Patterns of Substitution Rate Variation at Many Nuclear Loci in Two Species Trios in the Brassicaceae Partitioned with ANOVA
There are marked variations among loci and among lineages in rates of nucleotide substitution. The generation time hypothesis (GTH) is a neutral explanation for substitution rate heterogeneity that has genomewide application, predicting that species with shorter generation times accumulate DNA sequence substitutions faster than species with longer generation times do since faster genome replication provides more opportunities for mutations to occur and reach fixation by genetic drift. Relatively few studies have rigorously evaluated the GTH in plants, and there are numerous alternative hypotheses for plant substitution rate variation. One major challenge has been finding pairs of closely related plant species with contrasting generation times and appropriate outgroup taxa that all also have DNA sequence data for numerous loci. To test for causes of rate variation, we obtained sequence data for 256 genes for Arabidopsis thaliana, normally reproducing every year, and the biennial Arabidopsis lyrata with three closely related outgroup taxa (Brassica rapa, Capsella grandiflora, and Neslia paniculata) as well as the biennial Brassica oleracea and the annual B. rapa lineage with the outgroup N. paniculata. A sign test indicated that more loci than expected by chance have faster rates of substitution on the branch leading to the annual than to the perennial for one three-species trio but not another. Tajima's 1D and 2D tests, and a likelihood ratio test that incorporated saturation correction, rejected rate homogeneity for up to 26 genes (up to 14 genes when correcting for multiple tests), consistently showing faster rates for the annual lineage in the Arabidopsis species trio. ANOVA showed significant rate heterogeneity between the Arabidopsis and Brassica species trios (about 6 % of rate variation) and among loci (about 26-32 % of rate variation). The lineage-by-locus interaction which would be caused by locus- and lineage-specific natural selection explained about 13 % of substitution rate variation in one ANOVA model using substitution rates from genes partitioned into odd and even codons but was not a significant effect without partitioned genes. Annual/perennial lineage and species trio by annual/perennial lineage each explained about 1 % of substitution rate variation.
Braverman, John M., Matthew B. Hamilton, and Brent A. Johnson. 2016. “Patterns of Substitution Rate Variation at Many Nuclear Loci in Two Species Trios in the Brassicaceae Partitioned with ANOVA.” Journal of Molecular Evolution 83.3 (2016: Oct): 97-109.
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