Gene expression profiling in the endometrium of pregnant mammals

A major challenge in biology is to determine how evolutionarily novel characters originate, however, mechanistic explanations for the origin of novelties are almost completely unknown. The evolution of mammalian pregnancy is an excellent system in which to study the origin of novelties because extant mammals preserve major stages in the transition from egg-laying to live-birth. To determine the molecular bases of this transition, we characterized the pregnant/gravid uterine transcriptome from tetrapods, including species in the three major mammalian lineages, and used ancestral transcriptome reconstruction to trace the evolutionary history of uterine gene expression. We show that thousands of genes evolved or lost uterine expression during the origins of mammalian pregnancy, including the loss of genes responsible for the mineralization of the eggshell in the Mammalian and Therian stem-lineages, and the recruitment of genes into uterine expression that mediate maternal-fetal communication and maternal immunotolerance of the fetal allograft in the Therian and Eutherian stem-lineages. Our results indicate that one of the defining mammalian novelties evolved through a step-wise process that dramatically changed uterine gene expression, generating a suite of evolutionary innovations that support prolonged gestations. We report genome-wide gene expression generated by mRNA-Seq from the pregnant endometrium of dog, armadillo, and the platypus.