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Placental calcium provision in a lizard with prolonged oviductal egg retention

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Abstract

A prominent scenario for the evolution of viviparity and placentation in reptiles predicts a step-wise pattern with an initial phase of prolonged oviductal egg retention accompanied by progressive reduction in eggshell thickness culminating in viviparity; calcium placentotrophy evolves secondarily to viviparity. Saiphos equalis is an Australian scincid lizard with a reproductive mode that is uncommon for squamates because eggs are retained in the oviduct until late developmental stages, and the embryonic stage at oviposition varies geographically. We studied calcium mobilization by embryos in two populations with different oviductal egg retention patterns to test the hypothesis that the pattern of nutritional provision of calcium is independent of the embryonic stage at oviposition. Females from one population are viviparous and oviposit eggs containing fully formed embryos, whereas embryos in oviposited eggs of the second population are morphologically less mature, and these eggs hatch several days later. The reproductive mode of this population is denoted as prolonged oviductal egg retention. Yolk provided the highest proportion of calcium to hatchlings in both populations. Eggs of both populations were enclosed in calcified eggshells, but shells of the population with prolonged egg retention had twice the calcium content of the viviparous population and embryos recovered calcium from these eggshells. Placental transfer accounted for a substantial amount of calcium in hatchlings in both populations. Hatchling calcium concentration was higher in the population with prolonged egg retention because these embryos mobilized calcium from yolk, the eggshell and the placenta. This pattern of embryonic calcium provision in which both a calcified eggshell and placentotrophy contribute to embryonic nutrition is novel. The reproductive pattern of S. equalis illustrates that calcified eggshells are compatible with prolonged oviductal egg retention and that viviparity is not requisite to calcium placentotrophy.

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Acknowledgments

We are grateful to Scott van Barneveld for help with collection of specimens, to Laura Lindsay and Chris Murphy for advice and use of laboratory facilities, and to Phillip Scheuerman and Brian Evanshen for use of the Atomic Absorption Spectrophotometer. Animals were collected under permit S10693 issued by the New South Wales National Parks and Wildlife Service. All procedures related to animals were approved by The University of Sydney Animal Care and Ethics Committee (L04/9-2006/1/4444). Funding was provided by a grant from The National Science Foundation (IOB-0615695) (JRS and TWE) and an Australian Research Council Discovery Grant (MBT).

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Correspondence to James R. Stewart.

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Communicated by I. D. Hume.

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Linville, B.J., Stewart, J.R., Ecay, T.W. et al. Placental calcium provision in a lizard with prolonged oviductal egg retention. J Comp Physiol B 180, 221–227 (2010). https://doi.org/10.1007/s00360-009-0400-2

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  • DOI: https://doi.org/10.1007/s00360-009-0400-2

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