Contrasting Rates of Molecular Evolution and Patterns of Selection among Gymnosperms and Flowering Plants

Abstract

The majority of variation in rates of molecular evolution among seed plants remains both unexplored and unexplained. Although some attention has been given to flowering plants, reports of molecular evolutionary rates for their sister plant clade (gymnosperms) are scarce, and to our knowledge differences in molecular evolution among seed plant clades have never been tested in a phylogenetic framework. Angiosperms and gymnosperms differ in a number of features, of which contrasting reproductive biology, life spans, and population sizes are the most prominent. The highly conserved morphology of gymnosperms evidenced by similarity of extant species to fossil records and the high levels of macrosynteny at the genomic level have led scientists to believe that gymnosperms are slow-evolving plants, although some studies have offered contradictory results. Here, we used 31,968 nucleotide sites obtained from orthologous genes across a wide taxonomic sampling that includes representatives of most conifers, cycads, ginkgo, and many angiosperms with a sequenced genome. Our results suggest that angiosperms and gymnosperms differ considerably in their rates of molecular evolution per unit time, with gymnosperm rates being, on average, seven times lower than angiosperm species. Longer generation times and larger genome sizes are some of the factors explaining the slow rates of molecular evolution found in gymnosperms. In contrast to their slow rates of molecular evolution, gymnosperms possess higher substitution rate ratios than angiosperm taxa. Finally, our study suggests stronger and more efficient purifying and diversifying selection in gymnosperm than in angiosperm species, probably in relation to larger effective population sizes.

Keywords: angiosperms; gymnosperms; life-history traits; mutation; selection; substitution rates.

Fig. 1.

Phylogenetic tree obtained from a concatenated alignment of 42 single-copy genes and 66 species distributed between two main seed plant lineages (angiosperms in green, gymnosperms in blue, and outgroup in black) inferred by RAxML. Stem branches for angiosperms and gymnosperms were used for model testing using the branch models implemented in codeml. Results of the model testing can be found in table 2.

Fig. 2.

(A) Boxplots showing differences in number of synonymous substitutions (dS), nonsynonymous substitutions (dN), absolute rate of silent-site divergence (μ), and substitution rate ratio (ω), among life forms defined as angiosperms herbs (green), angiosperms shrub/trees (light green), and gymnosperms (blue). Results of the statistical tests of comparisons among groups can be found in supplementary table S6, Supplementary Material Online. (B) Proportion of sites under negative selection, when all sites are evaluated (top left), when S < –15 (top right), and when S > –15 (bottom left); and proportion of sites under positive selection (bottom right). Green boxes represent angiosperm species, and blue boxes, gymnosperms. (C) Distribution of the selection coefficient (f(S)) of new mutations. It was calculated for all species in each taxonomic family studied, assuming a gamma distribution of ω among sites. Parameter estimates α and β were obtained from running the site model 5 in codeml (PAML) using a concatenated alignment of 29,000–31,000 sites per taxonomic family. Selection coefficients were then obtained replacing α and β in equation 1. Green dotted vertical lines are used to show the distribution of f(S) when S ≈ 0 and ω = 1 (neutrality). Taxonomic families containing less than 5 species were not analyzed due to difficulties in constructing the phylogenetic trees in RaxML.