Considering the Influence of Nonadaptive Evolution on Primate Color Vision

Abstract

Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; NX chromosomes = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.

Novel opsin gene variation in large-bodied, diurnal lemurs

“…Yet other day-active lemurs appear to have a single opsin allele and are strictly dichromatic [9][10][11]. There is some behavioural evidence linking differences in opsin gene variation to differences in colour vision phenotypes among lemurs [8,12], and it has been suggested that this variation might be influenced by ecological differences, including the degree of diurnal behaviour [10].…”

“…There is some behavioural evidence linking differences in opsin gene variation to differences in colour vision phenotypes among lemurs [8,12], and it has been suggested that this variation might be influenced by ecological differences, including the degree of diurnal behaviour [10]. This hypothesis has been difficult to evaluate, however, because X-linked opsin data are only available for a few lemur taxa [6][7][8][9][10][11]. To help fill this gap, we provide the first comprehensive examination of X-linked opsin variation across members of the lemur family Indriidae.…”

The Genetic and Evolutionary Drives behind Primate Color Vision

“…Although polymorphism has been reported in just four species, it is possible that this may be an underestimate of the number of trichromatic prosimian species since many of the studies have been restricted to small cohorts of animals. However, a recent study using a large sample group of the red-bellied lemurs (Eulemur rubriventer) showed that this species has a 100% frequency of the L allele with Thr at site 285, probably due to a genetic bottle neck event in the studied population (Jacobs and Bradley, 2016). Indeed this same group later demonstrated that amongst lemur species, the presence of M or L pigments is highly variable .…”

“…However, it is important to notice that, in many cases, different combinations of residues across the three sites ( (Jacobs and Deegan, 2003a). In the other two families that form the New World monkey parvorder, Data taken from Mollon et al (1984), Travis et al (1988), Boissinot et al (1998), Tan and Li (1999), Jacobs and Deegan (2001, 2003a,b, 2005, Saito et al (2004), Talebi et al (2006), Veilleux and Bolnick (2009), Bunce et al (2011), Corso et al (2016, and Jacobs and Bradley (2016).…”

Group benefit associated with polymorphic trichromacy in a Malagasy primate (Propithecus verreauxi)

“…Very little work has examined the ecology of color vision in trichromat or potentially trichromat lemur populations343536. Although trichromacy among lemurs may be functionally different from trichromacy in platyrrhines due to lower retinal cone density37 and lower visual acuity3839, experimental evidence suggests that trichromacy can influence lemur foraging behavior40.…”