Owls (Strigiformes) represent a fascinating group of birds that are the ecological night-time counterparts to diurnal raptors (Accipitriformes). The nocturnality of owls, unusual within birds, has favored an exceptional visual system that is highly tuned for hunting at night, yet the molecular basis for this adaptation is lacking. Here, using a comparative evolutionary analysis of 120 vision genes obtained by retinal transcriptome sequencing, we found strong positive selection for low-light vision genes in owls, which contributes to their remarkable nocturnal vision. Not surprisingly, we detected gene loss of the violet/ultraviolet-sensitive opsin (SWS1) in all owls we studied, but two other color vision genes, the red-sensitive LWS and the blue-sensitive SWS2, were found to be under strong positive selection, which may be linked to the spectral tunings of these genes toward maximizing photon absorption in crepuscular conditions. We also detected the only other positively selected genes associated with motion detection in falcons and positively selected genes associated with bright-light vision and eye protection in other diurnal raptors (Accipitriformes). Our results suggest the adaptive evolution of vision genes reflect differentiated activity time and distinct hunting behaviors.

Reciprocal coevolutionary changes in predation and anti-predator behaviours have long been hypothesized, but evolutionary-scale evidence is rare. Here, we reconstructed the evolutionary-scale changes in the diel activity patterns of a predator-prey system (carnivorous and herbivorous mammals) based on a molecular phyloecological approach, providing evidence of long-term antagonistic coevolutionary changes in their diel activities. Our molecular reconstruction of diel activity patterns, which is supported by morphological evidence, consistently showed that carnivorous mammals were subjected to a shift from diurnality to nocturnality, while herbivorous mammals experienced a shift from nocturnality to diurnality during their evolutionary histories. A shift in the diel activity of the herbivores as a result of carnivore avoidance is hypothesized based on molecular, morphological and behavioural evidence, and our results suggest an evolutionary-scale arms race of diel activity shifts between carnivorous and herbivorous mammals.

Nocturnality is a key evolutionary innovation of mammals that enables mammals to occupy relatively empty nocturnal niches. Invasion of ancestral mammals into nocturnality has long been inferred from the phylogenetic relationships of crown Mammalia, which is primarily nocturnal, and crown Reptilia, which is primarily diurnal, although molecular evidence for this is lacking. Here we used phylogenetic analyses of the vision genes involved in the phototransduction pathway to predict the diel activity patterns of ancestral mammals and reptiles. Our results demonstrated that the common ancestor of the extant Mammalia was dominated by positive selection for dim-light vision, supporting the predominate nocturnality of the ancestral mammals. Further analyses showed that the nocturnality of the ancestral mammals was probably derived from the predominate diurnality of the ancestral amniotes, which featured strong positive selection for bright-light vision. Like the ancestral amniotes, the common ancestor of the extant reptiles and various taxa in Squamata, one of the main competitors of the temporal niches of the ancestral mammals, were found to be predominate diurnality as well. Despite this relatively apparent temporal niche partitioning between ancestral mammals and the relevant reptiles, our results suggested partial overlap of their temporal niches during crepuscular periods.

The diapsid lineage (birds) and synapsid lineage (mammals), share a suite of functionally similar characteristics (e.g. endothermy) that are considered to be a result of their convergent evolution, but the candidate selections leading to this convergent evolution are still under debate. Here, we used a newly developed molecular phyloecological approach to reconstruct the diel activity pattern of the common ancestors of living birds. Our results strongly suggest that they had adaptations to nocturnality during their early evolution, which is remarkably similar to that of ancestral mammals. Given their similar adaptation to nocturnality, we propose that the shared traits in birds and mammals may have partly evolved as a result of the convergent evolution of their early ancestors adapting to ecological factors (e.g. low ambient temperature) associated with nocturnality. Finally, a conceptually unifying ecological model on the evolution of endothermy in diverse organisms with an emphasis on low ambient temperature is proposed. We reason that endothermy may evolve as an adaptive strategy to enable organisms to effectively implement various life-cycle activities under relatively low-temperature environments. In particular, a habitat shift from high-temperature to relatively low-temperature environments is identified as a common factor underlying the evolution of endothermy.