Parallel evolution of placental calcium transfer in the lizard Mabuya and eutherian mammals

Abstract

ABSTRACT An exceptional case of parallel evolution between lizards and eutherian mammals occurs in the evolution of viviparity. In the lizard genus Mabuya, viviparity provided the environment for the evolution of yolk-reduced eggs and obligate placentotrophy. One major event that favored the evolution of placentation was the reduction of the eggshell. As with all oviparous reptiles, lizard embryos obtain calcium from both the eggshell and egg yolk. Therefore, the loss of the eggshell likely imposes a constraint for the conservation of the egg yolk, which can only be obviated by the evolution of alternative mechanisms for the transport of calcium directly from the mother. The molecular and cellular mechanisms employed to solve these constraints, in a lizard with only a rudimentary eggshell such as Mabuya, are poorly understood. Here, we used RT-qPCR on placental and uterine samples during different stages of gestation in Mabuya, and demonstrate that transcripts of the calcium transporters trpv6, cabp28k, cabp9k and pmca are expressed and gradually increase in abundance through pregnancy stages, reaching their maximum expression when bone mineralization occurs. Furthermore, CABP28K/9K proteins were studied by immunofluorescence, demonstrating expression in specific regions of the mature placenta. Our results indicate that the machinery for calcium transportation in the Mabuya placenta was co-opted from other tissues elsewhere in the vertebrate bodyplan. Thus, the calcium transportation machinery in the placenta of Mabuya evolved in parallel with the mammalian placenta by redeploying the expression of similar calcium transporter genes.