Diurnality and Nocturnality in Primates: An Analysis from the Rod Photoreceptor Nuclei Perspective

Abstract

Diurnality, associated with enhanced visual acuity and color vision, is typical of most modern Primates. However, it remains a matter of debate when and how many times primates re-acquired diurnality or returned to nocturnality. We analyzed the features specific to nocturnal and diurnal vision that were recently found in the nuclei of mammalian rod photoreceptor cells in 11 species representing various groups of the Primates and related tree shrew and colugo. In particular, heterochromatin in rod nuclei of nocturnal mammals is clustered in the center of rod nuclei (inverted architecture), whereas rods of diurnal mammals retain rods with peripheral heterochromatin (conventional architecture). Rod nuclei of the nocturnal owl monkey have a state transitional to the inverted one. Surprisingly, rod nuclei of the tarsier have a conventional nuclear architecture typical for diurnal mammals, strongly implying that recent Tarsiiformes returned to nocturnality from the diurnal state. Diurnal lemurs retain inverted rod nuclei typical of nocturnal mammals, which conforms to the notion that the ancestors of all Lemuroidea were nocturnal. Data on the expression of proteins indispensable for peripheral heterochromatin maintenance (and, respectively, conventional or inverted nuclear organization) in rod cells support the view that the primate ancestors were nocturnal and transition to diurnality occurred independently in several primate and related groups: Tupaia, diurnal lemurs, and, at least partially independently, in Simiiformes (monkeys and apes) and Tarsiiformes.

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Acknowledgments

We are grateful to all colleagues who supplied us with retina samples, to Stefan Müller (LMU, Munich) for a discussion of the Aotus karyotype, and to an anonymous reviewer for very helpful comments. The study was supported by the DFG (JO903/1 to BJ, SFB/TR5 to HL and SO1054/1 to IS).

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The authors declare that they have no conflict of interest.

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Correspondence to Irina Solovei.

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Boris Joffe and Leo Peichl contributed equally.

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Joffe, B., Peichl, L., Hendrickson, A. et al. Diurnality and Nocturnality in Primates: An Analysis from the Rod Photoreceptor Nuclei Perspective. Evol Biol 41, 1–11 (2014). https://doi.org/10.1007/s11692-013-9240-9

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Keywords

  • Primates
  • Rod photoreceptor cell nuclei
  • Heterochromatin
  • Nocturnal vision
  • Diurnal vision