Caudal oviduct coiling in a viperid snake, Crotalus durissus

Abstract

Sperm storage is common in the oviducts of female snakes and results in the decoupling of mating from ovulation and fertilization. In the majority of female snakes examined, sperm storage occurs in receptacles of the infundibular regions of the oviducts. In pitvipers (Viperida, Crotalinae), the storage of sperm was described in the caudal regions of the oviducts (utero‐vaginal junction) through a mechanism termed uterine muscular twisting (UMT). Uterine muscular twisting was described as a twisting of the oviducts after copulation because of uterine contractions. The twisting remains until ovulation at which time the oviducts straighten and sperm migrate cranially to fertilize ovulated ova. Here, we demonstrate that the UMT is not formed by twisting (rotation around axis) of the oviducts of Crotalus durissus but rather coils formed by the inner layers of the oviducts at the utero‐vaginal junction. Contrary to previous findings, coiling of the oviducts is present in females throughout the year, not only in the postcopulatory period; however, the degree of coiling is variable and may be linked to the seasonal reproductive cycle of C. durissus. We categorize the degree of coiling as pronounced coil, discreet coil or absent coil.

Full text

Acta Zoologica. 2020;101:69–77. wileyonlinelibrary.com/journal/azo
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© 2018 The Royal Swedish Academy of Sciences
1
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INTRODUCTION
The reproductive tract of snakes consists of oviducts (derived
from the paramesonephric ducts) and cloaca (Fox, 1997;
Siegel, Miralles, Chabarria, & Aldridge, 2011). The oviducts
are paired, the right being longer than the left (Perkins &
Palmer, 1996), with the left oviduct absent in some smaller
species of snakes (Aldridge, 1992; Blackburn, 1998). The
oviducts are divided into several regions according to struc-
ture and function, from cranial to caudal: infundibulum, tube,
isthmus, uterus and vagina (Blackburn, 1998; Girling, 2002;
Siegel, Miralles, Trauth, & Aldridge, 2011; Uribe, Gonzales‐
Porter, Palmer, & Guillette, 1998). However, terminology of
the oviduct is variable (Girling, 2002); for example, the tube
has been termed the posterior infundibulum by numerous au-
thors (Almeida‐Santos & Orsi, 2002; Blackburn, 1998; Fox,
1956, 1997; Halpert, Garstka, & Crews, 1982; Rojas, 2009;
Saint‐Girons, 1975; Sever & Ryan, 1999; Siegel, Miralles,
Chabarria, et al., 2011). In an effort to standardize nomencla-
ture of the oviduct, Blackburn (1998) simplified the terminol-
ogy to three basic regions in snakes, from cranial to caudal:
infundibulum, uterus and vagina (Blackburn, 1998). In a re-
cent review, Siegel, Miralles, Chabarria, et al. (2011) termed
the uterus and vagina of (Blackburn, 1998) the glandular
uterus and nonglandular uterus, respectively, owing to the
fact that both regions appear to be derived from the parame-
sonephric ducts, with the cranial region (glandular uterus)
possessing endometrial glands, which are absent in the more
caudal region (nonglandular uterus). Thus, nonglandular
uterus and vagina are often synonymous. Distended portions
of the cranial region of the cloaca have also been termed the
vagina, vaginal pouch or pouch in snakes, but the embryonic
origin of these structure has not been assessed (for review
see Siegel, Miralles, & Aldridge, 2011; Siegel, Miralles,
Received: 21 June 2018
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Revised: 27 July 2018
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Accepted: 7 August 2018
DOI: 10.1111/azo.12271
ORIGINAL ARTICLE
Caudal oviduct coiling in a viperid snake, Crotalus durissus
Diego F. Muniz‐Da‐Silva1,2
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Juliana Passos1,2
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Dustin S. Siegel3
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Selma M. Almeida‐Santos2
1Setor de Anatomia, Departamento
de Cirurgia, Faculdade de Medicina
Veterinária e Zootecnia,Universidade São
Paulo, Cidade Universitária, São Paulo,
Brazil
2Laboratório de Ecologia e Evolução,
Instituto Butantan, São Paulo, Brazil
3Department of Biology,Southeast Missouri
State University, Cape Girardeau, Missouri
Correspondence
Diego F. Muniz‐Da‐Silva, Setor de
Anatomia, Departamento de Cirurgia,
Faculdade de Medicina Veterinária e
Zootecnia, Universidade São Paulo, Cidade
Universitária, São Paulo, SP, Brazil.
Email: diegomuniz.vet@gmail.com
Funding information
CNPq
Abstract
Sperm storage is common in the oviducts of female snakes and results in the decou-
pling of mating from ovulation and fertilization. In the majority of female snakes
examined, sperm storage occurs in receptacles of the infundibular regions of the
oviducts. In pitvipers (Viperida, Crotalinae), the storage of sperm was described in
the caudal regions of the oviducts (utero‐vaginal junction) through a mechanism
termed uterine muscular twisting (UMT). Uterine muscular twisting was described
as a twisting of the oviducts after copulation because of uterine contractions. The
twisting remains until ovulation at which time the oviducts straighten and sperm
migrate cranially to fertilize ovulated ova. Here, we demonstrate that the UMT is not
formed by twisting (rotation around axis) of the oviducts of Crotalus durissus but
rather coils formed by the inner layers of the oviducts at the utero‐vaginal junction.
Contrary to previous findings, coiling of the oviducts is present in females through-
out the year, not only in the postcopulatory period; however, the degree of coiling is
variable and may be linked to the seasonal reproductive cycle of C. durissus. We
categorize the degree of coiling as pronounced coil, discreet coil or absent coil.
KEYWORDS
female, oviduct, reproduction, Serpentes, uterine muscular twisting