A histological and ultrastructural investigation of the female reproductive system of the water snake (Erythrolamprus miliaris): Oviductal cycle and sperm storage

Abstract

We studied the structural and cellular organisation of the oviduct of Erythrolamprus miliaris including its morphological variation during the reproductive cycle using light microscopy, scanning electron microscopy and transmission electron microscopy. Four anatomically distinct regions compose the oviduct of E. miliaris including the anterior and posterior infundibulum, glandular uterus, non‐glandular uterus and pouch. The cells of the oviductal epithelium secrete material by apocrine and merocrine processes, which vary between the anatomical regions and according to each phase of the reproductive cycle. The infundibular epithelium secretes electron dense vacuoles, which suggests the production of lipids, whereas the epithelial secretion of the glandular uterus, non‐glandular uterus and pouch creates lucent and slightly electron dense vacuoles, indicating the production of glycoproteins. The timing of mating, vitellogenesis and sperm storage directly influences the morphofunctional alterations in the oviducts of E. miliaris. Sperm storage occurs only in the infundibular receptacles with increased production of the neutral carbohydrates in the presence of male gametes. Sperm storage happens in vitellogenic, non‐vitellogenic and pregnant females of E. miliaris. Thus, females may be able to produce multiple clutches at different seasons of the year regardless of mating during autumn.

Full text

Acta Zoologica. 2019;100:69–80. wileyonlinelibrary.com/journal/azo
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69
© 2017 The Royal Swedish Academy of Sciences
Accepted: 13 November 2017
DOI: 10.1111/azo.12234
ORIGINAL ARTICLE
A histological and ultrastructural investigation of the female
reproductive system of the water snake (Erythrolamprus miliaris):
Oviductal cycle and sperm storage
Claudio Augusto Rojas
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Verônica Alberto Barros
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Selma Maria Almeida-Santos
Laboratory of Ecology and Evolution,
Butantan Institute, São Paulo, Brazil
Correspondence
Claudio Augusto Rojas, Laboratory of
Ecology and Evolution, Butantan Institute,
São Paulo, Brazil.
Email: dipsas@hotmail.com
Funding information
Conselho Nacional de Desenvolvimento
Científico e Tecnológico-CNPQ
Abstract
We studied the structural and cellular organisation of the oviduct of Erythrolamprus
miliaris including its morphological variation during the reproductive cycle using
light microscopy, scanning electron microscopy and transmission electron micros-
copy. Four anatomically distinct regions compose the oviduct of E. miliaris includ-
ing the anterior and posterior infundibulum, glandular uterus, non- glandular uterus
and pouch. The cells of the oviductal epithelium secrete material by apocrine and
merocrine processes, which vary between the anatomical regions and according to
each phase of the reproductive cycle. The infundibular epithelium secretes electron
dense vacuoles, which suggests the production of lipids, whereas the epithelial secre-
tion of the glandular uterus, non- glandular uterus and pouch creates lucent and
slightly electron dense vacuoles, indicating the production of glycoproteins. The tim-
ing of mating, vitellogenesis and sperm storage directly influences the morphofunc-
tional alterations in the oviducts of E. miliaris. Sperm storage occurs only in the
infundibular receptacles with increased production of the neutral carbohydrates in
the presence of male gametes. Sperm storage happens in vitellogenic, non- vitellogenic
and pregnant females of E. miliaris. Thus, females may be able to produce multiple
clutches at different seasons of the year regardless of mating during autumn.
KEYWORDS
Erythrolamprus miliaris, histology, oviduct, sperm storage receptacle, ultrastructure
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INTRODUCTION
The reptilian oviduct shows some anatomical variation
among different lineages (Blackburn, 1998; Girling, 2002).
At the macroscopical level, the oviducts are more elongated
in snakes than lizards, and at the microscopical level, the ovi-
ducts may show the presence or absence of glands and dif-
ferent types of epithelium in each portion (Blackburn, 1998;
Girling, 2002). Despite the existence of different oviductal
patterns, the tissue structure is very similar among the clades.
From the innermost layer to the outer layer, the oviduct is
composed by the epithelium, shell gland, connective tissue,
circular muscle, longitudinal muscle and serosa (Barros,
Rojas, & Almeida- Santos, 2014b; Girling, 2002; Rojas,
Barros, & Almeida- Santos, 2015). However, it is important
to highlight that there are different proposals of nomenclature
for the oviductal regions in snakes (Blackburn, 1998; Rojas
et al., 2015; Siegel, Miralles, Chabarria, & Aldridge, 2011;
Siegel & Sever, 2008a,b). For example, the infundibulum may
be divided into anterior and posterior and the uterus in glan-
dular and non- glandular portions (Blackburn, 1998; Siegel &
Sever, 2008a,b). Siegel et al. (2011) also suggest the use of
the term “pouch” to characterise the most caudal oviductal
portion, previously known as the Giacomini’s diverticulum