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Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome.

ABSTRACT: We used a comparative approach spanning three species and 90 million years to study the evolutionary history of the avian sex chromosomes. Using whole transcriptomes, we assembled the largest cross-species dataset of W-linked coding content to date. Our results show that recombination suppression in large portions of the avian sex chromosomes has evolved independently, and that long-term sex chromosome divergence is consistent with repeated and independent inversions spreading progressively to restrict recombination. In contrast, over short-term periods we observe heterogeneous and locus-specific divergence. We also uncover four instances of gene conversion between both highly diverged and recently evolved gametologs, suggesting a complex mosaic of recombination suppression across the sex chromosomes. Lastly, evidence from 16 gametologs reveal that the W chromosome is evolving with a significant contribution of purifying selection, consistent with previous findings that W-linked genes play an important role in encoding sex-specific fitness.

SUBMITTER: Wright AE

PROVIDER: S-EPMC4278454 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome.

Wright Alison E AE Harrison Peter W PW Montgomery Stephen H SH Pointer Marie A MA Mank Judith E JE

Evolution; international journal of organic evolution 20140829 11

We used a comparative approach spanning three species and 90 million years to study the evolutionary history of the avian sex chromosomes. Using whole transcriptomes, we assembled the largest cross-species dataset of W-linked coding content to date. Our results show that recombination suppression in large portions of the avian sex chromosomes has evolved independently, and that long-term sex chromosome divergence is consistent with repeated and independent inversions spreading progressively to r ...[more]

PMID: 25066800

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Project description:BackgroundInversion Symmetry is a generalization of the second Chargaff rule, stating that the count of a string of k nucleotides on a single chromosomal strand equals the count of its inverse (reverse-complement) k-mer. It holds for many species, both eukaryotes and prokaryotes, for ranges of k which may vary from 7 to 10 as chromosomal lengths vary from 2Mbp to 200 Mbp. Building on this formalism we introduce the concept of k-mer distances between chromosomes. We formulate two k-mer distance measures, D1 and D2, which depend on k. D1 takes into account all k-mers (for a single k) appearing on single strands of the two compared chromosomes, whereas D2 takes into account both strands of each chromosome. Both measures reflect dissimilarities in global chromosomal structures.ResultsAfter defining the various distance measures and summarizing their properties, we also define proximities that rely on the existence of synteny blocks between chromosomes of different bacterial strains. Comparing pairs of strains of bacteria, we find negative correlations between synteny proximities and k-mer distances, thus establishing the meaning of the latter as measures of evolutionary distances among bacterial strains. The synteny measures we use are appropriate for closely related bacterial strains, where considerable sections of chromosomes demonstrate high direct or reversed equality. These measures are not appropriate for comparing different bacteria or eukaryotes. K-mer structural distances can be defined for all species. Because of the arbitrariness of strand choices, we employ only the D2 measure when comparing chromosomes of different species. The results for comparisons of various eukaryotes display interesting behavior which is partially consistent with conventional understanding of evolutionary genomics. In particular, we define ratios of minimal k-mer distances (KDR) between unmasked and masked chromosomes of two species, which correlate with both short and long evolutionary scales.Conclusionsk-mer distances reflect dissimilarities among global chromosomal structures. They carry information which aggregates all mutations. As such they can complement traditional evolution studies , which mainly concentrate on coding regions.

Project description:BACKGROUND: Comparative genomics is a powerful tool to transfer genomic information from model species to related non-model species. Channel catfish (Ictalurus punctatus) is the primary aquaculture species in the United States. Its existing genome resources such as genomic sequences generated from next generation sequencing, BAC end sequences (BES), physical maps, linkage maps, and integrated linkage and physical maps using BES-associated markers provide a platform for comparative genomic analysis between catfish and other model teleost fish species. This study aimed to gain understanding of genome organizations and similarities among catfish and several sequenced teleost genomes using linkage group 8 (LG8) as a pilot study. RESULTS: With existing genome resources, 287 unique genes were identified in LG8. Comparative genome analysis indicated that most of these 287 genes on catfish LG8 are located on two homologous chromosomes of zebrafish, medaka, stickleback, and three chromosomes of green-spotted pufferfish. Large numbers of conserved syntenies were identified. Detailed analysis of the conserved syntenies in relation to chromosome level similarities revealed extensive inter-chromosomal and intra-chromosomal rearrangements during evolution. Of the 287 genes, 35 genes were found to be duplicated in the catfish genome, with the vast majority of the duplications being interchromosomal. CONCLUSIONS: Comparative genome analysis is a powerful tool even in the absence of a well-assembled whole genome sequence. In spite of sequence stacking due to low resolution of the linkage and physical maps, conserved syntenies can be identified although the exact gene order and orientation are unknown at present. Through chromosome-level comparative analysis, homologous chromosomes among teleosts can be identified. Syntenic analysis should facilitate annotation of the catfish genome, which in turn, should facilitate functional inference of genes based on their orthology.

Dataset Information

Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome.

Publications

Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome.

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