The evolution of cis and trans-regulators in eukaryotes – CisTransEvol

Gene regulation plays an essential role in shaping species differences and modulating phenotypes across development and environmental conditions. It essentially works through the recruitment of trans-acting intermediates to cis-acting DNA sequences affecting the expression of the nearby gene. While gene expression regulation is central in molecular, cellular, developmental, and system biology, its detailed mechanisms have relatively little been incorporated into modern evolutionary theory. We previously discovered two processes specific to gene expression evolution in diploids, cis-regulator runaway and divergence. They arise because of (i) transient dominance modifications that automatically occur following the evolution of cis-acting regulatory elements and (ii) coevolution of these cis-acting elements with trans-acting regulators. We have shown that accounting for these processes calls into question a half-century of theory on sex chromosome evolution and may completely rejuvenate empirical and theoretical work in this field. Here, we will develop the evolutionary theory of cis- and trans-regulators at full scale and empirically test its core features and predictions. Specifically, there are sound reasons to believe that this new theory also has the potential to revolutionize our understanding of other fundamental and enigmatic features of eukaryotic life. It may be a crucial missing element for illuminating the deep evolutionary mysteries of (i) the origin of eukaryotic genome complexity and (ii) the structure of eukaryotic gene regulatory networks. It also may explain (iii) how and why sex – asex transitions fail or succeed and, therefore, why eukaryotic sex is maintained. CisTransEvol offers a radically new groundbreaking approach to important problems in evolutionary biology. If successful, it will be a tremendous advance in our understanding of eukaryotic life-forms and provides a general framework for gene expression evolution in eukaryotes.