Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicopsspp.)

Abstract

The evolution of viviparity requires eggshell thinning to bring together the maternal uterus and extraembryonic membranes to form placentae for physiological exchanges. Eggshell thinning likely involves reduced activity of the uterine glands that secrete it. We tested these hypotheses by comparing the uterine and eggshell structure and histochemistry among oviparous and viviparous water snakes (Helicops) using phylogenetic methods. Eggshell thinning occurred convergently in all three origins of viviparity in Helicops and was accomplished by the loss of the mineral layer and thinning of the shell membrane. Uterine glands secrete the shell membrane in both oviparous and viviparous Helicops. These glands increase during vitellogenesis regardless of the reproductive mode, but they always reach smaller sizes in viviparous forms. As there is no phylogenetic signal in eggshell thickness and gland dimensions, we conclude that interspecific differences are related to reproductive mode and not phylogeny. Therefore, our results support the hypothesis that eggshell thinning is associated with the evolution of viviparity and that such thinning result from a reduction in gland size in viviparous taxa. Interestingly, the shell membrane thickness of viviparous females of the reproductively bimodal Helicops angulatus is intermediate between their oviparous and viviparous congeners. Thus, although eggshell thinning is required by the evolution of viviparity, a nearly complete loss of this structure is not. However, uterine gland dimensions are similar across viviparous Helicops. Fewer glands or their functional repurposing may explain the thinner shell membrane in viviparous species of Helicops in comparison to viviparous females of the bimodal H. angulatus.

Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy

“…Thus, viviparous mothers lack or have reduced anatomical structures involved in eggshell production (e.g. Heulin et al ., 2005; Braz et al ., 2018), and provide calcium to embryos via a placenta and in the yolk (Linville et al ., 2010). Species in five skink genera also transport substantial quantities of other nutrients to developing embryos via the placenta (termed obligate placentotrophy), although the condition is otherwise rare (reviewed in Thompson & Speake, 2006; Van Dyke & Griffith, 2018).…”

“…Paul et al ., 2020), histology of gestational tissues (e.g. Guillette Jr. & Jones, 1985; Adams et al ., 2007; Braz et al ., 2018), and behaviour and performance (e.g. Recknagel & Elmer, 2019), which may be underpinned by differences in regulation of gene expression between reproductive modes (e.g.…”

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

“…For this, we used the cell-Sens Imaging software. Values for all measured variables were then averaged to obtain a mean value per female (Braz et al, 2018). We tested for variation in the pouch epithelial height and posterior infundibulum epithelial height between reproductive stages using a t-test and a Wilcoxon signed-rank test, respectively (Zar, 1999).…”

Morphology and seasonality of the sexual segment of the kidney in genus Bothrops snakes

“…We used the periodic acid-Schiff (PAS) reaction to identify neutral carbohydrates and Alcian blue (AB) 8GX (pH 2.5) to identify carboxyl and sulfate-ester groups of acid mucosubstances (Kiernan, 2008). To detect proteins, we used Coomassie brilliant blue (CBB) R250 diluted at 0.04 mg ml À1 (Braz et al, 2018).…”