Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds

Abstract

29Songbirds have a species number almost equivalent to that of mammals, and are classic 30 models for studying mechanisms of speciation and sexual selection. Sex chromosomes are 31 hotspots of both processes, yet their evolutionary history in songbirds remains unclear. To 32 elucidate that, we characterize female genomes of 11 songbird species having ZW sex 33 chromosomes, with 5 genomes of bird-of-paradise species newly produced in this work. We 34 conclude that songbird sex chromosomes have undergone at least four steps of recombination 35 suppression before their species radiation, producing a gradient pattern of pairwise sequence 36 divergence termed 'evolutionary strata'. Interestingly, the latest stratum probably emerged due 37 to a songbird-specific burst of retrotransposon CR1-E1 elements at its boundary, or 38 chromosome inversion on the W chromosome. The formation of evolutionary strata has 39 reshaped the genomic architecture of both sex chromosomes. We find stepwise variations of Z-40 linked inversions, repeat and GC contents, as well as W-linked gene loss rate that are 41 associated with the age of strata. Over 30 W-linked genes have been preserved for their 42 essential functions, indicated by their higher and broader expression of orthologs in lizard than 43 those of other sex-linked genes. We also find a different degree of accelerated evolution of Z-44 linked genes vs. autosomal genes among different species, potentially reflecting their diversified 45 intensity of sexual selection. Our results uncover the dynamic evolutionary history of songbird 46 sex chromosomes, and provide novel insights into the mechanisms of recombination 47

Female-specific and dosage selections restore genes through transpositions onto the degenerated songbird W chromosomes

“…The genes involved in the such cases 149 nevertheless have probably already become pseudogenes. Our results are in line with the 150 reported cases in avian W or mammalian Y chromosomes that dosage-sensitive genes are 151 retarded for their functional degeneration due to the strong selective constraints (Bellott,et al 152 2014; Smeds, et al 2015;Bellott, et al 2017;Xu, et al 2019). We also provided new evidence 153 that sex-specific selection is shaping the evolution of the W chromosome, which was assumed 154 to be less frequent than that shaping the Y chromosome, due to the more frequent and intensive 155 male-targeted sexual selection.…”

“…Some 43 genes with important regulatory functions or high dosage-sensitivity have been demonstrated to 44 be degenerating much slower than others on the mammalian Y (Bellott, et al 2014;Cortez, et 45 al. 2014) or avian W chromosomes (Smeds, et al 2015;Bellott, et al 2017;Xu, et al 2019) due 46 to a much higher level of selective constraints. The human Y chromosome has evolved 47 palindromic sequence structures to repair deleterious mutations and facilitate gene conversions 48 between Y-linked genes (Rozen, et al 2003).…”

Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

“…And studies in fungi species Microbotryum lychnidis-dioicae 61 and Neurospora tetrasperma 62 indicated that patterns of evolutionary strata can form without sexual antagonism or chromosome inversions. We have previously reported that the youngest evolutionary stratum of songbirds has probably formed due to the lineage-specific burst of TEs 63 . In this work, we provided clear evidence that the youngest evolutionary stratum of Chilean tinamou formed without chromosome inversions between Z and W chromosomes (Figure 3).…”

Evolutionary dynamics of sex chromosomes of paleognathous birds

“…Retention of divergent Wlinked gametologs could appear consistent with incomplete dosage compensation, if the reads arising from the W-linked copy no longer map to the Z-linked copy and are thus invisible in the absence of a W assembly. However, previous work in birds suggest that only a very small fraction of Z-linked genes in the DR retain W gametologs Xu et al 2019), making this explanation unlikely to account for the bulk of expression differences between sexes in the DR.…”

“…Theoretical models predict that suppression of recombination will be favored so that the sexually antagonistic alleles that are beneficial in the heterogametic sex can be linked genetically to the sex determination locus (Rice 1987;Ellegren 2011). Recombination suppression leads to the formation of evolutionary strata, which can occur multiple times in the course of sex chromosome evolution (Lahn and Page 1999;Bergero and Charlesworth 2009;Cortez et al 2014;Zhou et al 2014;Wright et al 2016;Xu et al 2019). Despite differences in their autosomal origins and heterogamety, eutherian mammals and neognathous birds followed similar but independent trajectories of sex chromosome evolution (Graves 2015;Bellott et al 2017).…”