Monotreme transcriptomes shed light on evolution of lactation and placentation

Abstract

Placentation and lactation are hallmark mammalian reproductive traits and key processes facilitating the transfer of nutrients from the mother to the offspring. The basal mammalian lineage of egg-laying monotremes features a short gestation period supported by a simple placenta and an elongated lactation, similar to marsupials. Eutherian mammals by contrast evolved longer gestation facilitated by extensive placentation and shorter lactation. To understand the gene expression underpinning maternal-foetal nutrient transfer across mammals, we generated transcriptome datasets for the monotreme reproductive tract and mammary gland and compared this to expression in representative species from the other mammalian clades: marsupials (Tammar wallaby) and eutherians (mouse). This revealed extensive overlapping gene expression between the therian placenta and monotreme reproductive tract, including the first observation of retroviral gene expression in the echidna reproductive tract. Interestingly, we discovered that transport and development functions supporting foetal growth are expressed in echidna mammary gland and eutherian placenta, likely a signature of the shift from prolonged lactation to longer placentation. Together, this demonstrates that diverse modes of maternal-foetal nutrient transfer are underpinned by similar gene networks across mammals.