Dataset Information

Neo-sex chromosomes and adaptive potential in tortricid pests.

ABSTRACT: Changes in genome architecture often have a significant effect on ecological specialization and speciation. This effect may be further enhanced by involvement of sex chromosomes playing a disproportionate role in reproductive isolation. We have physically mapped the Z chromosome of the major pome fruit pest, the codling moth, Cydia pomonella (Tortricidae), and show that it arose by fusion between an ancestral Z chromosome and an autosome corresponding to chromosome 15 in the Bombyx mori reference genome. We further show that the fusion originated in a common ancestor of the main tortricid subfamilies, Olethreutinae and Tortricinae, comprising almost 700 pest species worldwide. The Z-autosome fusion brought two major genes conferring insecticide resistance and clusters of genes involved in detoxification of plant secondary metabolites under sex-linked inheritance. We suggest that this fusion significantly increased the adaptive potential of tortricid moths and thus contributed to their radiation and subsequent speciation.

SUBMITTER: Nguyen P

PROVIDER: S-EPMC3637691 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Neo-sex chromosomes and adaptive potential in tortricid pests.

Nguyen Petr P Sýkorová Miroslava M Šíchová Jindra J Kůta Václav V Dalíková Martina M Čapková Frydrychová Radmila R Neven Lisa G LG Sahara Ken K Marec František F

Proceedings of the National Academy of Sciences of the United States of America 20130408 17

Changes in genome architecture often have a significant effect on ecological specialization and speciation. This effect may be further enhanced by involvement of sex chromosomes playing a disproportionate role in reproductive isolation. We have physically mapped the Z chromosome of the major pome fruit pest, the codling moth, Cydia pomonella (Tortricidae), and show that it arose by fusion between an ancestral Z chromosome and an autosome corresponding to chromosome 15 in the Bombyx mori referenc ...[more]

PMID: 23569222

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Project description:Understanding sex-biased natural selection can be enhanced by access to well-annotated chromosomes including ones inherited in sex-specific fashion. The eastern yellow robin (EYR) is an endemic Australian songbird inferred to have experienced climate-driven sex-biased selection and is a prominent model for studying mitochondrial-nuclear interactions in the wild. However, the lack of an EYR reference genome containing both sex chromosomes (in birds, a female bearing Z and W chromosomes) limits efforts to understand the mechanisms of these processes. Here, we assemble the genome for a female EYR and use low-depth (10×) genome resequencing data from 19 individuals of known sex to identify chromosome fragments with sex-specific inheritance. MaSuRCA hybrid assembly using Nanopore and Illumina reads generated a 1.22-Gb EYR genome in 20,702 scaffolds (94.2% BUSCO completeness). Scaffolds were tested for W-linked (female-only) inheritance using a k-mer approach, and for Z-linked inheritance using median read-depth test in male and female reads (read-depths must indicate haploid female and diploid male representation). This resulted in 2,372 W-linked scaffolds (total length: 97,872,282 bp, N50: 81,931 bp) and 586 Z-linked scaffolds (total length: 121,817,358 bp, N50: 551,641 bp). Anchoring of the sex-linked EYR scaffolds to the reference genome of a female zebra finch revealed 2 categories of sex-linked genomic regions. First, 653 W-linked scaffolds (25.7 Mb) were anchored to the W sex chromosome and 215 Z-linked scaffolds (74.4 Mb) to the Z. Second, 1,138 W-linked scaffolds (70.9 Mb) and 179 Z-linked scaffolds (51.0 Mb) were anchored to a large section (coordinates ∼5 to ∼60 Mb) of zebra finch chromosome 1A. The first ∼5 Mb and last ∼14 Mb of the reference chromosome 1A had only autosomally behaving EYR scaffolds mapping to them. We report a female (W chromosome-containing) EYR genome and provide genomic evidence for a neo-sex (neo-W and neo-Z) chromosome system in the EYR, involving most of a large chromosome (1A) previously only reported to be autosomal in passerines.

Project description:Sex chromosomes originated from autosomes but have evolved a highly specialized chromatin structure. Drosophila Y chromosomes are composed entirely of silent heterochromatin, while male X chromosomes have highly accessible chromatin and are hypertranscribed as a result of dosage compensation. Here, we dissect the molecular mechanisms and functional pressures driving heterochromatin formation and dosage compensation of the recently formed neo-sex chromosomes of Drosophila miranda. We show that the onset of heterochromatin formation on the neo-Y is triggered by an accumulation of repetitive DNA. The neo-X has evolved partial dosage compensation and we find that diverse mutational paths have been utilized to establish several dozen novel binding consensus motifs for the dosage compensation complex on the neo-X, including simple point mutations at pre-binding sites, insertion and deletion mutations, microsatellite expansions, or tandem amplification of weak binding sites. Spreading of these silencing or activating chromatin modifications to adjacent regions results in massive mis-expression of neo-sex linked genes, and little correspondence between functionality of genes and their silencing on the neo-Y or dosage compensation on the neo-X. Intriguingly, the genomic regions being targeted by the dosage compensation complex on the neo-X and those becoming heterochromatic on the neo-Y show little overlap, possibly reflecting different propensities along the ancestral chromosome that formed the sex chromosome to adopt active or repressive chromatin configurations. Our findings have broad implications for current models of sex chromosome evolution, and demonstrate how mechanistic constraints can limit evolutionary adaptations. Our study also highlights how evolution can follow predictable genetic trajectories, by repeatedly acquiring the same 21-bp consensus motif for recruitment of the dosage compensation complex, yet utilizing a diverse array of random mutational changes to attain the same phenotypic outcome.

Dataset Information

Neo-sex chromosomes and adaptive potential in tortricid pests.

Publications

Neo-sex chromosomes and adaptive potential in tortricid pests.

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