Asymmetric Costs of Coordination Errors Generate Selection on Social and Sensorimotor Phenotypes in an Animal Collective

Abstract

Animal collectives are dynamic social environments where individuals must continually coordinate their behavior with neighbors. Sensorimotor limitations like processing delays make coordination errors inevitable and, in high-stakes contexts like collective predator evasion and courtship, errors can be extremely costly. Identifying errors and quantifying their costs are challenging in flocks and schools, so collective behavior models traditionally treat errors as random noise. However, if instead the rate and severity of costly errors within collectives are biased towards certain phenotypes, selection against error-prone phenotypes is a neglected feature of the selective landscape. We tested this in experimental choruses of a call-alternating frog (tungara frogs, Physalaemus [=Engystomops] pustulosus). Here inadvertent synchronous calls represent discrete coordination errors attributable to sensorimotor limitations rather than strategy, and they carry steep attractiveness costs; mate-searching females disfavor synchronous calls, especially the following calls of synchronous call pairs. Synchronous calls were frequent, and synchrony outcomes varied non-randomly by social and sensorimotor phenotypes. Inter-male compatibility in intrinsic call rhythms structured synchrony, causing males with slower rhythms to synchronize at higher rates. Furthermore, during synchrony, males with longer response latencies more often produced costlier following calls. Bayesian simulations combining interaction data with experimentally derived female preference estimates revealed that these mechanistic linkages between male phenotypes and synchrony outcomes generated systematic female biases against males with slower call rhythms and longer response latencies. Thus, coordination errors are not unstructured noise. Rather, phenotype-dependent variation in the frequency and/or severity of errors can generate directional selection on social phenotypes and their sensorimotor underpinnings in animal collectives.