Unexpected Conservation of the X-Linked Color Vision Gene in Nocturnal Prosimians: Evidence from Two Bush Babies

Bush babies have had a long history of nocturnal life and it would be interesting to know whether their color vision genes have become degenerate. Therefore, we used PCR techniques to sequence the X-linked pigment gene of two of these nocturnal prosimians: Galago senegalensis and Otolemur garnettii. Southern hybridization of genomic DNA of G. senegalensis showed a single X-linked pigment gene. Interestingly, the deduced pigment sequences of the two bush babies are identical. By comparing the X-linked pigments of bush baby, human, squirrel monkey, and marmoset, 38 variable positions were identified. At those positions that may cause a spectral shift, the bush baby pigment has identical or biochemically similar residues to those of the marmoset cone pigment with a spectral peak of 543 nm. This result is consistent with the estimate of 544–545 nm for the spectral peak of the X-linked pigment of Otolemur crassicaudatus, which is closely related to Otolemur garnettii. The neighbor-joining tree of mammalian X-linked pigments showed a significantly shorter branch in the bush baby lineage than in other primate lineages. A relative rate test showed that the nonsynonymous substitution rate of the bush baby X-linked pigment gene is about three times slower than that of the human red pigment gene, though the synonymous substitution rates of the two genes are similar. The slower nonsynonymous rate in the bush baby lineage suggests that the bush baby X-linked pigment gene is under functional constraints, in spite of its nocturnal life. Two radical changes at positions in the intradiskal surface next to the sixth transmembrane domain were observed in the X-linked cone pigment of bush babies but not in other primates. They are changes from Ala to Ser and from Asn to His, which are similar in function to the corresponding residues in rhodopsins. These two changes may be of importance for dim light sensitivity, which is consistent with our proposal that the evolution of the bush baby X-linked pigment gene is under selective pressure. In addition, the 2.5% divergence in introns 2 and 5 of the X-linked pigment gene between the two bush babies supports their classification into two separate genera.