Abstract

Unlike all other New World (platyrrine) monkeys, both male and female howler monkeys (Alouatta sp.) are obligatory trichromats. In all other platyrrines, only females can be trichromats, while males are always dichromats, as determined by multiple behavioral, electrophysiological, and genetic studies. In addition to obligatory trichromacy, Alouatta has an unusual fovea, with substantially higher peak cone density in the foveal pit than every other diurnal anthropoid monkey (both platyrrhines and catarrhines) and great ape yet examined, including humans. In addition to documenting the general organization of the retinal ganglion cell layer in Alouatta, the distribution of cones is compared to retinal ganglion cells, to explore possible relationships between their atypical trichromacy and foveal specialization. The number and distribution of retinal ganglion cells and displaced amacrine cells were determined in six flat-mounted retinas from five Alouatta caraya. Ganglion cell density peaked at 0.5 mm between the fovea and optic nerve head, reaching 40,700–45,200 cells/mm2. Displaced amacrine cell density distribution peaked between 0.5–1.75 mm from the fovea, reaching mean values between 2,050–3,100 cells/mm2. The mean number of ganglion cells was 1,133,000±79,000 cells and the mean number of displaced amacrine cells was 537,000±61,800 cells, in retinas of mean area 641±62 mm2. Ganglion cell and displaced amacrine cell density distribution in the Alouatta retina was consistent with that observed among several species of diurnal Anthropoidea, both platyrrhines and catarrhines. The principal alteration in the Alouatta retina appears not to be in the number of any retinal cell class, but rather a marked gradient in cone density within the fovea, which could potentially support high chromatic acuity in a restricted central region.

Highlights

  • Platyrrhines (New World monkeys) differ from catarrhines (Old World monkeys, gibbons, apes, and humans) in the variety of color vision phenotypes they exhibit

  • Male Alouatta caraya were obtained from the breeding colony of the Centro Nacional de Primatas – CENP (Ananindeua, Para, Brazil)

  • Measurement of the number and types of retinal neurons and photoreceptors, their distribution, the exact conformation of the eye, and the neuron number and volume of central visual system structures has long been used as a source of information about how visual systems may be specialized for particular niches, contrasted with what features are conserved across visual systems [45,46,47,48,49,50]

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Summary

Introduction

Platyrrhines (New World monkeys) differ from catarrhines (Old World monkeys, gibbons, apes, and humans) in the variety of color vision phenotypes they exhibit. Old World monkeys and great apes, both males and females are trichromats, because in both males and females, three different genes (two in the X-chromosome and one in chromosome 7) code three different opsins. The platyrrhine retina has single-cone midget bipolar cells [16,17] and the necessary post-receptoral mechanisms for trichromacy [18,19,20] Given this common retinal architecture, and the presence of three separate opsins, both male and female Alouatta are regular trichromats and their color vision seems to be very similar to that of catarrhines [21,22]

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