A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

Abstract

X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show extensive sequence differentiation, but not degeneration of the Y chromosomes. A new method based on gene trees shows both chromosomes are sex‐linked. Furthermore, the gene trees from the two Y chromosomes have identical topologies, showing they have been coinherited since the reciprocal translocation occurred. Reciprocal translocations can thus reshape sex linkage on a much greater scale compared with inversions, the type of rearrangement that is much better known in sex chromosome evolution, and they can greatly amplify the power of sexually antagonistic selection to drive genomic rearrangement. Two more populations show evidence of other rearrangements, suggesting that this species has unprecedented structural polymorphism in its sex chromosomes.

Causes and consequences of reciprocal translocations on sex chromosomes

“…The translocation breakpoint links the segregation of the two Y chromosomes and is therefore the centre of differentiation on the new Y chromosome that does not carry the SDR. On chromosomes 1 and 2 in the Ammarnäs population of R. temporaria , Toups et al () observe patterns of male‐female F ST that are consistent with these predictions.…”

“…The genomic data presented by Toups et al () support the presence of a reciprocal translocation between the ancestral sex chromosome (chromosome 1) and an autosome (chromosome 2) in an R. temporaria population in Ammarnäs, Sweden. Gene trees on both chromosomes have Y chromosome clades that are found only in males and have topologies that are consistent with one another, indicating co‐inheritance.…”

“…By increasing linkage and strengthening these associations, a reciprocal translocation can spread (Charlesworth, ). Although there are no direct data on sexually antagonistic selection in R. temporaria , Toups et al () measure expression in males and females. They find that chromosome 2, which became linked to the SDR in the Ammarnäs population, is also enriched for genes with female‐biased expression in a different population of R. temporaria where chromosome 2 is autosomal.…”

“…In the Ammarnäs R. temporaria population, both Y chromosomes should degenerate because recombination rates with both X chromosomes are low in males. However, Toups et al () find that loci on both Y chromosomes have expression levels, dN/dS ratios (nonsynonymous to synonymous substitutions) and numbers of large deletions that are comparable to those of the autosomes. One explanation is that the recombination rate in males is not low enough to cause detectable degeneration.…”

“…With the adoption of new sequencing technologies and methodologies (Tattini, D'Aurizio, & Magi, ), structural variants are likely to be identified with increasing frequency and confidence in nonmodel organisms. Toups et al () present the first genomic analysis of the uniquely extensive structural variation on sex chromosomes in R. temporaria . They find that new sex‐linked regions become differentiated but do not find evidence of neo‐Y chromosome degeneration.…”