Variation and heritability of retinal cone ratios in a free‐ranging population of rhesus macaques

Abstract

A defining feature of catarrhine primates is uniform trichromacy—the ability to distinguish red (long; L), green (medium; M), and blue (short; S) wavelengths of light. Although the tuning of photoreceptors is conserved, the ratio of L:M cones in the retina is variable within and between species, with human cone ratios differing from other catarrhines. Yet, the sources and structure of variation in cone ratios are poorly understood, precluding a broader understanding of color vision variability. Here, we report a large‐scale study of a pedigreed population of rhesus macaques (Macaca mulatta). We collected foveal RNA and analyzed opsin gene expression using cDNA and estimated additive genetic variance of cone ratios. The average L:M ratio and standard error was 1.03:1 ± 0.02. There was no age effect, and genetic contribution to variation was negligible. We found marginal sex effects with females having larger ratios than males. S cone ratios (0.143:1 ± 0.002) had significant genetic variance with a heritability estimate of 43% but did not differ between sexes or age groups. Our results contextualize the derived human condition of L‐cone dominance and provide new information about the heritability of cone ratios and variation in primate color vision.

The sensory ecology of primate food perception, revisited

“…In general, catarrhines have experienced strong purifying selection to maintain trichromacy and exhibit a low incidence of color vision defects 91–93 . The ratio of LWS to MWS cones in the retinas of catarrhines also seems relatively consistent, with an average of 1:1 94,95 . Humans are an exception, with high levels of genetic variation in the OPN1MW and OPN1LW genes and variable cone ratios, both leading to highly variable color vision 94,96 .…”

“…[91][92][93] The ratio of LWS to MWS cones in the retinas of catarrhines also seems relatively consistent, with an average of 1:1. 94,95 Humans are an exception, with high levels of genetic variation in the OPN1MW and OPN1LW genes and variable cone ratios, both leading to highly variable color vision. 94,96 Color vision in platyrrhines is also highly variable, however, for different reasons (Figure 3); owl monkeys (genus Aotus) have lost functionality in the OPN1SW opsin gene and cone-based color vision.…”

The biology of aging in a social world: insights from free-ranging rhesus macaques

“…Longitudinal studies will be necessary to determine whether these changes truly represent markers of aging rather than arising from population-level factors such as differential mortality (i.e., selective disappearance) (Nussey et al, 2008). Similar to humans, retinal cone gene expression in this population does not show any significant age-associated differences (Munds et al, 2022) and additional research combining cross-sectional ocular measures with transcriptomic data from the eye may provide novel insights into the genetic underpinnings of age-related eye diseases.…”

A Color Guide for Color Blind People Using Image Processing and OpenCV

“…Rachel A Munds et al [13], stated that, one characteristic that distinguishes catarrhine primates is that they have uniform trichromacy. According to Miguel Angel Martinez [14] it is widely believed that individuals with color vision deficiencies have a greater ability to detect objects that are camouflaged compared to individuals with normal color vision.…”