Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species

Abstract

In geographic areas where pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breed in sympatry, hybridization occurs, leading to gene flow (introgression) between the two recently diverged species. Notably, while such introgression is observable at autosomal loci it is apparently absent at the Z chromosome, suggesting an important role for genes on the Z chromosome in creating reproductive isolation during speciation. To further understand the role of Z-linked loci in the formation of new species, we studied genetic variation of the two species from regions where they live in allopatry. We analyzed patterns of polymorphism and divergence in introns from 9 Z-linked and 23 autosomal genes in pied and collared flycatcher males. Average variation on the Z chromosome is greatly reduced compared to neutral expectations based on autosomal diversity in both species. We also observe significant heterogeneity between patterns of polymorphism and divergence at Z-linked loci and a relative absence of polymorphisms that are shared by the two species on the Z chromosome compared to the autosomes. We suggest that these observations may indicate the action of recurrent selective sweeps on the Z chromosome during the evolution of the two species, which may be caused by sexual selection acting on Z-linked genes. Alternatively, reduced variation on the Z chromosome could result from substantially higher levels of introgression at autosomal than at Z-linked loci or from a complex demographic history, such as a population bottleneck.

Figure 1.

Descriptive statistics of polymorphism and divergence in collared and pied flycatchers at 9 Z-linked loci (9657 bp) and 23 autosomal loci (11539 bp). For both classes of loci the observed number of segregating sites divided by the total length of loci is displayed. The number of polymorphisms segregating in each species is shown alongside the number of shared polymorphisms and the number of fixed differences between species (per base pair).

Figure 2.

Haplotype variation illustrated by neighbor-joining trees using p-distances of individual alleles at each of the nine Z-linked genes.