Diurnality, nocturnality, and the evolution of primate visual systems.

Abstract

Much of the recent research on the evolution of primate visual systems has assumed that a minimum number of shifts have occurred in circadian activity patterns over the course of primate evolution. The evolutionary origins of key higher taxonomic groups have been interpreted by some researchers as a consequence of a rare shift from nocturnality to diurnality (e.g., Anthropoidea) or from diurnality to nocturnality (e.g., Tarsiidae). Interpreting the evolution of primate visual systems with an ecological approach without parsimony constraints suggests that the evolutionary transitions in activity pattern are more common than what would be allowed by parsimony models, and that such transitions are probably less important in the origin of higher level taxa. The analysis of 17 communities of primates distributed widely around the world and through geological time shows that primate communities consistently contain both nocturnal and diurnal forms, regardless of the taxonomic sources of the communities. This suggests that primates in a community will adapt their circadian pattern to fill empty diurnal or nocturnal niches. Several evolutionary transitions from one pattern to the other within narrow taxonomic groups are solidly documented, and these cases probably represent a small fraction of such transitions throughout the Cenozoic. One or more switches have been documented among platyrrhine monkeys, Malagasy prosimians, Eocene omomyids, Eocene adapoids, and early African anthropoids, with inconclusive but suggestive data within tarsiids. The interpretation of living and extinct primates as fitting into one of two diarhythmic categories is itself problematic, because many extant primates show significant behavioral activity both nocturnally and diurnally. Parsimony models routinely interpret ancestral primates to have been nocturnal, but analyses of morphological and genetic data indicate that they may have been diurnal, or that early primate radiations were likely to have generated both nocturnal and diurnal forms, especially given the unusual annual light regimes faced by Early Tertiary primates living outside today's latitudinal tropics. We review the essential morphology and physiology of the primate visual system to look for features that might constrain evolutionary switches, and we find that the pattern of variation within and among primate groups in eye size, corneal size, retinal morphology, and opsin distribution are all consistent with the idea that there is considerable evolutionary flexibility in the visual system. These results suggest that primate lineages may evolve from diurnal to nocturnal, and vice versa, more readily and more rapidly than has been suggested by the use of strict parsimony models. This has implications for interpreting the fossil record and reconstructing key evolutionary events in primate evolution.