Evolutionary analysis of the female-specific avian W chromosome

Abstract

The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear-cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.

Figure 1. Male-to-female expression ratios (log₂) for genes on the collared flycatcher sex chromosomes.

Box plots of mean values over seven different tissues are shown. Left, genes from the Z chromosome without a W-linked copy (n=600; ref. 22); middle, genes from the small (630 kb) pseudoautosomal region (PAR; n=20; ref. 21); right, gametologous gene pairs (n=44). Boxes show distribution quartiles with the median in bold. Whiskers show minimum and maximum of the distribution unless this is more than 1.5 times the interquartile distance. Outliers exceed this limit.

Figure 2. Examples of phylogenetic trees of gametologous gene pairs demonstrating the presence of at least two evolutionary strata on the flycatcher Z chromosome.

(a) CHD1, (b) GNAQ, (c) VCP and (d) ZNF131. a and b are genes where Z-W recombination ceased prior to the split of flycatcher and chicken lineages, meaning that genes cluster by gametologs. (c) and (d) are genes where Z–W recombination ceased subsequent to the split of flycatcher and chicken lineages, meaning that genes cluster by species. a and d are examples of genes where chickens lacks a known W-linked gametolog. Species codes: Sca, Struthio camelus (ostrich); Gga, Gallus gallus (chicken); Tgu Taeniopygia guttata (zebra finch); Fal, Ficedula albicollis (collared flycatcher).

Figure 3. Population genomics of NRW sequences.

(a) Pairwise nucleotide diversity (π) for different Ficedula species, showing drastically reduced levels of diversity on the NRW. (b) Degree of genetic differentiation (F_st) between different Ficedula populations (within collared flycatcher and pied flycatcher, respectively) and species (collared flycatcher versus each of the three other black-and-white flycatcher species and the outgroup species red-breasted flycatcher). Colour codes: red, NRW; yellow, Z chromosome; blue, autosomes.

Figure 4. Phylogenetic relationships among flycatcher NRW haplotypes.

(a) Monophyletic clustering of NRW haplotypes of each flycatcher species (left) but not of a 10 kb autosomal region (right). (b) Maximum likelihood trees representing the NRW (left) and mtDNA (right) gene genealogies of 10 Spanish pied flycatchers. Bootstrap percentages for maximum likelihood trees (100 replicates) are shown above branches. Colour codes: pied flycatcher, turquoise; Atlas flycatcher blue; collared flycatcher, red; semi-collared flycatcher, orange.