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Learn More. Sex-specific chromosomes, like the W of most female birds and the Y of male mammals, usually have lost most genes owing to a lack of recombination. We analyze newly available genomes of 17 bird species representing the avian phylogenetic range, and find that more than half of them do not have as fully degenerated W chromosomes as that of chicken. W-linked genes are subject to ongoing functional decay after recombination was suppressed, and the tempo of degeneration slows down in older strata.
Overall, we unveil a complex history of avian sex chromosome evolution. In many species with separate sexes, sex is determined by a pair of heteromorphic sex chromosomes that differ in their size, morphology, and gene content. Mammals have male heterogametic sex chromosomes XX in female, XY in malewhereas birds have female heterogametic sex chromosomes ZW in female and ZZ in male 1. Both sex systems have originated independently from different ancestral autosomes after the two lineages diverged more than million years ago Ma 1 — 4yet they share many common features with respect to their genomic composition and evolutionary history.
Recombination suppression is thought to follow the origination of a sex-determining locus and may initially encompass only a small chromosomal segment surrounding that locus, but then progressively spre along Y or W chromosomes, possibly owing to the accumulation of sexually antagonistic alleles at PARs that benefit one sex but harm the other 8.
Each stratum is characterized by a distinct range of levels of sequence homology between the remaining XY or ZW gene pairs, reflecting the punctuated evolutionary time points when recombination between the sex chromosomes ceased 9 No complete avian chrW has been sequenced, but partial annotation of W-linked genes in chicken Gallus gallus 15 implied that there are at least three strata 1016and some may have formed independently in different avian lineages 17 — A recent investigation of the karyotype of avian species revealed great variation in the size and morphology of chrW, sometimes even between closely related species 21suggesting a dynamic evolutionary history of bird sex chromosomes.
Living birds consist of two sister lineages, the Palaeognathae flightless ratites and Tinamous and the Neognathae, which themselves consist of two major lineages, the Galloanserae land and water fowls and the Neoaves all other neognaths.
Karyotyping suggests that most ratite paleognaths, like ostrich Struthio camelus and emu Dromaius novaehollandiaehave homomorphic sex chromosomes with extensive recombining and euchromatic PARs that resemble the ancestral state 24 — In contrast, their sister group Tinamous shows interspecific variation in sizes and locations of PARs Whether all Neognathae species have an almost completely degenerated chrW similar to that of chicken 28 is unknown. Here, we analyzed female genomes of 17 bird species newly generated by the Avian Genomics Consortium that span the avian taxonomic diversity 2329in order to unveil the broad evolutionary history of bird ZW chromosomes.
For three species—chicken, emu, and crested ibis—we analyzed sequence data of both sexes 31 — We additionally improved the ostrich draft genome to a chromosome assembly with optical mapping 34 N Comparative cytogenetic mapping and genome sequence analysis show that there are very few interchromosomal rearrangements among bird species 35 — 38 ; thus, we anchored genome scaffold sequences of the remaining species using the ostrich Z chromosome chrZ for all Palaeognathae and chicken Z for all Neognathae 3.
We present evolutionary strata patterns of investigated bird species with partially degenerated chrW, except for chicken and chimney swift as comparison, together with their revised phylogeny A full pattern for all the investigated species is presented in fig. S2 and summarized in fig. Note that different species may not share the same S1, S2, and S3; and part of S0 25 to 35 Mb in the figure has been reshuffled because of chromosome inversions that occurred in the ancestor of Neognathae Fig. The blank region around 75 to 85 Mb corresponds to a chicken-specific amplification of testis gene clusters 3 table S7.
We also labeled genes ly used for cytological mapping 26 and the reported S0 gene KCMF1 4 traced through the phylogeny with blue dotted linesas well as the putative male sex-determining gene DMRT1 traced with the dotted red line Mapped is the evolutionary strata gene synteny between sequenced reptile boa and lizard and avian species. Each line connects a pair of orthologous genes between species, and different colors of lines represent different strata of genes: S0 grayostrich S1 yellowNeognathae S1 brownNeoaves S2 orangeDMRT1 red.
Genomic regions encompassing S0 and S1 have experienced multiple inversions across different species, relocating DMRT1 to the middle of the Z chromosome after the divergence between Neognathae and Palaeognathae. In contrast, genomic regions within Neoaves S2 and S3 show high level of syntenic conservation across species. To distinguish between the recombining PAR that has nearly identical sequences between chrZ and chrW and the region lacking recombination that has become differentiated between chrZ and chrW along the sex chromosome, we developed an approach that involves examination of read sequencing depth along chrZ Although most sequences in the female-specific W-linked region may have lost almost all homology with chrZ, some ZW homolog pairs often called gametologs may remain.
However, W-linked regions are probably too divergent to allow short sequencing re derived from them [ base pairs bp long in this study] to align with their Z homologs, especially if they are from more ancient strata. Consequently, PARs will show a level of read depth similar to that of autosomes, whereas differentiated regions will have only half the mapped read coverage depth in females Fig.
Based on this principle, we find evidence of extreme differences in the length of the PAR versus differentiated region on sex chromosomes across species Fig. The putative avian male sex-determining gene DMRT1 39 always resides in the differentiated region in all species, consistent with it being the initial seed for progressive recombination suppression Fig.
However, the size of the PAR varies substantially among species Table 1. We confirm that we have identified the true PAR in ostrich, as we find that eight genes that have been cytologically mapped to both chrZ and chrW 26 are appropriately distributed along our assembled ostrich chrZ Fig. Whereas most Neognathae have restricted recombination between their sex chromosomes into only a very short terminal PAR Fig.
This also indicates that recombination suppression in the genomic segment adjacent to the PAR has evolved independently in at least some bird lineages see below. If these W-segments are only differentiated to a moderate degree, they may have retained sufficient sequence homology to map to the differentiated region along chrZ. We identify abundant W-linked sequences from all three Palaeognathae species, one of the two Galloanserae species and in five of the Neoaves Table 1 and table S3and many fewer candidate W-derived fragments homologous to chrZs in chicken and the remaining Neoaves species Fig.
Comparison of read depths between the two sexes in chicken, crested ibis, and emu verified that the candidate W-linked scaffolds are specific to females figs. S3 and S4. Additionally, most of the candidate W-linked scaffolds of chicken exclusively align to W-linked or unmapped chrUn fragments of the reference chicken genome derived from Sanger sequencing fig. These together confirmed that we have identified truly W-linked scaffolds.
We further annotated genes in these W-derived scaffolds, ranging from 24 in the Pekin duck to 55 in ostrich and in the white-throated tinamou Table 1 and table S4compared to 26 and 14 W-linked genes ly annotated through transcriptome sequencing in chicken and ostrich, respectively figs. S6 and 7 and table S5 15 Some W-linked genes may be missing or fragmented table S5if they are highly enriched for transposable elements or too similar to their Z-linked homologs in sequence. This indicates that, although our current chrW genome assemblies are interrupted by highly repetitive noncoding regions, they contain substantial amounts of coding regions of genes.
Overall, we find that avian chrWs show great variation in their degree of degeneration, and more than one-third of the sampled Neognathae species harbor chrWs that are not as fully degenerated as that of chicken fig. The identified W-linked fragments are stratified by differences in their occurrences and alignment identities along chrZ figs.
S9 and S10exhibiting patterns of evolutionary strata. This provides evidence that, similar to those of mammals 4avian sex chromosomes suppressed recombination through a series of punctuated events 1016 The strata present a gradient of ages, reflected by higher levels of sequence homology between chrW and chrZ sequences as one moves toward the PAR Fig. S9 to S The putative male sex-determining gene of birds, DMRT1 39is located within the first stratum we denote this region as stratum S0 that evolved in the ancestor of all extant birds, around 98 to Ma The boundaries of S0 can still be clearly traced by the nearby stratum in ostrich and emu Fig.
Shown are Venn diagrams of overlapping gene content between orthologous strata of different Palaeognathae A to C and Neognathae D to F species. To the right of each diagram is a maximum-likelihood tree for a specific example gene constructed from Z- and W-linked gametologs of that stratum.
S12, S14, S16, and S The tree is constructed with ostrich or green anole lizard as outgroup, with bootstraps. Maximum-likelihood trees constructed with multiple S0 genes including KCMF1 show that Z-linked gametologs of Palaeognathae and Neognathae cluster with each other by species rather than with their W-linked gametologs fig.
S12confirming that recombination between chrZ and chrW at S0 was abolished in the common ancestor of all birds 17 Fig. Consistent with their postulated ancient origin, almost no W-linked genes were identified within the orthologous region of S0 in all the studied species Table 1the exception being emu, whose W-linked S0 region has not completely degenerated 23 All residual W-linked fragments within emu S0 show similar levels of divergence from their homologous chrZ sequences fig.
S9suggesting that they stopped recombining at the same time. Adjacent to the S0 stratum, we identified one additional stratum S1 in ostrich and emu, and at least two strata S1 and S2 in the white-throated tinamou.
This indicates that these younger strata formed independently in these three anciently diverged species. A small segment of the ostrich PAR is embedded within the inferred emu S1, which suggests a chromosomal rearrangement between these two birds Fig.
White-throated tinamou has a much smaller PAR due to two separate strata that formed about 50 21 to 95 Ma and 29 7 to 82 Ma table S6after its divergence with ostrich about 58 to 95 Ma Thus, common and lineage-specific events characterize sex chromosome evolution in Palaeognathae birds. In comparison, Neognathae species exhibit either three or four strata along their sex chromosomes Fig. We infer that the oldest Neognathae-specific stratum S1 formed in an ancestor of all Neognathae adjacent to the S0 region described above Fig.
We also recovered W-linked sequence fragments within this stratum by reordering them against the ostrich chrZ as a proxy for the proto-Z fig. Consistent with its ancestral emergence and in chicken 16Neognathae S1 harbors almost no identifiable W-linked fragments or genes in Galloanserae, and we find only few W-linked fragments with low sequence identities versus chrZ in Neoaves figs. S9 and S Adjacent to S1, we identify a younger Neognathae stratum S2 that spans a similar region in all Neognathae Fig. S16suggesting the Galliformes chickenAnseriformes Pekin duckand Neoaves may have each independently formed stratum S2, after the shared origination of S1.
One Neoaves species, the white-tailed tropicbird, seems to have experienced no further recombination suppressions after stratum S2, and its current PAR appears to be comparable to the Neoaves ancestor PAR Fig. By contrast, orthologs of tropicbird PAR genes are located in differentiated regions of all the other Neoaves, including brown mesite Mesitornis unicolorsuggesting that the youngest stratum S3 evolved independently in different lineages. Indeed, only five genes overlap between the different S3 regions Fig.
Recombination suppression at evolutionary strata may have been mediated by chromosomal inversions, as has been suggested for mammals 9 Genomic comparison of four avian species with de novo assembled genomes against the reptile outgroups green anole lizard Anolis carolinensis 42 and boa snake Boa constrictor 43 Fig.
S18 allow us to infer the presence of inversions on chrZ and further inform on the formation paths of evolutionary strata in birds. Both cytogenetic mapping 44 and our genomic comparison have shown that ostrich has maintained the most ancestral gene synteny relative to other avian species with only a few intrachromosomal rearrangements Fig. We specifically compared gene synteny spanning the ostrich S0 with the assembled genomes of green anole lizard and boa snake and to cytogenetic data from three other reptiles rat snake, gecko lizard, Chinese soft-shelled turtle 45and identified a chromosomal inversion on ostrich chrZ relative to reptiles, which are all collinear within their orthologous regions on the corresponding autosome fig.
This suggests that an inversion on the proto-Z abolished recombination between chrZ and chrW at S0 in an ancestor of all birds. Gene content and synteny within the ostrich S1 region is largely conserved between the green anole lizard and ostrich, suggesting that a putative inversion creating the ostrich-specific S1 stratum must have occurred on chrW Fig. Multiple genomic rearrangements within Neognathae S0 and S1 regions among Neognathae species preclude us from inferring the origin of Neognathae S1 figs. S13 and SSex dating in White bird
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