Expression and Evolution of Short Wavelength Sensitive Opsins in Colugos: A Nocturnal Lineage That Informs Debate on Pri
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RESEARCH ARTICLE
Expression and Evolution of Short Wavelength Sensitive Opsins in Colugos: A Nocturnal Lineage That Informs Debate on Primate Origins Gillian L. Moritz • Norman T.-L. Lim • Maureen Neitz • Leo Peichl • Nathaniel J. Dominy
Received: 19 December 2012 / Accepted: 29 March 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com
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 Electronic supplementary material The online version of this article (doi:10.1007/s11692-013-9230-y) contains supplementary material, which is available to authorized users. G. L. Moritz (&) N. J. Dominy Department of Biological Sciences, Dartmouth College, The Class of 1978 Life Sciences Center, 78 College Street, Hanover, NH 03755, USA e-mail: [email protected] N. T.-L. Lim Department of Wildlife, Fish and Conservation Biology, University of California, One Shields Avenue, Davis, CA 95616, USA M. Neitz Department of Ophthalmology, University of Washington, Box 356485, 1959 NE Pacific Street, Seattle, WA 98195, USA L. Peichl Max Planck Institute for Brain Research, Deutschordenstrasse 46, 60528 Frankfurt am Main, Germany N. J. Dominy (&) Department of Anthropology, Dartmouth College, 6047 Silsby Hall, Hanover, NH 03755, USA e-mail: [email protected]
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. Keywords Retina Visual pigment Dermoptera Scandentia Primates
Introduction All organisms must obtain information about their physical environment and respond to changing conditions such as circadian variation in light intensity and spectral compositi
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