Infundibular sperm storage and uterine muscular twisting in the Amazonian lancehead, Bothrops atrox

Abstract

Although knowledge about the reproduction of snakes of the genus Bothrops has increased recently, many questions remain regarding sperm storage by these neotropical pitvipers. The relationship between two known sperm storage sites-the nonglandular uterus and the infundibulum-has yet to be detailed for Bothrops. In addition, the formation of uterine muscular twisting (UMT) and its function in sperm storage in the nonglandular uterus have been questioned. This article presents data on both sperm storage sites (posterior infundibulum and nonglandular uterus) in the Amazonian lancehead, Bothrops atrox, aiming to address the role of UMT in bothropoid reproduction considering female reproductive stages, timing of sperm storage, and morphology and histochemistry of sperm receptacles. The oviduct of B. atrox is composed of the infundibulum (anterior and posterior), the glandular uterus, the nonglandular uterus and the pouch. Sperm storage occurs in the posterior infundibulum and nonglandular uterus in vitellogenic females. In the posterior infundibulum sperm is stored in receptacles, while in the nonglandular uterus it is stored in crypts in the UMT of vitellogenic females. Both sperm storage sites possess granules testing positive for neutral mucopolysaccharides in the presence of spermatozoa, possibly favoring the conditions for spermatozoa surveillance during sperm storage in the reproductive tract.

Reproduction in the bushmaster (Lachesis muta): Uterine muscular coiling and female sperm storage

“…Contrary to expectations, we observed UMC in a gravid female of L. muta. Similar findings have also been reported in two species of pitvipers, Bothrops atrox and B. jararacussu (Silva et al, 2019;. The gravid female with UMC had recently ovulated (judging by the absence of an embryo in the egg), which may explain why the UMC had not yet uncoiled.…”

“…Seigel and Sever (2006;2008a) argue that sperm only pass through the UMC region before reaching the posterior infundibulum, where they would actually be stored. Recently, Silva et al (2019) stated that although the UMC does not completely block the passage of sperm to more cranial regions of the oviduct, its morphology and secretory activity may contribute to sperm survival and viability until fertilization, as previously proposed by Almeida-Santos and Salomão (2002). Our finding of gravid and nonreproductive (previtellogenic) females with sperm in the oviduct agrees with the idea that UMC does not act as a barrier to the passage of sperm (Silva et al, 2019).…”

“…Recently, Silva et al (2019) stated that although the UMC does not completely block the passage of sperm to more cranial regions of the oviduct, its morphology and secretory activity may contribute to sperm survival and viability until fertilization, as previously proposed by Almeida-Santos and Salomão (2002). Our finding of gravid and nonreproductive (previtellogenic) females with sperm in the oviduct agrees with the idea that UMC does not act as a barrier to the passage of sperm (Silva et al, 2019). The presence of sperm in these females may also be a remnant of previous reproductive event.…”

“…The UMC consists of a morphological change in the circular muscle layer and the mucosa layer characterized by a spiral-like pattern when contracted (Muniz-Da- Silva et al, 2020). The furrows formed by the UMC may retain sperm in this region (Almeida-Santos & Salomão, 1997Barros et al, 2012;Barros et al, 2014a), and its secretory activity may maintain sperm viability (Silva et al, 2019). Salomão (1997, 2002) also proposed that Neotropical pitvipers (Bothrops and Crotalus) retain an ancestral reproductive pattern, characterized by autumn mating and spring ovulation.…”

Exceptional long-term sperm storage by a female vertebrate

“…Post mating, spermatozoa ascend the reproductive tract until reaching these, and sperm is believed to be stored until ovulation. Similarly, uterine muscular twisting has been reported in viperids and also could play a role [ 60 – 65 ]. After copulation, uterine contractions may result in a twisting of the oviducts, with untwisting and therefore sperm migration occurring only after ovulation [ 63 ].…”