Ancient Male Recombination Shaped Genetic Diversity of Neo-Y Chromosome inDrosophila albomicans

Abstract

Researchers studying Y chromosome evolution have drawn attention to neo-Y chromosomes in Drosophila species due to their resembling the initial stage of Y chromosome evolution. In the studies of neo-Y chromosome of Drosophila miranda, the extremely low genetic diversity observed suggested various modes of natural selection acting on the nonrecombining genome. However, alternative possibility may come from its peculiar origin from a single chromosomal fusion event with male achiasmy, which potentially caused and maintained the low genetic diversity of the neo-Y chromosome. Here, we report a real case where a neo-Y chromosome is in transition from an autosome to a typical Y chromosome. The neo-Y chromosome of Drosophila albomicans harbored a rich genetic diversity comparable to its gametologous neo-X chromosome and an autosome in the same genome. Analyzing sequence variations in 53 genes and measuring recombination rates between pairs of loci by cross experiments, we elucidated the evolutionary scenario of the neo-Y chromosome of D. albomicans having high genetic diversity without assuming selective force, i.e., it originated from a single chromosomal fusion event, experienced meiotic recombination during the initial stage of evolution and diverged from neo-X chromosome by the suppression of recombination tens or a few hundreds of thousand years ago. Consequently, the observed high genetic diversity on the neo-Y chromosome suggested a strong effect of meiotic recombination to introduce genetic variations into the newly arisen sex chromosome.

Accelerated pseudogenization on the neo-X chromosome in Drosophila miranda

“…Therefore, the X chromosome could also degenerate by the same mechanisms that cause Y degeneration, but to a lesser extent. Contrary to the above statement, however, such reduction in efficacy of natural selection may be unlikely to cause the X-chromosome degeneration in Drosophila species, because meiotic recombination is restricted to females in many Drosophila species2122. Therefore, the proportion of recombining chromosomes for the X is two-thirds, whereas the proportion for autosomes is two-fourths23.…”

Genetic Diversity on the Sex Chromosomes

“…Genetic diversity is reduced on the neo-Y chromosome in D. miranda relative to the neo-X chromosome at single nucleotide markers (Yi and Charlesworth 2000) and microsatellite loci (Bachtrog and Charlesworth 2000) relative to neo-X loci. In contrast, analyses of the genetic diversity on the neo-Y chromosome in D. albomicans did not find low Y-linked diversity (Satomura and Tamura 2016). It is possible that the results of these studies may be reconciled by considering the effects of time since total recombination suppression on the Y chromosome (the neo-Y in D. albomicans is about 0.5 Myr old [Lin et al.…”

Gene-by-gene or localized dosage compensation on the neo-X chromosome in Drosophila miranda

“…Note that meiotic male recombination also seems to have resulted in comparable levels of nucleotide diversity and a large number of shared polymorphism between the neo-X and neo-Y, which emerged independently in D. albomicans (Satomura and Tamura 2016). With our knowledge, however, male recombination in D. pseudoobscura , a closely related species of D. miranda , has not been reported in the long research history since 1930s initiated by Dobzhansky.…”