Long-range linkage maintained male-specific loci on a young Y chromosome prior to recombination shutdown

Suppression of recombination on the Y chromosome maintains linkage between male-specific loci and is commonly established by inversions. Here, we describe a young, inversion-free Y chromosome (neo-Y) in Drosophila albomicans with a unique history and paradoxical signature of exchange. Prior to recombination shutdown in males, it repeatedly recombined with the X-linked counterpart (neo-X) but at the same time preserved complete long-range linkage of the chromosome ends. By assembling multiple neo-Ys chromosomes and QTL-mapping, we show that double crossovers maintained linkage between the male-sex determining region at one end to sexually antagonistic alleles and a locus essential for spermatogenesis at the other. We argue that such long-range linkage of distal sex-specific loci disfavors inversions but instead encourages the emergence of achiasmy.