Genomics of an avian neo-sex chromosome reveals the evolutionary dynamics of recombination suppression and sex-linked genes

Abstract

How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (Myr) of divergence and degeneration obscure their evolutionary history. Sylvioidea songbirds is an emerging model for understanding avian sex chromosome evolution because a unique chromosome fusion event ∼24 Myr ago has formed enlarged “neo-sex chromosomes” consisting of an added (new) and an ancestral (old) part. Here, we report the female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). We confirm that the added region has been translocated to both Z and W, and show that the added-W part has been heavily reorganised within itself and with the ancestral-W. Next, we show that recombination between Z and W continued after the fusion event, and that recombination suppression took ∼10 Myr to be completed and arose locally and non-linearly along the sex chromosomes. This pattern is inconsistent with that of large inversions and instead suggests gradual and mosaic recombination suppression. We find that the added-W mirrors the ancestral-W in terms of repeat accumulation, loss of genetic variation, and gene degeneration. Lastly, we show that genes being maintained on W are slowly evolving and dosage sensitive, and that highly conserved genes across broad taxonomic groups, regardless of sex-linkage, evolve slower on both Z and W. This study reveals complex expansion of recombination suppression along avian sex chromosomes, and that the evolutionary trajectory of sex-linked genes is highly predictable and governed partly by sex-linkage per se, partly by their functional properties.

The genomic architecture of the passerine MHC region: High repeat content and contrasting evolutionary histories of single copy and tandemly duplicated MHC genes

“…These repeats may have contributed both to the expansion of the MHC genes and the gene rearrangements in the core MHC region compared to earlier bird orders. Repeats cannot be efficiently removed from lowrecombining chromosomal regions, and as expected the great reed warbler ancestral W-chromosome, a sex-linked region that does not recombine, is extremely enriched for repeats compared to the rest of the genome (Sigeman et al, 2021). How then can the repeat content be so high in the rather large MHC region, approximately 5.5 Mb in the great reed warbler?…”

“…Suh) containing Repbase repeats (Bao et al, 2015), repeats from chicken and the zebra finch (Hillier et al, 2004;Warren et al, 2010) and curated repeats from hooded crow and flycatcher (Suh et al, 2018;Vijay et al, 2016). In contrast to Sigeman et al (2021) we did not include uncurated de novo predicted repeats in the repeat library as we observed a considerable overlap with multicopy genes.…”

“…The final assembly (acrAru1) consisted of 3,013 scaffolds with a cumulative length of 1.2 Gb and an N50 of 21.5 Mb (Table S1). Moreover, it had 93% complete single copy bird orthologues as assessed with BUSCO v.3.0.2 (aves_odb9 data set, N = 4,915) (Simão et al, 2015), and 22,524 genes were annotated (Sigeman et al, 2021). Eighteen scaffolds with MHC-genes (MHC-I and/or -IIB genes) and MHC-related genes, that is, genes expected to be found in the MHC-region such as TAP1 and TAP2, were identified in the genome: three MHC-I scaffolds (292, 314 and 476 kb), 11 MHC-IIB scaffolds (50-2,058 kb), two scaffolds with both MHC-I and -IIB genes (755 and 1,288 kb) and two MHC-related scaffolds (122 and 426 kb), covering a total genomic read length of approximately 5.5 Mb (Table S2).…”

A Chromosome-Level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus)

“…To date, the closest relative to the reed warbler with a published reference genome is the great tit ( Parus major ) (GCA_001522545.3, deposited in NCBI; Laine et al 2016 ), but the unpublished genome of the garden warbler ( Sylvia borin ) is available in public databases (GCA_014839755.1, deposited in NCBI). There is also a genome in preprint from the Acrocephalus genus, the great reed warbler ( A. arundinaceus ) ( Sigeman, Strandh, et al 2020 ), but the scaffolds are not chromosome length.…”

A Chromosome-level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus)

“…To date, the closest relative to the reed warbler with a published reference genome is the great tit (Parus major) (GCA_001522545.3, deposited in NCBI; Laine et al 2016), but the unpublished genome of the garden warbler (Sylvia borin) is available in public databases (GCA_014839755.1, deposited in NCBI). There is also a genome in preprint from the Acrocephalus genus, the great reed warbler (A. arundinaceus) (Sigeman et al 2020a), but the scaffolds are not chromosome-length.…”