Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Brigitte Müller,Josef Ammermüller,Leo Peichl,Cornelia Hagemann,Gabriel C. Knop,Martin Glösmann,Walter S. Leal

doi:10.1371/journal.pone.0006390

Abstract

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.

Highlights

IntroductionCone photoreceptors are used for daylight vision, and most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima in the short-wavelength (blue or ultraviolet light) and long-wavelength (green or red light) ranges and provide the basis for dichromatic colour discrimination [1,2]
Cone photoreceptors are used for daylight vision, and most mammals possess two cone populations with two visual pigments that have absorption maxima in the short-wavelength and long-wavelength ranges and provide the basis for dichromatic colour discrimination [1,2]
The two cone pigments provide the basis for spectral contrast detection and perhaps true dichromatic colour vision

Summary

Introduction

Cone photoreceptors are used for daylight vision, and most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima in the short-wavelength (blue or ultraviolet light) and long-wavelength (green or red light) ranges and provide the basis for dichromatic colour discrimination [1,2]. A behavioural study of the flower bat Glossophaga soricina in dark-adapted conditions found no evidence for colour discrimination, but did detect UV sensitivity and concluded that this was a property of the b-band of the rod opsin, and that G. soricina lacked a separate shortwave-sensitive cone photoreceptor [11]. The only published electrophysiological study on spectral sensitivity of bat photoreceptors examined four microchiropteran species, including Carollia perspicillata; that study postulated the existence of two visual pigments: a rod opsin (lmax 500 nm) and a second pigment absorbing at about 560–580 nm [12]. A UV-sensitive pigment was not addressed in that study because stimuli were limited to wavelengths .440 nm

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