Cnidarian Eyes as a Meta-Model to Explore Evolutionary Repeatability Over Deep Time

Understanding the extent and nature of evolutionary repeatability is a fundamental goal in biology, with broad relevance to fields including protein engineering, macroevolution, and climate change biology. Studies of evolutionary repeatability often capitalize on convergent evolution as a source of natural replication to examine which genes are recruited or reused in similar traits or adaptations in different lineages. At least two key questions remain: First, how often are the same genes reused across convergent lineages; i.e., what is the extent of gene reuse? Second, what properties make genes more likely to be reused; i.e., what is the nature of gene reuse? An emerging hypothesis is that the overall extent of gene reuse declines with increasing divergence time between converged lineages. While this prediction is supported over shorter timescales, it remains insufficiently tested on deeper times. In this review, I argue that functional compatibility-the degree to which a gene's capabilities align with the functional demands of convergent traits-is a critical factor governing both the extent and nature of gene reuse. I also examine how definitions of gene reuse, ranging from identical substitutions in orthologs to recruitment of paralogs from the same gene families, might affect interpretations and quantification of gene reuse. To explore these ideas, I compare results from the fields of comparative genomics and evo-devo, highlighting possible tension between studies of shorter (<100 MY) versus longer timescales. I also present animal eyes-especially eyes of Medusozoa (Cnidaria)-as a compelling meta-model for studying evolutionary repeatability. Animal eyes have well characterized genetic and functional bases in model organisms and they evolved convergently many times, including at least nine times in cnidarians, spanning a wide range divergence times. Therefore animals eyes, especially when including Medusozoa, will have the potential to test the extent and nature of gene reuse across a wide range of divergence times, providing a more comprehensive understanding of the interplay between constraint, innovation, and divergence time across the history of life.