Heterogeneous histories of recombination suppression on stickleback sex chromosomes
Description
How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X-Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.
Notes
Scripts and data used for comparative study of blackspotted stickleback (Gasterosteus wheatlandi) sex chromosomes.
Scripts:
ConstructFasta.wheatlandi.R - Takes a phased haploid vcf file and outputs a fasta file used to generate gene trees
ExtractPaternalAllele.R - Takes a phased genotype file and extracts the alleles inherited by the father (i.e., blackspotted stickleback in this manuscript).
IDautosomalpeaks.R - Identifies autosomal regions that duplicated onto the Y chromosome in the shared ancestor of blackspotted and Japan Sea stickleback
phasescript.crosses.R - Phases sequences based on patterns of transmission in pedigree of parent-offspring quartets (used for analysis of blackspotted stickleback sex chromosomes)
phasescriptXII.allSpecies.R - Phases sequences based on patterns of transmission in pedigree of parent-offspring quartets (used for gene tree analysis of Chr 12 neo-sex chromosome using data from blackspotted and Japan Sea stickleback quartets)
phasescriptXIX.allSpecies.R - Phases sequences based on patterns of transmission in pedigree of parent-offspring quartets (used for gene tree analysis of Chr 19 ancestral sex chromosome using data from blackspotted and Japan Sea stickleback quartets)
PopGenPlots.R - script used for basic population genetics analysis (FST, pi, Tajima's D) of blackspotted stickleback sex chromosomes, including creation of plots for manuscript
ReadDepth.R - Analyzes male-to-female read depth ratio along sex chromosomes
XYconsistency.R - Gene tree approach for detecting suppressed recombination between X and Y chromosomes
Data:
wheatlandi.pedigree - pedigree file indicating identity of blackspotted stickleback father, threespine mother, son, and daughter for the 15 crosses used to obtain phased blackspotted X and Y chromosome sequences
phasedchrXII.wheatlandi.masked.SibFilter.haploid.vcf- phased haploid vcf file for threespine x blackspotted stickleback parent-offspring quartets, mapped to Glazer et al. stickleback genome (Chr 12)
phasedchrXIX.wheatlandi.masked.SibFilter.haploid.vcf- phased haploid vcf file for threespine x blackspotted stickleback parent-offspring quartets, mapped to Glazer et al. stickleback genome (Chr 19)
wheatlandi.masked.chrXII.minQ999.mindepth26.maxdepth52.minGQ20.recode.vcf - unphased filtered vcf file for threespine x blackspotted stickleback parent-offspring quartets, mapped to Nath et al. 2021 stickleback genome (Chr 12)
wheatlandi.masked.chrXIX.minQ999.mindepth26.maxdepth52.minGQ20.recode.vcf - unphased filtered vcf file for threespine x blackspotted stickleback parent-offspring quartets, mapped to Nath et al. 2021 stickleback genome (Chr 19)
allspecies.pedigree - pedigree file indicating identity of father, mother, son, and daughter for the 4 threespine x blackspotted stickleback crosses and 4 threespine x Japan Sea stickleback crosses used in multispecies gene tree analysis
allspecies.masked.chrXII.phased.groves.haploid.vcf - phased haploid vcf file used for multispecies gene tree analysis of Chr 12 (mapped to Glazer et al. reference genome)
allspecies.masked.chrXIX.phased.groves.haploid.vcf - phased vcf file used for multispecies gene tree analysis of Chr 19 (mapped to Glazer et al. reference genome)
JS.wheatlandi.overlappingWindows.txt - all10kb autosomal windows that show outlier (top 2%) male-female FST in both blackspotted and Japan Sea stickleback
JS.wheatlandi.overlappingSNPs.txt - SNPs falling within shared autosomal male-female FST outlier windows listed in above file
Funding provided by: National Institutes of Health
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000002
Award Number: R01-GM116853
Files
JS.wheatlandi.overlappingSNPs.txt
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Additional details
Related works
- Is cited by
- 10.1093/molbev/msab179 (DOI)
- Is derived from
- 10.5281/zenodo.5567729 (DOI)