Why Aye‐Ayes See Blue

Abstract

The capacity for cone-mediated color vision varies among nocturnal primates. Some species are colorblind, having lost the functionality of their short-wavelength-sensitive-1 (SWS1) opsin pigment gene. In other species, such as the aye-aye (Daubentonia madagascariensis), the SWS1 gene remains intact. Recent studies focused on aye-ayes indicate that this gene has been maintained by natural selection and that the pigment has a peak sensitivity (lambda(max)) of 406 nm, which is -20 nm closer to the ultraviolet region of the spectrum than in most primates. The functional significance behind the retention and unusual lambda(max) of this opsin pigment is unknown, and it is perplexing given that all mammals are presumed to be colorblind in the dark. Here we comment on this puzzle and discuss recent findings on the color vision intensity thresholds of terrestrial vertebrates with comparable optics to aye-ayes. We draw attention to the twilight activities of aye-ayes and report that twilight is enriched in short-wavelength (bluish) light. We also show that the intensity of twilight and full moonlight is probably sufficient to support cone-mediated color vision. We speculate that the intact SWS1 opsin pigment gene of aye-ayes is a crepuscular adaptation and we report on the blueness of potential visual targets, such as scent marks and the brilliant blue arils of Ravenala madagascariensis.

Nocturnal light environments and species ecology: implications for nocturnal color vision in forests

“…These nocturnal spectral irradiance measurements differed from those collected in non-forested regions in other geographic areas that do not show a dominant peak at 560nm for moonlit nights (Munz and McFarland, 1973;Johnsen et al, 2006;Melin et al, 2012). The dominant yellow-green spectral irradiance of nocturnal skies in Malagasy forests under both moonlit and moonless nights suggests that the surrounding green foliage in these habitats may have a significant influence on spectral irradiance.…”

“…Nocturnal color vision has been documented in frogs (Gomez et al, 2010), geckos (Roth and Kelber, 2004) and insects (Kelber et al, 2002;Somanathan et al, 2008); however, its feasibility among mammals is still hotly debated. Some researchers suggest that color discrimination at night may be a physiological reality for certain species (Perry et al, 2007;Warrant, 2008;Müller et al, 2009;Zhao et al, 2009a;Zhao et al, 2009b;Melin et al, 2012), whereas others view it as unlikely (Ahnelt and Kolb, 2000;Wang et al, 2004). Although the understory of closed canopy rainforests is likely too dim for color vision at night (particularly at smaller lunar phases and low lunar altitude), the higher nocturnal light intensities available in more open canopy habitats/microhabitats (supplementary material TableS4) may be bright enough to permit nocturnal color vision.…”

“…In contrast, research examining the relationships between nocturnal light environments, nocturnal visual morphology and behavior has been relatively limited (e.g. Osorio and Vorobyev, 2005;Johnsen et al, 2006;Melin et al, 2012). Nocturnal environments can be extremely photon-limited, exhibiting light levels that are five to nine orders of magnitude darker than daylight (Munz and McFarland, 1973;Lythgoe, 1979;Pariente, 1980).…”

Extraordinary diversity of visual opsin genes in dragonflies

“…Biochemical and molecular genetic approaches to spectral sensitivity of the respective opsin genes, and also electrophysiological and neuroethological approaches to photoreceptive characteristics of the dorsal and ventral regions of adult eyes, will be important for testing the hypothesis in future studies. In this context, it may be relevant that dorso-ventrally differentiated expression patterns of several opsin genes have been identified in compound eyes of butterflies (9,(53)(54)(55), and SW-sensitive vision has been shown to be advantageous for twilight-active animals (56)(57)(58).…”

Ferment in the family tree

“…It is a peculiar lemur that uses percussive foraging to prey on the larvae of cerambycid (longhorn) beetles. Given that beetle larvae are an improbable source of alcohol, the A294V transition of aye-ayes is very likely a spurious mutation: except that aye-ayes appear to have an enduring mutualism with the traveler's tree (Ravenala madagascariensis; Strelitziaceae) (11,12). Aye-ayes probably pollinate R. madagascariensis when they probe the large (30-cm) inflorescences for nectar ( Fig.…”