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

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.
Keywords
comparative methods;  eggshell formation;  oviduct histochemistry;  oviparity;  shell glands;  uterine morphology

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Braz HBP, Almeida-Santos SM, Murphy CR., Thompson MB.. Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicops spp.). J Exp Zool B Mol Dev Evol. 2018 May;330(3):165-80. doi:10.1002/jez.b.22800.
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