Abstract

Color vision in marsupials has recently emerged as a particularly interesting case among mammals. It appears that there are both dichromats and trichromats among closely related species. In contrast to primates, marsupials seem to have evolved a different type of trichromacy that is not linked to the X-chromosome. Based on microspectrophotometry and retinal whole-mount immunohistochemistry, four trichromatic marsupial species have been described: quokka, quenda, honey possum, and fat-tailed dunnart. It has, however, been impossible to identify the photopigment of the third cone type, and genetically, all evidence so far suggests that all marsupials are dichromatic. The tammar wallaby is the only Australian marsupial to date for which there is no evidence of a third cone type. To clarify whether the wallaby is indeed a dichromat or trichromatic like other Australian marsupials, we analyzed the number of cone types in the “dichromatic” wallaby and the “trichromatic” dunnart. Employing identical immunohistochemical protocols, we confirmed that the wallaby has only two cone types, whereas 20–25% of cones remained unlabeled by S- and LM-opsin antibodies in the dunnart retina. In addition, we found no evidence to support the hypothesis that the rod photopigment (rod opsin) is expressed in cones which would have explained the absence of a third cone opsin gene. Our study is the first comprehensive and quantitative account of color vision in Australian marsupials where we now know that an unexpected diversity of different color vision systems appears to have evolved.

Highlights

  • Eutherian mammals only retain three of the five ancestral vertebrate photopigment genes: RH1, SWS1, and M/LWS

  • The data confirmed previous reports indicating that 1) the wallaby retina contains only two cone types and 2) a considerable proportion of cones in the dunnart retina remains unlabeled by Sand LM-opsin antibodies

  • Employing immunohistochemistry and molecular biology, we found no evidence of rod opsin being expressed in dunnart cones

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Summary

Introduction

Eutherian mammals only retain three of the five ancestral vertebrate photopigment genes: RH1 (rod opsin), SWS1 (short wavelength sensitive UV-/S-cones), and M/LWS (middle-to-long wavelength sensitive LM-cones; for reviews see [1,2,3]). This basic gene arrangement suggests dichromacy in all eutherian mammals with monochromacy only occurring secondarily where expression of the S-opsin gene has ceased, e.g. in marine species Some bat species have reverted to secondary monochromacy [15], and it is still unclear whether the M/LWS gene duplication in a Megabat [13] implies trichromatic color vision

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