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, 10 (1), 2170

Extinction of Chromosomes Due to Specialization Is a Universal Occurrence

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Extinction of Chromosomes Due to Specialization Is a Universal Occurrence

Jason Wilson et al. Sci Rep.

Abstract

The human X and Y chromosomes evolved from a pair of autosomes approximately 180 million years ago. Despite their shared evolutionary origin, extensive genetic decay has resulted in the human Y chromosome losing 97% of its ancestral genes while gene content and order remain highly conserved on the X chromosome. Five 'stratification' events, most likely inversions, reduced the Y chromosome's ability to recombine with the X chromosome across the majority of its length and subjected its genes to the erosive forces associated with reduced recombination. The remaining functional genes are ubiquitously expressed, functionally coherent, dosage-sensitive genes, or have evolved male-specific functionality. It is unknown, however, whether functional specialization is a degenerative phenomenon unique to sex chromosomes, or if it conveys a potential selective advantage aside from sexual antagonism. We examined the evolution of mammalian orthologs to determine if the selective forces that led to the degeneration of the Y chromosome are unique in the genome. The results of our study suggest these forces are not exclusive to the Y chromosome, and chromosomal degeneration may have occurred throughout our evolutionary history. The reduction of recombination could additionally result in rapid fixation through isolation of specialized functions resulting in a cost-benefit relationship during times of intense selective pressure.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1
Ortholog Ka/Ks-GO Relationship: Average Ka/Ks values of 6,734 human genes across their related orthologs plotted against their number of GO terms. Each data point represents a human gene with surviving mammalian orthologs (n = 6,734). The x-axis corresponds to the number of gene ontology annotations that were found to be associated with each gene. The y-axis corresponds to a human gene’s average Ka/Ks value across its related species comparisons. The results of a gamma regression analysis indicated the association was statistically significant (p = 8.25×1020). This figure was generated using R statistical software (Version 3.5.3).
Figure 2
Figure 2
GO Ka/Ks Relationships: (a) Average Ka/Ks values of the 11,016 GO terms with unique gene sets in our dataset across each term’s related genes and human sequence comparisons plotted against the number of chromosome arms a given GO term was found. (b) Average Ka/Ks values of the same GO terms plotted against their number of related genes (trimmed within 3 SD of the mean number of genes for clarity). Each data point represents a GO annotation (n = 11,016). (a) The x-axis corresponds to the number of chromosome arms a given GO annotation was expressed on (the number of chromosome arms containing a gene that was associated with the given GO annotation). The y-axis corresponds to a GO annotation’s average Ka/Ks value across its related genes and their species comparisons. The results of a gamma regression analysis indicated the association was statistically significant (p = 7.01×1019). (b) The x-axis corresponds to the number of genes a given GO annotation was associated with. The y-axis corresponds to a GO annotation’s average Ka/Ks value across its related genes and their species comparisons. The results of a gamma regression analysis indicated the association was not statistically significant (p = 0.05). The accompanying figures were generated using R statistical software (Version 3.5.3).
Figure 3
Figure 3
GO Chromosome Arm and Gene Relationship: Number of genes related to each GO term plotted against the number of chromosome arms it was found (trimmed to within 3 SD of the mean number of genes for clarity). Each data point represents a GO annotation (n = 11,020). The x-axis corresponds to the number of chromosome arms a given GO annotation was expressed on (the number of chromosome arms containing a gene that was associated with the given GO annotation). The y-axis corresponds to the number of genes a given GO annotation was associated with. The results of a gamma regression analysis indicated the association was statistically significant (p < 0.0005). This figure was generated using R statistical software (Version 3.5.3).
Figure 4
Figure 4
Chromosome Arm Dendrogram: Hierarchical clustering of the chromosome arms based on functional relatedness of their genes. Hierarchical clustering of the chromosome arms based on functional relatedness of their genes. Chromosome arm functionality was obtained by deriving weighted frequencies for each GO annotation within our dataset. Frequencies were weighted based on the specificity of the GO annotation to a given chromosome arm. Distance measure is Euclidean. Multi-node clusters are joined based on minimum increase in within group variance.

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