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Five major shifts of diversification through the long evolutionary history of Magnoliidae (angiosperms) - PubMed

Julien Massoni  1 ,

Five major shifts of diversification through the long evolutionary history of Magnoliidae (angiosperms)

Julien Massoni et al. BMC Evol Biol. .

Abstract

Background: With 10,000 species, Magnoliidae are the largest clade of flowering plants outside monocots and eudicots. Despite an ancient and rich fossil history, the tempo and mode of diversification of Magnoliidae remain poorly known. Using a molecular data set of 12 markers and 220 species (representing >75% of genera in Magnoliidae) and six robust, internal fossil age constraints, we estimate divergence times and significant shifts of diversification across the clade. In addition, we test the sensitivity of magnoliid divergence times to the choice of relaxed clock model and various maximum age constraints for the angiosperms.

Results: Compared with previous work, our study tends to push back in time the age of the crown node of Magnoliidae (178.78-126.82 million years, Myr), and of the four orders, Canellales (143.18-125.90 Myr), Piperales (158.11-88.15 Myr), Laurales (165.62-112.05 Myr), and Magnoliales (164.09-114.75 Myr). Although families vary in crown ages, Magnoliidae appear to have diversified into most extant families by the end of the Cretaceous. The strongly imbalanced distribution of extant diversity within Magnoliidae appears to be best explained by models of diversification with 6 to 13 shifts in net diversification rates. Significant increases are inferred within Piperaceae and Annonaceae, while the low species richness of Calycanthaceae, Degeneriaceae, and Himantandraceae appears to be the result of decreases in both speciation and extinction rates.

Conclusions: This study provides a new time scale for the evolutionary history of an important, but underexplored, part of the tree of angiosperms. The ages of the main clades of Magnoliidae (above the family level) are older than previously thought, and in several lineages, there were significant increases and decreases in net diversification rates. This study is a new robust framework for future investigations of trait evolution and of factors influencing diversification in this group as well as angiosperms as a whole.

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Figures

Figure 1

Age estimates for the root and different nodes within the tree of Magnoliidae. Estimates are in million years, and the root is constrained with a maximum age. Names of families refer to the crown node ages except when SL (stem lineage) is mentioned. A, BEAST analyses with mean age estimates and 95% credibility intervals. B, r8s (penalized likelihood) analyses with best-scoring ML tree age and 95% credibility intervals. *The stem lineage of Siparunaceae, in the BEAST analysis with the maximum age of angiosperms set to 140 million years, did not correspond to the same node in other analyses. Abbreviation: SL, stem lineage.

Figure 2

Diversification analyses. Results of the MEDUSA analyses obtained using 1000 posterior trees randomly sampled from the BEAST posterior: A, angio-140, B, angio-200. Topologies are the maximum clade credibility tree of 1000 randomly selected trees (phylogenetic relationships between A and B are identical). Names of terminals refer to compartments defined in the Methods sections and detailed in Additional file 5. Branch colors illustrate the mean net diversification rate (r). Red dots denote significant shifts in r, their size being proportional to their frequency among the 1000 trees tested. Numbered shifts in Figure 2A: 1, crown node of the clade of Piperaceae and Saururaceae; 2, crown node of the clade of Piperaceae excluding Verhuellia; 3, crown node of Calycanthaceae; 4, crown node of the clade of Himantandraceae and Degeneriaceae; 5, crown node of the clade of Miliuseae and Monocarpia. The diagram in the top-right corner represents the frequency of the different model sizes (number of shifts) in the 1000-model collections for the two analyses (angio-140 and angio-200). Abbreviations: sp., species; Myr, million years.

Figure 3

Chronogram of the angio-140 analysis obtained with BEAST. Maximum clade credibility tree obtained with BEAST and the maximum age constraint for the crown node of angiosperms set to 140 million years. Node bars are 95% credibility intervals. Blue dots symbolize minimum age constraints, and green dots the maximum age constraints applied to crown eudicots and crown angiosperms. The geologic time scale follows Gradstein et al. [39]. Abbreviations: Oligo., Oligocene; Mio., Miocene; Plio., Pliocene; Win., Winteraceae; Can., Canellaceae; Ari., Aristolochiaceae (incl. Lactoris); Sau., Saururaceae; Pip., Piperaceae; Cal., Calycanthaceae; Ath., Atherospermataceae; Her., Hernandiaceae; Lau., Lauraceae; Mon., Monimiaceae; Myr., Myristicaceae; Deg., Degeneriaceae; Him., Himantandraceae; Mag., Magnoliaceae; Eup., Eupomatiaceae; Ann., Annonaceae.

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