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Dichromatic vision in a fruit bat with diurnal proclivities: the Samoan flying fox (Pteropus samoensis)

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Abstract

A nocturnal bottleneck during mammalian evolution left a majority of species with two cone opsins, or dichromatic color vision. Primate trichromatic vision arose from the duplication and divergence of an X-linked opsin gene, and is long attributed to tandem shifts from nocturnality to diurnality and from insectivory to frugivory. Opsin gene variation and at least one duplication event exist in the order Chiroptera, suggesting that trichromatic vision could evolve under favorable ecological conditions. The natural history of the Samoan flying fox (Pteropus samoensis) meets these conditions—it is a large bat that consumes nectar and fruit and demonstrates strong diurnal proclivities. It also possesses a visual system that is strikingly similar to that of primates. To explore the potential for opsin gene duplication and divergence in this species, we sequenced the opsin genes of 11 individuals (19 X-chromosomes) from three South Pacific islands. Our results indicate the uniform presence of two opsins with predicted peak sensitivities of ca. 360 and 553 nm. This result fails to support a causal link between diurnal frugivory and trichromatic vision, although it remains plausible that the diurnal activities of P. samoensis have insufficient antiquity to favor opsin gene renovation.

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Acknowledgments

We acknowledge with gratitude the contributions of V. A. Brown, S. Kawamura, G. L. Moritz, N. P. Giannini, K. Kries, A. Miles, A. L. Russell, R. C. B. Utzurrum and M. Watsa. Funding was received from the Natural Sciences and Engineering Research Council of Canada (Postdoctoral Fellowship to ADM), the National Institutes of Health (Ruth L. Kirschstein National Research Service Award no. F32 GM064287 to NJD), and the David and Lucile Packard Foundation (Fellowship in Science and Engineering no. 2007-31754 to NJD). These procedures were approved by the Institutional Animal Care and Use Committee of the University of Tennessee, Knoxville (protocol no. 890).

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Authors and Affiliations

  1. Department of Anthropology, Dartmouth College, Hanover, NH, 03755, USA

    Amanda D. Melin, Christina F. Danosi & Nathaniel J. Dominy

  2. Department of Anthropology, Washington University in St. Louis, One Brookings Drive, St. Louis, MO, 63130, USA

    Amanda D. Melin

  3. Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

    Christina F. Danosi & Nathaniel J. Dominy

  4. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, 37996, USA

    Gary F. McCracken

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  1. Amanda D. Melin
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Correspondence to Amanda D. Melin.

Electronic supplementary material

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359_2014_951_MOESM1_ESM.pdf

Alignment of SWS gene of one Pteropus samoensis individual sequenced in the present study along with P. giganteus (GenBank accession no EU912361.1), P. pumilus [GenBank Accession no EU912362.1], and P. rodricensis [GenBank Accession no EU912363.1]. Introns and exons are labeled above their starting position. The critical tuning sites and the Schiff base counterion (Glu-113) are highlighted in red and listed with the corresponding amino acids (PDF 67 kb)

359_2014_951_MOESM2_ESM.pdf

The LWS gene of Pteropus giganteus [GenBank accession no EU912348.1] in alignment with data from the present study (representing seven individuals of P. samoensis). Introns and exons are labeled above their starting position. The critical tuning sites are highlighted in red and listed with the corresponding amino acids (PDF 85 kb)

359_2014_951_MOESM3_ESM.pdf

Partial protein sequences for the SWS opsin gene of Pteropus samoensis, aligned relative to congeners [GenBank accession nos: P. giganteus - EU912361.1, P. pumilus - EU912362.1, P. rodricensis - EU912363.1] (PDF 77 kb)

359_2014_951_MOESM4_ESM.pdf

Partial protein sequences for the LWS opsin gene of seven Pteropus samoensis individuals, aligned relative to congener P. giganteus [GenBank accession no: EU912348.1] (PDF 77 kb)

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Melin, A.D., Danosi, C.F., McCracken, G.F. et al. Dichromatic vision in a fruit bat with diurnal proclivities: the Samoan flying fox (Pteropus samoensis). J Comp Physiol A 200, 1015–1022 (2014). https://doi.org/10.1007/s00359-014-0951-x

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  • DOI: https://doi.org/10.1007/s00359-014-0951-x

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