Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara

Abstract

SUMMARYEmbryos of oviparous squamate reptiles typically obtain calcium from both yolk and eggshell but differ from other oviparous amniotes (turtles, birds and crocodilians) because they are heavily dependent on calcium-rich yolk. Eggs of viviparous squamates lack calcareous eggshells, and embryos receive calcium solely from yolk or from both yolk and placenta. The pattern of calcium mobilization by amniote embryos has been predicted to influence the evolution of viviparity if embryos are dependent on calcium from the eggshell and calcium placentotrophy evolves subsequent to viviparity. We studied the pattern of maternal provision and embryonic utilization of calcium of an oviparous and a viviparous population of the reproductively bimodal lizard Lacerta vivipara to test the hypotheses: (1) oviparous embryos are not dependent on eggshell calcium and (2) calcium content of viviparous hatchlings does not differ from oviparous hatchlings. Our findings do not support either of these hypotheses because oviparous females oviposited eggs with heavily calcified shells and calcium-poor yolk, and embryonic mobilization of shell calcium was greater than for other oviparous squamates. The calcium content of yolk from viviparous females did not differ from oviparous yolk, but viviparous eggs lacked calcareous eggshells. Uterine secretion by viviparous females compensated for the low calcium content of yolk, and placental calcium transfer was among the highest recorded for squamates. The pattern of calcium provision in these two populations suggests that dependence on uterine calcium, either stored temporarily in an eggshell or transferred directly across a placenta, did not constrain the evolution of reproductive mode in this lineage.

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).…”

“…Both of these populations have been used previously for studies of embryonic development (Stewart et al, 2004;Stewart et al, 2009). Captured lizards were transported to the Station Biologique de Paimpont.…”

Developmental expression of calcium transport proteins in extraembryonic membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae)

“…In the absence of an alternative source of calcium, the evolution of viviparity would result in a nutritional deficit to developing embryos (Packard et al, 1977). Recent research on lizard species with geographic variation in their mode of parity reveals that embryos of viviparous populations receive roughly the same amount of calcium from placental transport as oviparous embryos extract from eggshells (Stewart et al, 2009;Linville et al, 2010). In addition, the ontogenetic pattern of embryonic calcium mobilization does not differ between reproductive modes.…”

“…Oviparous females oviposit eggs with thick eggshells containing an outer layer of calcium carbonate (Heulin, 1990;Heulin et al, 2002) that provide a substantial amount (81%) of the calcium contained in hatchlings (Stewart et al, 2009). Viviparous females produce thin eggshells that lack an outer layer of calcium carbonate and give birth to (Heulin, 1990;Heulin et al, 1991).…”

“…Viviparous females produce thin eggshells that lack an outer layer of calcium carbonate and give birth to (Heulin, 1990;Heulin et al, 1991). These females provide most of the calcium (76%) contained in neonates via placental transport and the pattern of embryonic acquisition of calcium does not differ from that of oviparous embryos (Stewart et al, 2009 Tissues were harvested from Z. vivipara embryos from populations that were the subject of a previous study of embryonic patterns of calcium acquisition (Stewart et al, 2009). Oviparous females were collected in September 2008 (N15) from Louvie, France (43°06ЈN, 0°23ЈW, elevation 370m).…”