Diurnality and Nocturnality in Primates: An Analysis from the Rod Photoreceptor Nuclei Perspective
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.
KeywordsPrimates Rod photoreceptor cell nuclei Heterochromatin Nocturnal vision Diurnal vision
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).
Conflict of interest
The authors declare that they have no conflict of interest.
- Cone, R. A. (1972). Rotational diffusion of rhodopsin in the visual receptor membrane. Nature: New Biology, 236, 39–43.Google Scholar
- Donati, G., Santini, L., Razafindramanana, J., Boitani, L., & Borgognini-Tarli, S. (2013). (Un-)expected nocturnal activity in “Diurnal” Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation. American Journal of Physical Anthropology, 150, 99–106.PubMedCrossRefGoogle Scholar
- Finotelo, L. F., Amaral, P. J., Pieczarka, J. C., de Oliveira, E. H., Pissinati, A., Neusser, M., et al. (2010). Chromosome phylogeny of the subfamily Pitheciinae (Platyrrhini, Primates) by classic cytogenetics and chromosome painting. BMC Evolutionary Biology, 10, 189.PubMedCentralPubMedCrossRefGoogle Scholar
- Martin, R. D., & Ross, C. F. (2005). The evolutionary and ecological context of primate vision. In J. Kremers (Ed.), The primate visual system: A comparative approach (pp. 1–36). Chichester: John Wiley and Sons.Google Scholar
- Moritz, G. L., Lim, N. T.-L., Netz, M., Peichl, L., & Dominy, N. J. (2013). Expression and evolution of short wavelength sensitive opsins in colugos: A nocturnal lineage that informs debate on primate origins. Evolutionary Biology. doi: 10.1007/s11692-013-9230-y.
- Prakhongcheep, O., Hirai, Y., Hara, T., Srikulnath, K., Hirai, H., & Koga, A. (2013). Two types of alpha satellite DNA in distinct chromosomal locations in Azara’s Owl Monkey. DNA Research. doi: 10.1093/dnares/dst004.
- Tattersall, I. (2006). Origin of the Malagasy strepsirrhine primates. In L. Gould & M. L. Sauther (Eds.), Lemurs: Ecology and adaptation (pp. 3–17). New York: Springer.Google Scholar