Liminal Light and Primate Evolution

Abstract

The adaptive origins of primates and anthropoid primates are topics of enduring interest to biological anthropologists. A convention in these discussions is to treat the light environment as binary—night is dark, day is light—and to impute corresponding selective pressure on the visual systems and behaviors of primates. In consequence, debate has tended to focus on whether a given trait can be interpreted as evidence of nocturnal or diurnal behavior in the primate fossil record. Such classification elides the variability in light, or the ways that primates internalize light in their environments. Here, we explore the liminality of light by focusing on what it is, its many sources, and its flux under natural conditions. We conclude by focusing on the intensity and spectral properties of twilight, and we review the mounting evidence of its importance as a cue that determines the onset or offset of primate activities as well as the entrainment of circadian rhythms. Expected final online publication date for the Annual Review of Anthropology, Volume 49 is October 21, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The sensory ecology of primate food perception, revisited

“…At night, the color of light in forests tends to resemble “forest shade,” regardless of lunar phase or canopy openness 112 . Illustration by William Scavone, and reproduced from Dominy and Melin 113 …”

“…In contrast, the loss of SWS cones and functional color vision in many nocturnal exudate feeders (e.g., Phaner, Allocebus , Galago ) is hypothesized to be associated with a greater emphasis on luminance rather than chromatic cues, 87,144,145 as luminance contrast can be more useful in identifying gum resources, which often stain darkly against tree bark 145 . A linked and important advancement of the past two decades has been the recognition that “diurnal” and “nocturnal” light environments, and especially their transitional phases (e.g., twilight) are variable, dynamic, and influenced by habitat types, lunar cycles, and anthropogenic disturbance 112–114,146 . Data from behavioral study of foraging in dichromatic marmosets ( Callithrix jacchus ) indicates complex impacts of light levels on color perception due to input from rods under mesopic conditions 147 ; such phenomena remain poorly understood.…”

“…Data from behavioral study of foraging in dichromatic marmosets ( Callithrix jacchus ) indicates complex impacts of light levels on color perception due to input from rods under mesopic conditions 147 ; such phenomena remain poorly understood. Overall, mesopic and liminal light environments likely had a profound and underappreciated impact on early primate sensory evolution and ecology, and are still important to many species 113,140 …”

“…Others have extended this concept to other senses, speaking of primate lightscapes and how they affect susceptibility to predation, 113 or aeroscapes, the study of air movement and olfactory‐guided foraging (termed anemotaxis). Moving forward, it is tempting to envision discussions of primate odor‐scapes and taste‐scapes––after all, we know already that fruit sugar content can vary spatially, even within a tree crown 242 .…”

Origins and evolution of biological novelty

“…For instance, the transition from dichromatic to trichromatic vision (i.e., colour vision mediated by three receptors) in old world monkeys and apes was made possible by the the duplication of a single green opsin gene followed by neofunctionalization (resulting in a red sensitive opsin) (Hunt et al 1998;Dulai et al 1999). This novel sensory trait is likely advantageous for detecting fruit among green foliage, and may have contributed to subsequent speciation and the transition to novel diets and habitats (Dominy and Lucas 2001;Carvalho et al 2017;Dominy and Melin 2020). Certain selective environments in combination with genomic context (e.g., rounds of genome duplication in fishes) may also precipitate an explosion of opsin duplicates.…”