Baton pass hypothesis: successive incorporation of unconserved endogenous retroviral genes for placentation during mammalian evolution


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Abstract

It is well accepted that numerous RNAs derived from endogenous retroviruses (ERVs) are expressed in mammalian reproductive structures, particularly in the uterus, trophoblast, and placenta. Syncytin 1 and syncytin 2 in humans and syncytin A and syncytin B in mice are membrane proteins originating fromEnvgenes ofERVs. These ERVs are involved in the fusion of trophoblast cells, resulting in multinucleated syncytiotrophoblast formation. Evidence accumulated indicates that syncytin-like fusogenic proteins are expressed in the placenta of rabbits, dogs/cats, ruminant ungulates, tenrecs, and opossums. Thesyncytingenes so far characterized are known to be endogenized to the host genome only within the past 12–80 million years, more recently than the appearance of mammalian placentas, estimated to be 160–180 million years ago. We speculate thatERVs includingsyncytin-like gene variants integrated into mammalian genomes in a locus-specific manner have replaced the genes previously responsible for cell fusion. We therefore propose the ‘baton pass’ hypothesis, in which multiple successiveERVvariants ‘take over’ cell-fusion roles, resulting in increased trophoblast cell fusion, morphological variations in placental structures, and enhanced reproductive success in placental mammals.Mammalian placenta are diversified in their morphological appearances. Endogenous retroviruses have undoubtedly contributed to these placentas. We propose ‘baton pass’ hypothesis, in which different genes, but homologous functions, contributed to placental evolution.

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