The repeatability of the genetic mechanisms underlying behavioral evolution

Diverse species of the spider genus Tetragnatha spin similar web architectures; different anoles lizard species bob their heads with the same styles and speeds; distinct species of damselflies avoid predators using the same behavioral modules and techniques. These and many other striking examples of convergent evolution of behaviors have been observed in nature for decades. Does this convergence reflect constraints that lead to evolutionary repeatability or flexibility that provides many ways of achieving the same end? Genetics clearly play a role, but it remains challenging to identify the genes that underlie behavioral evolution because classical genetics identifies alleles that are not evolutionarily relevant while most quantitative genetic methods lack the resolution to identify causative variants. Convergent evolution in developmental or physiological traits has been discovered in over a hundred specific examples of genes and mechanisms that cause shared phenotypes, so it is possible. Therefore, we propose to discover the first genes and molecular mechanisms that underlie convergent evolution of behaviors. The Caenorhabditis nematodes offer a powerful experimental platform to connect phenotypic variation to genetic differences. Starting with the keystone model organism, C. elegans, and existing data, we will characterize and classify genetic variation across wild isolates from three species of Caenorhabditis - C. briggsae, C. elegans, and C. tropicalis. These genotype data combined with high-throughput, high-content imaging of behaviors from these same wild isolates will be input into unsupervised machine learning algorithms to create a high-resolution genotype-phenotype map. This map will be queried for signatures of selection at orthologous genes to identify which variants are most important evolutionarily. The result will be the first systematic glimpse into the genomic “knobs” that control behavior at single-variant resolution and insights into the repeatability of the evolution of behaviors across species.