Postdoc Researcher
Unit for Theoretical Biology, Department of Evolutionary Biology
University of Vienna
Abstract
Human pregnancy is notoriously difficult. More than 10% of women have experienced a miscarriage, and some 30-50% of fertilized embryos are shed in menstruation without the mother ever knowing she was pregnant. Why is reproduction, the essential part of an organism’s life for its evolutionary success, subject to such frequent failure? One explanation is that the female reproductive system has evolved not just to nurture offspring, but to select among them, and this legacy created predispositions to pregnancy complications which persist to today. Overproduction of offspring, and subsequent selection of few to carry to term, evolved independently in distant mammalian lineages: pronghorns, tenrecs, elephant shrews, viscachas, and – if spontaneous miscarriages are counted – in humans. Extreme phenotypes have resulted, such as fertilization of more than 100 zygotes reduced to just two survivors at term. This extreme scenario is called a “selection arena”, and its theorized function is to identify embryos distinct from others in DNA integrity, specific alleles, or signaling output. A selection arena is a complex innovation, unlikely evolve in a single step. I hypothesize that selection arenas arise from 1) a restricted implantation window, spatially or temporally as in menstruation 2) biosensory functions of uterine cells to screen embryos and 3) a way to rapidly prototype embryos, such as polyovulation. I use examples of extreme embryo selection in the elephant shrew and plains viscacha to outline how these three components – the arena, biosensor, and contestant arms of embryo selection – evolve in concert. A yet untested prediction in these systems is whether embryos exhibit inter-individual variation in genomic integrity and whether that associates with signaling outputs perceivable by the mother. Addressing these questions has the potential to inform how complex traits evolve, with relevance to quality-control processes beyond biology and their vulnerability to dysfunction.