Our paper: Lineage-specific transposons drove massive gene expression recruitments during the evolution of pregnancy in mammals

Our next “our paper” guest post is by Vincent Lynch [@VinJLynch] who’s just joined the UChicago faculty from a postdoc at Yale. He’s posting about his recently arXived paper:

Lineage-specific transposons drove massive gene expression recruitments during the evolution of pregnancy in mammals. ArXived here.
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Explaining how morphology evolves is a major challenge in biology. While it’s clear that changes in gene regulation are ultimately responsible for the development and evolution of complex characters, we are only just beginning to understand the molecular mechanisms of gene regulatory evolution. This is largely due to the emergence of new technologies, such as mRNA-Seq and ChIP-Seq, which give biologists the tools to explore evolution across the genome and in non-model species.

We took advantage of these methods to explore the evolution of gene expression in the uterus during the origin of pregnancy in mammals. Using mRNA-Seq, we show that gene expression evolved extremely rapidly during major stages in the evolution of pregnancy, for example during the origin of maternal resource provisioning in the stem-lineage of Mammalia, placentation in the stem-lineage of Theria, and implantation in the stem-lineage of Eutheria. Using ChIP-Seq to identify the cis-regulatory elements of genes recruited into uterine expression in mammals suggests that the majority of enhancers and promoters derived from mammalian lineage-specific transposons.

While recent technological advances are changing the way we do biology (see Wagner 2013), as these emerging methods come into the mainstream we must collectively define our new standards of evidence. What experiments and methods build a convincing case for X? Is it sufficient, for example, to conclude that a transposon donated a novel promoter to a gene if a ChIP-Seq peak for a histone mark associated with promoters lies within the transposon? If we then expand that observation across the genome, can we reasonably conclude that transposons are casually responsible for gene regulatory change? For these reasons we chose to post our manuscript as a work-in-progress to arXiv, both as our contribution to the larger discussion of what constitutes the standards of evidence in this emerging field of biology and as an opportunity to receive feedback from our colleagues to complement formal peer-review.

Vincent Lynch

Lineage-specific transposons drove massive gene expression recruitments during the evolution of pregnancy in mammals

Lineage-specific transposons drove massive gene expression recruitments during the evolution of pregnancy in mammals
Vincent J. Lynch, Mauris Nnamani, Kathryn J. Brayer, Deena Emera, Joel O. Wertheim, Sergei L. Kosakovsky Pond, Frank Grützner, Stefan Bauersachs, Alexander Graf, Aurélie Kapusta, Cédric Feschotte, Günter P. Wagner
(Submitted on 22 Aug 2012)

A major challenge in biology is explaining how novel characters originate, however, the molecular mechanisms that underlie the emergence of evolutionary innovations are unclear. Here we show that while gene expression in the uterus evolves at a slow and relatively constant rate, it has been punctuated by periods of rapid change associated with the recruitment of thousands of genes into uterine expression during the evolution of pregnancy in mammals. We found that numerous genes and signaling pathways essential for the establishment of pregnancy and maternal-fetal communication evolved uterine expression in mammals. Remarkably the majority of genes recruited into endometrial expression have cis-regulatory elements derived from lineage-specific transposons, suggesting that that bursts of transposition facilitate adaptation and speciation through genomic and regulatory reorganization.