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Vision in dim light and the evolution of color pattern in a crepuscular/nocturnal frog

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Abstract

Some crepuscular and nocturnal animals are brightly marked yet the adaptive significance of their colorful patterns in low light, as found at twilight and night, is poorly understood. This phenomenon is particular prevalent in amphibians. Of the nearly 80% of nocturnal frogs, many exhibit color patterns with red, yellow, green and blue hues and/or contrasting spots and stripes. Despite the prevalence of these conspicuous visual signals in frogs, the function and adaptive significance of bright coloration for crepuscular/nocturnal frogs is still poorly understood. A critical first step in linking color pattern evolution with premating reproductive isolation and lineage divergence is determining whether color pattern plays a role in mate recognition in dim light. We studied the brightly colored Red-eyed Treefrog (Agalychnis callidryas), a crepuscular/nocturnal Neotropical treefrog that exhibits noteworthy geographic variation in color pattern and female choice for local male phenotypes. We measured retinal photoreceptor cell absorbance via microspectrophotometry and used visual modeling to assess whether distinct color pattern phenotypes were distinguishable as luminosity and chromaticity cues. We found that the Red-eyed Treefrog visual system is capable of discriminating differences in color patterns as brightness (luminosity) in their perception of nighttime visual cues. Differences in color (chromaticity) were also detectable in dim light, although less prominent than brightness. Combined, our data indicate that differences in these visual traits are discernable, can function for species and population recognition, and evolve through sexual selection. These social signals are thus analogous to the widespread visual displays exhibited by diurnal vertebrates, suggesting that the richness of similar sensory interactions among animals at twilight and after dark might be severely underappreciated. More generally, we demonstrate that combining studies of the visual system with population genetics, behavior, and natural history provides a framework for testing the evolution and adaptive function of color pattern.

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Data availability

MSP data available at Dryad. https://doi.org/10.5061/dryad.kkwh70s5n

Code availability

Code for pavo analyses, and moonlight illuminant data available at Dryad.https://doi.org/10.5061/dryad.kkwh70s5n R

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Acknowledgements

We thank A Vega for field assistance and valuable contributions to the system; RE Espinoza, WC Funk, HW Greene, L Harmon, KI Hoke, KR Lips, E Losos, EB Rosenblum, and KR Zamudio for discussion and constructive feedback on the manuscript; and T White for advice on running analyses in pavo. This work was supported by grants from the Organization for Tropical Studies, Smithsonian Tropical Research Institute, Tinker Foundation, Einaudi Center, Department of Ecology and Evolutionary Biology at Cornell University, and NSF (Doctoral Dissertation Enhancement Grant, DEB-0506043) to JMR. We thank the Ministry of the Environment and Energy in Costa Rica (MINAE—permit no.067-2003-FAU) for permission to conduct research and export samples. Two anonymous reviewers provided helpful suggestions that improved this manuscript.

Funding

Organization for Tropical Studies, Smithsonian Tropical Research Institute, Tinker Foundation, Einaudi Center, Department of Ecology and Evolutionary Biology at Cornell University, National Science Foundation Doctoral Dissertation Enhancement Grant, DEB-0506043.

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Correspondence to Jeanne M. Robertson.

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All methods were approved by the IACUC at Cornell University, protocols 2017–0043 (Loew) and 2003–0049 (Robertson). IACUC reviews and approves research in compliance with federal laws, regulations, and policies.

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Robertson, J.M., Bell, R.C. & Loew, E.R. Vision in dim light and the evolution of color pattern in a crepuscular/nocturnal frog. Evol Ecol 36, 355–371 (2022). https://doi.org/10.1007/s10682-022-10173-w

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  • DOI: https://doi.org/10.1007/s10682-022-10173-w

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