Coupling and decoupling of evolutionary mode between X- and Y-chromosomal red-green opsin genes in owl monkeys

Abstract

We previously discovered Y-chromosomal red-green opsin genes in two types of owl monkeys with different chromosomal characteristics. In one type, the Y-linked opsin gene is a single-copy intact gene and in the other, the genes exist as multiple pseudogenes on a Y/autosome fusion chromosome. In the present study, we first distinguished the two types of monkeys as distinct allopatric species on the basis of karyotypic characteristics: Aotus lemurinus griseimembra (Karyotype III, diploid chromosome number [2 n] = 53) and Aotus azarae boliviensis (Karyotype VI; male 2 n = 49; female 2 n = 50), belonging to the northern and southern species groups, respectively, separated by the Amazon River system. Our sequence analysis revealed a common L1-Alu-Alu insertion between the two species in the 3′-flanking region of the X-linked opsin genes. The insertion was absent in the Y-linked opsin genes and in the human red and green opsin genes, indicating that it occurred in the X copy before the split into northern and southern species and after the X to Y duplication, i.e. duplication preceded speciation. We also show that in the northern species, the Y-linked opsin gene has evolved concomitantly with the X-linked copy whereas in the southern species, the Y-autosome fusion possibly led to decoupling evolutionary processes between X- and Y-linked copies and subsequent degeneration and duplications of the Y-linked opsin gene.