Expression and Evolution of Short Wavelength Sensitive Opsins in Colugos: A Nocturnal Lineage That Informs Debate on Primate Origins.

Gillian L Moritz,Maureen Neitz,Norman T-L Lim,Nathaniel J Dominy,Leo Peichl

doi:10.1007/s11692-013-9230-y

Abstract

A nocturnal activity pattern is central to almost all hypotheses on the adaptive origins of primates. This enduring view has been challenged in recent years on the basis of variation in the opsin genes of nocturnal primates. A correspondence between the opsin genes and activity patterns of species in Euarchonta—the superordinal group that includes the orders Primates, Dermoptera (colugos), and Scandentia (treeshrews)—could prove instructive, yet the basic biology of the dermopteran visual system is practically unknown. Here we show that the eye of the Sunda colugo (Galeopterus variegatus) lacks a tapetum lucidum and has an avascular retina, and we report on the expression and spectral sensitivity of cone photopigments. We found that Sunda colugos have intact short wavelength sensitive (S-) and long wavelength sensitive (L-) opsin genes, and that both opsins are expressed in cone photoreceptors of the retina. The inferred peak spectral sensitivities are 451 and 562 nm, respectively. In line with adaptation to nocturnal vision, cone densities are low. Surprisingly, a majority of S-cones coexpress some L-opsin. We also show that the ratio of rates of nonsynonymous to synonymous substitutions of exon 1 of the S-opsin gene is indicative of purifying selection. Taken together, our results suggest that natural selection has favored a functional S-opsin in a nocturnal lineage for at least 45 million years. Accordingly, a nocturnal activity pattern remains the most likely ancestral character state of euprimates.Electronic supplementary materialThe online version of this article (doi:10.1007/s11692-013-9230-y) contains supplementary material, which is available to authorized users.

Highlights

All organisms must obtain information about their physical environment and respond to changing conditions such as circadian variation in light intensity and spectral composition
We show that the eye of the Sunda colugo (Galeopterus variegatus) lacks a tapetum lucidum and has an avascular retina, and we report on the Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users
We found that Sunda colugos have intact short wavelength sensitive (S-) and long wavelength sensitive (L-) opsin genes, and that both opsins are expressed in cone photoreceptors of the retina

Summary

Introduction

All organisms must obtain information about their physical environment and respond to changing conditions such as circadian variation in light intensity and spectral composition. It has been tempting to link the L-cone monochromacy of these species with dark (scotopic) light environments, and to assume that relaxation of natural selection is the cause of disabling mutations on the S-opsin gene This hypothesis is weakened in part by variation among closely related species with similar scotopic behaviors; for instance, the Syrian golden hamster, Mesocricetus auratus, is an L-cone monochromat, whereas the Siberian dwarf hamster, Phodopus sungorus, has both opsins intact (Calderone and Jacobs 1999). The S-opsin gene has been lost in some lineages, while both cone opsin genes have been maintained over many millions of years in others (Wang et al 2004; Muller and Peichl 2005; Muller et al 2007, 2009; Zhao et al 2009a, b) This latter finding suggests that dichromatic vision is advantageous for some nocturnal species; the functional and adaptive significance of such vision is uncertain. A similar pattern has been reported among nocturnal primates and it has had the effect of fueling debate focused on primate origins

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