Coordination Failures Generate Selection Gradients in Animal Collectives
Collective animal behavior occurs in high-stakes contexts like predator evasion and mate attraction. Consequently, individuals that fail to effectively coordinate their behavior with neighbors can face severe costs. While the coordination strategies individuals in collectives follow are well-described, sensorimotor limitations frequently subvert successful execution of these strategies. Yet, how the resulting coordination errors influence the evolution of collective strategies remains relatively unexplored, largely because quantifying errors and their costs in dynamic animal groups is immensely challenging. To address this, we investigated the causes and consequences of coordination errors in tungara frog choruses. Here, neighboring males typically alternate their calls. However, due to sensorimotor limitations, inadvertent synchronous calls are common. Synchronous calls are highly stereotyped and strongly disfavored by mate-searching females and so represent unambiguous and costly coordination errors. Additionally, within synchronous call pairs, females strongly disfavor following calls relative to leading calls. We found that synchrony outcomes varied non-randomly by sensorimotor phenotype. Inter-male compatibility in intrinsic call rhythms structured synchrony, leading males with slower rhythms to synchronize at overall higher rates. Furthermore, during synchrony, males with lengthier response latencies more often produced costlier following calls. Data-driven simulations revealed that, due to these mechanistic linkages between sensorimotor phenotype and synchrony outcomes, female biases against synchronous and following calls systematically penalized males with slower call rhythms and longer response latencies. Thus, coordination errors are not unstructured noise. Rather, phenotype-dependent variation in the frequency and severity of coordination errors can generate strong directional selection on sensorimotor phenotypes in animal collectives.