Bernstein and Crelin, '67). The type of pelvis that develops in the absence of the gonads in the mouse and rat is the female type, therefore, gonadal estrogen has no influence on the shaping of the pelvis during development. However, at puberty the ends of the coxal bones at the pubic joint undergo some resorption in the mouse due to the influflence of estrogen (Crelin, '54c; Gardner, '36). Estrogen at puberty presumably induces the resorption of the coxal bones where the interpubic ligament attaches in the female free-tailed bat. Hamre et al. ('28) studied the pelvis of the bat, Myotis lucifugus, and found that a typical pubic symphysis was present in males and immature females, whereas an interpubic ligament was present in sexually mature females. They reported that during pregnancy the ligament increased greatly in thickness and width. They concluded that the transformation of the pubic symphyseal tissue into an interpubic ligament was associated with the attainment of sexual maturity in the female, somewhat similar to the occurrence in the guinea pig (Talmage, '47). This is quite different in the mouse where the transformstion of symphyseal tissue into a ligament does not occur until duriqg the first pregnancy (Crelin, '54b; Crelin and Koch, 351 BAT PELVIS Crelin, E. S. 1954a Prevention of innominate bone separation during pregnancy in the mouse. Proc. SOC. Exp. Biol. and Med., 86: 22-24. 1954b The effects of androgen, estrogen and relaxin on intact and transplanted pelves i n mice. Am. J. Anat., 95: 47-73. 1954c The effects of estrogen and relaxin on the pubic symphysis and transplanted ribs in mice. Anat. Rec., 120: 23-32. 1960 The development of bony pelvic sexual dimorphism in mice. Ann. N. Y. Acad. Sci., 84: 879-512. 1963 The development and hormonal response of the autotransplanted interpubic joint i n mice. Anat. Rec., 146: 149-163. Crelin, E. S. and D. K. Blood 1961 The influence of the testes on the shaping of the bony pelvis in mice. Anat. Rec., 140: 375-379. Crelin, E. S . and M. W. Brightman 1957 The pelvis of the rat: its response to estrogen and relaxin. Anat. Rec., 128: 467483. Crelin, E. S . and W. E. Koch 1965 Development of mouse pubic joint in uivo following initial differentiation in uitro. Anat. Rec., 153: 161-171. Gardner, W. U. 1936 Sexual dimorphism of the pelvis of the mouse, the effect of estrogenic hormones upon the pelvis and upon the develI . Anat., 59: opment of scrota1 hernias. Am. . 459483. Gersh, I. and H. R. Catchpole 1960 The nature of ground substance of connective tissue. Perspectives in Biol. and Med., 111: 282-319. Hall, K. 1947 The effects of pregnancy and relaxin on the histology of the pubic symphysis in the mouse. J. Endocrin., 5: 174-182. 1960 Relaxin. J. Reprod. Fertil., I : 368-384. Hamre. C.. R. K. Meyer and S. J. Martin 1928 Sexu'al dimorphism- of the symphysis pubis of the bat Myotis Zucifugus (Miller). Anat. Rec., 41: 60-61. Horn, E. H. 1958 Effects of feeding thiouracil and/or thyroid powder upon pubic symphyseal separation in female mice. Endocrinology, 63: 481-486. Sherman, H. B. 1937 Breeding habits of the free-tailed bat. J. Mammal., 18: 176-187. Steinetz, B. G. and B. L. Beach 1963 Hormonal requirements for interpubic ligament formation. i n hvuouhvsectomized mice. Endocrinology, 72: fflL776. Steinetz, B. G., J. P. Manning, M. Butler and V. ACKNOWLEDGMENTS Beach 1965 Relationships of growth horThe authors thank Dr. R. J. Stephens mone, steroids and relaxin in the transformation of pubic joint cartilage to ligament i n hyand Dr. 0. W. Henson for procuring the pophysectomized mice. Endocrinology, 76: 876bats. Dr. Henson also assisted in the liter882. ature search. Talmage, R. V. 1947 Changes produced in the symphysis pubis of the guinea pig by the sex LITERATURE CITED steroids and relaxin. Anat. Rec., 99: 91-113. Bernstein. P. and E. S . Crelin 1967 Bony pelvic Vaughan, T. A. 1959 Functional morphology of three bats: Eumops, Myotis, Macrotus. U. of sexual dimorphism in the rat. Anat. Rec.; 157: Kansas Pub., Museum of Nat. Hist., 12: 1-153. 517-526. '65; Hall, '47). The ligament of the mouse is also quite different from that of the free-tailed bat in that it is relatively very much shorter in length and not very elastic during parturition (Crelin, '54b). In addition, the formation of a ligament is not essential for parturition to occur in the mouse (Crelin, '54a). The formation of the interpubic ligament in the bat is without doubt induced and controlled by hormones. Exactly what hormones has yet to be determined. In the mouse it is a combination of estrogen, relaxin, thyroxin and somatotropin (Crelin, '54b; Hall, '60; Horn, '58; Steinetz and Beach, '63). Although the increase in length of the ligament during parturition in the bat is essentially a stretching phenomenon, the ground substance in which the collagenous and elastic fibers are embedded must be in a less dense, colloid-poor, water-rich phase to allow the shifting of position and the sliding of the bundles of collagenous fibers in relationship to each other as the ligament is stretched. Again, this is undoubtedly the result of the influence of hormones as it is in the mouse (Crelin, '63; Gersh and Catchpole, '60; Steinetz et al., '65). The passing out of the single newborn bat from each mother was not witnessed in the present experiment. Sherman ('37) observed that it takes place in about a minute and a half in this species. Not only does the resistance of the mother's pelvic structures have to be overcome during parturition in the free-tailed bat, but the force of gravity as well. The mother hangs in the usual upside-down position while the baby is born tail-end first. - ~ ~~ PLATE 1 EXPLANATION OF FIGURES 2 Ventral view of the bony pelvis of a n adult male. The arrow indicates the pubic symphysis. x 5. 3 Lateral view of the bony pelvis of a n adult male. A projection of bone (P) at the pubic symphysis and a convexity ( C ) along the caudal border of the ischiopubic ramus are indicated. X 5. 4 Ventral view of the bony pelvis of an adult nonpregnant female. Arrows indicate the ends of the two coxal bones interconnected by an interpubic ligament. X 5. 5 Lateral view of the bony pelvis of a n adult nonpregnant female. The irregular surface of the pubic portion of the left coxal bone ( P ) where the interpubic ligament is attached is indicated. The pubic spine (S) is where the psoas minor muscle inserts and is the same in both sexes. X 5. 6 352 Ventral view of the bony pelvis of a pregnant female. Arrows indicate the ends of the two coxal bones interconnected by a n interpubic ligament. x 5. BAT PELVIS PLATE 1 E. S. Crelin and E. V. Newton 353 PLATE 2 EXPLANATION OF FIGURES 7 A newborn bat is shown in its folded condition below the bony pelvis of its mother. The arrow passes behind the interpubic ligament to indicate the route the newborn took through the pelvic birth canal. The newborn and pelvis are magnified exactly the same to show the great disparity between the size of the pelvic birth canal and the newborn free-tailed bat. X 3. 8 354 A full-term fetus, removed by Caesarian section and unfolded, is placed next to its mother to show the relatively large size of the fetus. BAT PELVIS E. S. Crelin and E. V. Newton PLATE 2 355 PLATE 3 EXPLANATION OF FIGURES 9 Section of the ends of the coxal bones ( B ) and attached interpubic ligament (L) from a pregnant bat. X 35. 10 Section of the free border of an interpubic ligament showing the capsular portion ( C ) containing an abundance of elastic fibers. X 400. 11 Section of the pubic symphysis from a n adult male. Indicated are the articular capsule ( C ) of the joint, the hypertrophic hyaline cartilage (H) lining the end of the coxal bone (B), and the compact lamina of fibro-elastic (FE) cartilage in the center of the joint. x 60. 12 Tangential section of the dense layer of elastic fibers in the capsular portion of a n interpubic ligament. x 500. 13 Section of the periphery of the capsular portion of a n interpubic ligament showing loosely-arranged elastic and collagenous fibers. X 500. 14 Section deep to the capsular portion of a n interpubic ligament showing bundles of elastic fibers (arrows) interspersed among dense bundles of collagenous fibers. X 500. 356 BAT PELVIS E. S. Crelin and E. V. Newton PL.\TTE 3 357
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