Legacy and innovation in the biological evolution of complex light-detecting and light-producing systems

One of the great paradigm shifts induced by the advent of comparative genomics was realizing genomes are not fine-tuned systems optimized for current function, but rather complicated Rube-Goldberg-like devices resulting from the long-term interplay of structure, function, and an uninterruptible history. With a particular focus on vision (eyes) and bioluminescence (photophores), I explore the metaphor of genetic toolkits, which can be operationalized as lists of genes involved in a trait of interest. A fascinating observation is that genes of a toolkit are often used again and again during repeated evolution of complex traits, sometimes in vastly different organisms. Such a pattern requires both the maintenance (availability), and the redeployment of ancient genes in repeatedly evolved structures. Maintenance of genetic toolkits over long evolutionary timescales requires gene multifunctionality to prevent loss when a trait of interest is absent. The deployment of toolkit genes in repeatedly evolved traits like eyes and light-producing organs sometimes involves similar, ancient genes but other times involves different genes specific to each repeated origin. How often a particular genetic solution is used time and again for the same function may depend on how many possible biological solutions are available. When few solutions exist and are available, evolution is constrained to use the same genes over and over. However, when many different solutions are possible, the innovative possibilities of evolution are often on display. Therefore, a focus on genetic toolkits highlights the combination of legacy plus innovation that drives the evolution of biological diversity.