Probing the Depths of Biological Diversity During the Second Century of GENETICS.

After a century of GENETICS, we understand better than ever the diversity of life and its immense evolutionary history. Nevertheless, we are still gazing at the tip of the iceberg of biological complexity. For virtually every biological rule, an exception lies in some organism on some branch of the tree of life. Meiosis is fair. Mating is random. Chromosomes govern inheritance. The genetic code is universal. All have exceptions (meiotic drive: Buckler et al. 1999 and Didion et al. 2016; mating: Jiang et al. 2013; inheritance: Fang et al. 2012 and Houri-Ze’evi et al. 2016; genetic code: Saccone et al. 2000). In contemplating what is in store for the journal GENETICS in its second century, we argue that our vision of genetics will move increasingly away from trying to understand the general pattern of biology toward grappling with its variability and, in so doing, better reveal the depths of biological complexity. Biological complexity is often discussed as the product of an evolutionary history spanning the 4.1 billion years since the origin of life (Bell et al. 2015), but even this number is misleadingly small. Evolution is not linear: it branches into species, which explore, in parallel, different ways of surviving and reproducing. This exploration spans more than 1014 years of evolutionary discovery (Figure 1), a staggering number. By comparison, there are an estimated 1014 letters in total in all of the published books across human history (Urban 2014). It is no wonder that life is so variable. Contemplating this breadth of evolutionary history is essential if one is to understand the richness of biology. Historically, we have done the reverse. We have stripped out the complexities, alternative contexts, and species interactions. This is a natural and necessary thing to do when first seeking out the impact of what a gene does or how a population evolves, but a full understanding of biology requires that we expand our viewpoint and consider alternative contexts and understudied organisms from across the tree of life. Why do genes not always perform in the same way? Why do populations not always evolve in the same direction? Although biologists, both theoreticians and empiricists, have beenmoving in this direction for decades, we argue that in the next century, our focuswill shift from a search for general rules to a greater appreciation of biological variability. We describe ways in which we expect this shift to impact genetics and evolution.