Evidence that genetic drift not adaptation drives fast-Z and large-Z effects in Ficedula flycatchers

The sex chromosomes have been hypothesized to play a key role in driving
adaptation and speciation across many taxa. The reason for this is thought
to be the hemizygosity of the heteromorphic part of sex chromosomes in the
heterogametic sex, which exposes recessive mutations to natural and sexual
selection. The exposure of recessive beneficial mutations increases their
rate of fixation on the sex chromosomes, which results in a faster rate of
evolution. In addition, genetic incompatibilities between sex-linked loci
are exposed faster in the genomic background of hybrids of divergent
lineages, which makes sex chromosomes contribute disproportionately to
reproductive isolation. However, in birds, which show a Z/W sex
determination system, the role of adaptation vs. genetic drift as the
driving force of the faster differentiation of the Z chromosome (fast-Z
effect) and the disproportionate role of the Z chromosome in reproductive
isolation (large-Z effect) are still debated. Here, we address this debate
in the bird genus Ficedula flycatchers based on population-level
whole-genome sequencing data of six species. Our analysis provides
evidence for both faster lineage sorting and reduced gene flow on the Z
chromosome than the autosomes. However, these patterns appear to be driven
primarily by the increased role of genetic drift on the Z chromosome,
rather than an increased rate of adaptive evolution. Genomic scans of
selective sweeps and fixed differences in fact suggest a reduced action of
positive selection on the Z-chromosome. Nevertheless, it is possible that
the faster lineage sorting of the Z chromosome due to genetic drift may
help drive the evolution of genetic incompatibilities between species.