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

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 mechanism 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 its 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.

Functional complexity in the chorioallantoic membrane of an oviparous snake: Specializations for calcium uptake from the eggshell

“…Calbindin‐D 28K is a cytosolic protein implicated in facilitation of transcytoplasmic movement of calcium. A similar pattern of expression of calbindin‐D 28K occurs in the chorioallantoic membranes of other oviparous and viviparous squamates (Fregoso et al, 2010; Hernandez‐Diaz et al, 2021; Stewart et al, 2011; Stinnett et al, 2012).…”

“…Although placental transport is a highly specialized reproductive function, transcytoplasmic calcium transport is a conserved physiological mechanism utilized by a variety of tissues (Bar, 2008; Hoenderop et al, 2005). Among squamates, calbindin‐D 28K is associated with transcytoplasmic calcium transport by chorioallantoic membranes of both oviparous and viviparous squamates (Hernandez‐Diaz et al, 2021; Fregoso et al, 2010; Stewart et al, 2011; Stinnett et al, 2012). In addition, both calbindin‐D 9K and calbindin‐D 28K are expressed in specialized chorionic epithelial cells in the placentotrophic lizard, Mabuya sp.…”

“…In addition, both calbindin‐D 9K and calbindin‐D 28K are expressed in specialized chorionic epithelial cells in the placentotrophic lizard, Mabuya sp. (Hernandez‐Diaz et al, 2021). Explanations for the similarity between squamates and mammals are relevant to the pattern of variation within Sauropsida.…”

“…Vascular support is provided by allantoic blood vessels and the tissue is the primary organ for physiological exchange of respiratory gases and water between the embryo and the external environment. The chorioallantoic membrane also serves a significant nutritional role in mobilizing calcium from the eggshell of oviparous reptiles (Packard, 1994), or directly from the uterus of viviparous species (Hernandez‐Díaz et al, 2021; Stewart & Ecay, 2010; Stinnett et al, 2012).…”