Negative correlation between rates of molecular evolution and flowering cycles in temperate woody bamboos revealed by plastid phylogenomics

Abstract

Background: Heterogeneous rates of molecular evolution are universal across the tree of life, posing challenges for phylogenetic inference. The temperate woody bamboos (tribe Arundinarieae, Poaceae) are noted for their extremely slow molecular evolutionary rates, supposedly caused by their mysterious monocarpic reproduction. However, the correlation between substitution rates and flowering cycles has not been formally tested.

Results: Here we present 15 newly sequenced plastid genomes of temperate woody bamboos, including the first genomes ever sequenced from Madagascar representatives. A data matrix of 46 plastid genomes representing all 12 lineages of Arundinarieae was assembled for phylogenetic and molecular evolutionary analyses. We conducted phylogenetic analyses using different sequences (e.g., coding and noncoding) combined with different data partitioning schemes, revealing conflicting relationships involving internodes among several lineages. A great difference in branch lengths were observed among the major lineages, and topological inconsistency could be attributed to long-branch attraction (LBA). Using clock model-fitting by maximum likelihood and Bayesian approaches, we furthermore demonstrated extensive rate variation among these major lineages. Rate accelerations mainly occurred for the isolated lineages with limited species diversification, totaling 11 rate shifts during the tribe's evolution. Using linear regression analysis, we found a negative correlation between rates of molecular evolution and flowering cycles for Arundinarieae, notwithstanding that the correlation maybe insignificant when taking the phylogenetic structure into account.

Conclusions: Using the temperate woody bamboos as an example, we found further evidence that rate heterogeneity is universal in plants, suggesting that this will pose a challenge for phylogenetic reconstruction of bamboos. The bamboos with longer flowering cycles tend to evolve more slowly than those with shorter flowering cycles, in accordance with a putative generation time effect.

Keywords: Generation time; Infrequent flowering; Molecular evolution; Plastid phylogenomics; Rate heterogeneity; Temperate woody bamboos.

Fig. 1

Phylogenetic relationships among major lineages of Arundinarieae based on complete plastid genomes. Unpartitioned maximum likelihood (ML) topology shown, and all unlabeled nodes received both maximum ML and Bayesian support values. The tropical woody bamboos as outgroups are not shown and the full tree is provided in Additional file 2

Fig. 2

Summary of conflicting phylogenetic relationships involving the major lineages of Arundinarieae. The different topologies are illustrated in (a) and supports from reconstruction of different plastid genomic sequences and/or partitioning methods are summarized in (b)

Fig. 3

Relative plastid rate of molecular evolution among the lineages of Arundinarieae from Bayesian analysis under the random local clock (RLC) model. Branch thickness is proportional to the inferred median rate for the branch with detail numbers. The tropical woody bamboos as outgroups are not shown and the full tree is provided in Additional file 9

Fig. 4

Reconstruction of the evolution of flowering cycles in Arundinarieae. The 14 documented records of flowering cycles are mapped on the pruned maximum likelihood (ML) tree in Fig. 1

Fig. 5

Rates of molecular evolution and flowering cycles are correlated in Arundinarieae. The flowering cycle is significantly negatively correlated with branch length inferred from unpartitioned maximum likelihood analysis using the simple (blue line) and Siegel’s repeated median (red line) linear regression. The filled circle represents the point of Gaoligongshania megalothyrsa