Color vision evolution in egg-laying mammals: insights from visual photoreceptors and daily activities of Australian echidnas
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Date
2024
Authors
Sakamoto, S.
Matsushita, Y.
Itoigawa, A.
Ezawa, T.
Fujitani, T.
Takakura, K.
Zhou, Y.
Zhang, G.
Grutzner, F.
Kawamura, S.
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Zoological Letters, 2024; 10(1):2-1-2-15
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Shiina Sakamoto, Yuka Matsushita, Akihiro Itoigawa, Takumi Ezawa, Takeshi Fujitani, Kenichiro Takakura, Yang Zhou, Guojie Zhang, Frank Grutzner, Shoji Kawamura, and Takashi Hayakawa
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Abstract
Egg-laying mammals (monotremes) are considered "primitive" due to traits such as oviparity, cloaca, and incomplete homeothermy, all of which they share with reptiles. Two groups of monotremes, the terrestrial echidna (Tachyglossidae) and semiaquatic platypus (Ornithorhynchidae), have evolved highly divergent characters since their emergence in the Cenozoic era. These evolutionary differences, notably including distinct electrosensory and chemosensory systems, result from adaptations to species-specific habitat conditions. To date, very few studies have examined the visual adaptation of echidna and platypus. In the present study, we show that echidna and platypus have different light absorption spectra in their dichromatic visual sensory systems at the molecular level. We analyzed absorption spectra of monotreme color opsins, long-wavelength sensitive opsin (LWS) and short-wavelength sensitive opsin 2 (SWS2). The wavelength of maximum absorbance (λ<sub>max</sub>) in LWS was 570.2 in short-beaked echidna (Tachyglossus aculeatus) and 560.6 nm in platypus (Ornithorhynchus anatinus); in SWS2, λ<sub>max</sub> was 451.7 and 442.6 nm, respectively. Thus, the spectral range in echidna color vision is ~ 10 nm longer overall than in platypus. Natural selection analysis showed that the molecular evolution of monotreme color opsins is generally functionally conserved, suggesting that these taxa rely on species-specific color vision. In order to understand the usage of color vision in monotremes, we made 24-h behavioral observations of captive echidnas at warm temperatures and analyzed the resultant ethograms. Echidnas showed cathemeral activity and various behavioral repertoires such as feeding, traveling, digging, and self-grooming without light/dark environment selectivity. Halting (careful) behavior is more frequent in dark conditions, which suggests that echidnas may be more dependent on vision during the day and olfaction at night. Color vision functions have contributed to dynamic adaptations and dramatic ecological changes during the ~ 60 million years of divergent monotreme evolution. The ethogram of various day and night behaviors in captive echidnas also contributes information relevant to habitat conservation and animal welfare in this iconic species, which is locally endangered.
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© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.