Evolution of viviparity and the maternal immune system: Major histocompatibility complex (MHC) class I genes in skinks

Abstract

With the evolution of viviparity, the complex immune system of vertebrates has become a potential threat to the “semi-foreign” fetus. Mammalian embryos avoid immune rejection by altering placental expression of two types of major histocompatibility complex (MHC) genes, classical class I and non-classical class I genes. While non-classical class I genes are not orthologous across different mammalian species, their role in immune evasion is likely to have evolved in conjunction with viviparity deep in mammalian evolutionary history. It is difficult to investigate the transition to viviparity in mammals, because they display a single, ancient origin of live birth. Alternatively, oviparous and viviparous modes of reproduction in closely related species of squamates (lizards and snakes) make them excellent models for studying the evolution of immunological interactions between mother and embryo. We designed primers to amplify the α1 and α2 regions of MHC class I genes in scincid lizards and present the first class I sequences for skinks. Class I genes are expressed in the uterus of both oviparous and viviparous skinks both at non-reproduction and late gravidity and pregnancy. We found four putative classical and at least two putative non-classical class I genes expressed in the uterus of the viviparous skink Pseudemoia entrecasteauxii, indicating that this species encodes and expresses the genes that may be responsible for the mammalian phenomenon of “hiding” the embryo from the maternal immune system during pregnancy.