Can colour vision re-evolve? Variation in the X-linked opsin locus of cathemeral Azara’s owl monkeys (Aotus azarae azarae)

Abstract

BackgroundDo evolutionary specializations lead to evolutionary constraint? This appears plausible, particularly when specialization leads to loss of complex adaptations. In the owl monkey lineage, nocturnality clearly arose from a diurnal ancestor. This behavioural shift was accompanied by morphological changes in the eye and orbit and complete loss of colour vision via missense mutations in the gene encoding the short-wave sensitive visual pigment (SWS opsin). Interestingly, at least one subspecies of owl monkey, Azara’s owl monkey (Aotus azarae azarae), has regained activity in daylight. Given that all primate species that are active in daylight, including primarily diurnal species and species that are active during both day and night, have at least dichromatic colour vision, it seems reasonable to propose that dichromacy would be adaptive in A. a. azarae. With a disabled SWS opsin, the main avenue available for Azara’s owl monkeys to re-evolve colour vision is via a polymorphism in the intact X-linked opsin locus, which commonly occurs in other New World monkeys. To examine this possibility we assayed variation in the X-linked opsin of A. a. azarae, focusing on the three exons (3, 4 and 5) that control spectral sensitivity.ResultsWe found low opsin genetic variation on a population level, and no differences at the three main sites that lead to variation in spectral sensitivity in the opsins of other New World monkeys. Two rare alleles with single amino acid variants are segregating in the population, but previous functional studies indicate that these are unlikely to affect spectral sensitivity.ConclusionsGenetic constraint on the re-evolution of colour vision is likely operating in Azara’s owl monkey, which may affect the niche that this subspecies is able to occupy.

Multifactorial processes underlie parallel opsin loss in neotropical bats

“…Although variation in the complement of photoreceptors across vertebrates is usually explained by disruptions to the protein-coding sequence (e.g. Mundy et al, 2016 and Zhao et al, 2009a), findings of mismatches between genotype and phenotype also indicate a role for transcriptional and even translational control in this process. It follows that because routes of gene loss are mainly studied at the genetic level or, in fewer cases, at the transcriptomic level, the input of changes in translation and other connections between the genetic, transcriptomic, and proteomic levels may be being underestimated.…”

Platyrrhine color signals: New horizons to pursue

“…), whose routine trichromacy has evolved independently from that of catarrhines, and monochromatic owl monkeys ( Aotus sp.) may provide unique test cases that generate new insight into primates color vision evolution . Finally, we note that it is important to explicitly evaluate female–female signaling, male–male signaling, female‐to‐male signaling, and male‐to‐female signaling separately in platyrrhines, given the sex‐linked nature of color vision variation.…”

The Genetic and Evolutionary Drives behind Primate Color Vision

“…In many of these species, a SWS1 opsin pseudogene is still present in the genome (Peichl, 2005). In the primate group (Table 2), the owl monkey, and several species of lorises, galagos and tarsiers (part of the prosimian branch) have been shown to carry a SWS1 pseudogene (Jacobs et al, 1996b;Kawamura and Kubotera, 2004;Tan et al, 2005); since these species do not possess a polymorphic or duplicated LWS gene, they are considered to have monochromatic vision (Jacobs et al, , 1996bTan and Li, 1999;Levenson et al, 2007;Mundy et al, 2016).…”