Structure and morphogenesis of the uterus, placenta, and paraplacental organs of the neotropical disc-winged bat Thyroptera tricolor spix (Microchiroptera: Thyropteridae).

Abstract

The structure and development of the female reproductive tract, fetal membranes and placental have not previously been recorded for any member of the family Thyropteridae. Recently implanted embryos were obtained in late January, limb-bud stages in March, and full-term fetuses in late May, suggesting a possible gestation length of approximately five months. It is likely, however, that Thyroptera experiences at least two breeding cycles per year. The uterus was narrowly bicornuate; the corpus uteri was unusually large and lacked the glandular density observed in the cornua. The cervix was long, pleated, and relatively aglandular. The oviducts opened at the apices of the cornua; oviductal papillae were absent. A bursa ovarii surrounded the ovary, but there was a small pore opening to the peritoneal cavity adjacent to the fimbriated end of the oviduct. Never more than a single embryo or fetus was present, and only a single corpus luteum was observed; thus Thyroptera, like most bats, is monovular. Ovoimplantation was interstitial; a decidua capsularis was present early but disappeared by the late limb-bud stage. The decidual reaction involved both glandular epithelium and stromal cells, but most of the decidua was destroyed by term. Amniogenesis was initiated after implantation, by cavitation. Primitive entoderm was formed precociously above, as well as below, the presumptive embryonic disc, and a thin extension of Reichert's membrane passed over the cell mass, separating it from the cytotrophoblast of the chorionic placenta. During the amniogenic period, the yolk-sac entoderm fused to the parietal trophoblast via an intervening Reichert's membrane, forming an extensive bilaminar omphalopleure; this was rapidly converted to a trilaminar structure in early post-implantation stages. An avascular chorio-vitelline relationship involved most of the chorionic wall in early post-implantation stages and persisted to term in the abembryonic hemisphere after the partial inversion of the yolk-sac roof in late presomite embryos. The invaginated yolk-sac roof (splanchnopleure) also persisted to term as a viable paraplacental component. A small sac-like allantois was formed between late presomite and early limb-bud stages but disappeared by the late limb-bud stage. Development of the definitive chorioallantoic placenta resembled that in other bats, but the maternal endothelium disappeared relatively early, and trophoblastic differentiation was precocious. The ultrastructural organization of the interhemal membrane was hemodichorial, and otherwise generally resembled the organization previously described in vespertilionid bats. Similarities and differences in the structure of the uterus, placenta, and paraplacental organs of Thyropteridae, in comparison with other families of bats, are discussed. On the basis of fetal membrane characteristics, the Thyropteridae show closer affinities with the Phyllostomatoidea than with the Vespertilionoidea, to which they are presently assigned.