Mechanistic constraint and evolutionary history matter for the origin of innovation in animal communication

Abstract Numerous phylogenetic comparative studies have attempted to explain differences in species phenotypes as a function of present-day social or physical environments. In some cases, these investigations have also shown dramatic convergences among distantly related species, illustrating how common selection pressures can produce repeated adaptation. In other cases, distantly related species exhibit phenotypes that appear quite different, and despite putative similarities in selection. Understanding why this is the case is central to our broader knowledge of how evolution operates in nature, and what accounts for the diversity we see in the natural world. Species responding differently to common selection pressures likely traces back to mechanistic constraints and evolutionary starting points bounding the direction of adaptation. These are common themes in evolutionary biology and there is a long history dating back to Lorenz and Tinbergen of considering ‘proximate’ and ‘ultimate’ factors for interpreting present-day behavior. Yet, integration of mechanism and history is still often missing from behavioral ecology. This might reflect the reasonable assumption that behavior is, for the most part, shaped through plasticity or adaptive evolution in response to conditions existing in present-day environments. Yet this assumption fails to explain why species in similar environments so often differ in behavior. Only when behavior is placed into its broader phylogenetic context and explored through the lens of ‘paths-of-least-resistance’ does adaptive innovation even become apparent. Iconic case studies including the sword of swordtails, the song of Darwin finches and the dewlap of anole lizards are examined through this lens to reveal hidden trajectories of adaptation that have led to innovation and diversity.