Development of the uterine shell glands during the preovulatory and early gestation periods in oviparous and viviparous Lacerta vivipara

Abstract

The evolutionary process leading to the emergence of viviparity in Squamata consists of lengthening the period of egg retention in utero coupled with marked reduction in the thickness of the eggshell. We used light microscopy and scanning electron microscopy to study uterine structure during the reproductive cycle of oviparous and viviparous females of the reproductively bimodal Lacerta vivipara. We compared the structure of the uterine shell glands, which secrete components of the eggshell, during preovulatory and early gestation phases of the reproductive cycle and also compared histochemistry of the eggshells. The uterine glands of both reproductive forms undergo considerable growth within a period of a few weeks during folliculogenesis and vitellogenesis preceding ovulation. The majority of the proteinaceous fibers of the shell membrane are secreted early in embryonic development and the uterine glands regress shortly thereafter. This supports previous observations indicating that, in Squamata, secretion of the shell membrane occurs very rapidly after ovulation. The most striking differences between reproductive modes were larger uterine glands at late vitellogenesis in oviparous females, 101 microm compared to 60 microm in viviparous females, and greater thickness of the shell membrane during early gestation in oviparous females (52-73 microm) compared to viviparous females (4-8 microm). Our intraspecific comparison supports the conclusions of previous studies that, prior to ovulation, the uterine glandular layer is less developed in viviparous than in oviparous species, and that this is the main factor accounting for differences in the thickness of the shell membrane of the two reproductive forms of squamates.

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

“…Previous dissection of recently ovulated eggs revealed that eggshells from oviparous females were eight times heavier (dry mass, 8 mg) than the embryonic membranes of viviparous females (1 mg), whereas yolk content of ovulated ova (mean dry mass, 55 mg) did not differ between the two reproductive modes (Stewart et al, 2009). Thus oviparous and viviparous female Z. vivipara are very similar in their pre-ovulation reproductive allocation except for the synthesis of the eggshell components that are stored in the uterine glands prior to ovulation and then deposited on the fertilized ova shortly after ovulation (Heulin et al, 2005). While synthesis of these shell components requires morphological modification of uterine epithelium (Adams et al, 2004), our results suggest that preparation for egg shelling has a negligible energy demand.…”

“…Large windows provided natural light for about 12 h day -1 . In order to elicit reproduction and synchronize the reproductive cycles, the lizards were overwintered in the laboratory using a standard protocol (Gavaud, 1983;Heulin et al, 2005). On 1 October, lizards were placed in small boxes containing damp sand and wet moss, and these boxes were placed in a dark chamber (brand Liebherr, Dortmund, Germany) that was cooled progressively from 10 to 4°C during the first week, and then maintained at a constant 4°C thereafter.…”

“…Therefore, viviparity in most squamates can be viewed as an extension of oviparous egg retention with associated complex physiological adaptation to support intrauterine life (Shine, 1983, Van Dyke et al, 2014). Yet one important difference between oviparous and viviparous squamates is the pronounced development of uterine eggshell glands prior to ovulation in oviparous forms (Heulin et al, 2005) (see also references therein). This difference could result in significantly higher maternal energy costs in oviparous species during the preovulation period.…”

“…Viviparous female Z. vivipara give birth to fully formed offspring (final stage 40) (Dufaure and Hubert, 1961), whereas oviparous females oviposit eggs with embryos between stages 30 and 35 (Braña et al, 1991;Heulin et al, 1991;Heulin et al, 2002). In the oviparous mode, the yolk (vitellus) and embryo are encased in an eggshell composed of a thick (40-65 μm) mat of fibrous protein overlaid by a thin (few micrometers) layer of calcium crystals (Heulin, 1990;Heulin et al, 2002;Heulin et al, 2005). The embryos of viviparous females are also lecithotrophic, but are enveloped in a very thin shell membrane (6-10 μm of fibrous protein without a calcium layer) throughout gestation (Panigel, 1956;Heulin, 1990).…”

The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes

“…Possibly to facilitate the flux of oxygen and carbon dioxide, squamates exhibit progressive thinning of the eggshell the longer eggs are retained before oviposition (Heulin 1990, Qualls 1999, Heulin et al 2002. The eggshell and shell membrane are thinned via reductions in either the number of shell glands present in the oviduct (Guillette 1993), or a reduction in the size of the shell gland which presumably impedes function (Heulin et al 2005). Most viviparous species retain a reduced eggshell membrane (Blackburn 1998), but it is lost during gestation in placentotrophic species (Blackburn et al 1984.…”