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. 2013 Nov 21;8(11):e80431.
doi: 10.1371/journal.pone.0080431. eCollection 2013.

The phylogeny and biogeographic history of ashes (fraxinus, oleaceae) highlight the roles of migration and vicariance in the diversification of temperate trees

Damien Daniel Hinsinger  1 , Jolly Basak, Myriam Gaudeul, Corinne Cruaud, Paola Bertolino, Nathalie Frascaria-Lacoste, Jean Bousquet
Affiliations

The phylogeny and biogeographic history of ashes (fraxinus, oleaceae) highlight the roles of migration and vicariance in the diversification of temperate trees

Damien Daniel Hinsinger et al. PLoS One. .

Abstract

The cosmopolitan genus Fraxinus, which comprises about 40 species of temperate trees and shrubs occupying various habitats in the Northern Hemisphere, represents a useful model to study speciation in long-lived angiosperms. We used nuclear external transcribed spacers (nETS), phantastica gene sequences, and two chloroplast loci (trnH-psbA and rpl32-trnL) in combination with previously published and newly obtained nITS sequences to produce a time-calibrated multi-locus phylogeny of the genus. We then inferred the biogeographic history and evolution of floral morphology. An early dispersal event could be inferred from North America to Asia during the Oligocene, leading to the diversification of the section Melioides sensus lato. Another intercontinental dispersal originating from the Eurasian section of Fraxinus could be dated from the Miocene and resulted in the speciation of F. nigra in North America. In addition, vicariance was inferred to account for the distribution of the other Old World species (sections Sciadanthus, Fraxinus and Ornus). Geographic speciation likely involving dispersal and vicariance could also be inferred from the phylogenetic grouping of geographically close taxa. Molecular dating suggested that the initial divergence of the taxonomical sections occurred during the middle and late Eocene and Oligocene periods, whereas diversification within sections occurred mostly during the late Oligocene and Miocene, which is consistent with the climate warming and accompanying large distributional changes observed during these periods. These various results underline the importance of dispersal and vicariance in promoting geographic speciation and diversification in Fraxinus. Similarities in life history, reproductive and demographic attributes as well as geographical distribution patterns suggest that many other temperate trees should exhibit similar speciation patterns. On the other hand, the observed parallel evolution and reversions in floral morphology would imply a major influence of environmental pressure. The phylogeny obtained and its biogeographical implications should facilitate future studies on the evolution of complex adaptive characters, such as habitat preference, and their possible roles in promoting divergent evolution in trees.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic tree resulting from BIM analysis of the combined dataset (cpDNA, ETS, ITS and phantastica).
Posterior probabilities ≥0.50 are indicated below the branches. Tree nodes that involve floral changes and the relative likelihoods of floral states are indicated by circles: black, complete flower (calyx+corolla); grey, incomplete flower (loss of corolla or calyx); white, naked flower (no calyx or corolla). On the right, schematic floral character states are shown at the tip of the branches. On the right, sections are indicated by vertical bars; the dotted line indicates the occurrence of F. platypoda, previously placed in the section Fraxinus , but here shown to be closely related to the incertae sedis species.
Figure 2
Figure 2. a. Chronogram generated from BEAST analysis and estimations of times of divergence and diversification of sections in Fraxinus (in mya), and showing the results from Lagrange analysis.
Bars at nodes represent the 95% confidence interval; stars indicate the calibration nodes. Map showing the colours used to identify the areas of occurrence of Fraxinus species: red, North America (Am); green, Asia (As); blue, Europe (Eu); yellow, North Africa. The same colours were used on the tree to indicate the reconstructed geographic range across the branches and nodes. For the Lagrange results, a slash indicates the split of areas into two daughter lineages, namely, left/right, where “up” and “down” are the ranges inherited by each descendant branch. The values in brackets represent relative probabilities. When a node has alternative scenarios within 2 log-likelihood units of the optimal reconstruction, the relative probability (fraction of the global likelihood) for the optimal reconstruction is indicated with a smaller font. Circles on nodes indicate migration events or vicariance processes as inferred according to the Lagrange analysis. b. Semilogarithmic Lineage Through Time (LTT) plot (solid line) averaged over 135,000 posterior trees from the BIM analysis: right axis, the solid line represents the cumulative number of lineages and the blue area, the 95% confidence interval; in dark grey, plot of the global deep-sea temperature and its variance, with temperature estimates, geological and biological events reported elsewhere ; age in millions of years.
Figure 3
Figure 3. Map illustrating major events in the biogeographic history of the genus Fraxinus.
(a) The genus likely appeared in North America (1), the section Dipetalae diverging early (2). (b) Diversifications leading to the sections Melioides and later Pauciflorae (3) in North America were followed by migrations to Asia, leading to the sections Ornus (4) and to the Asian species of the section Melioides (5). (c) The section Sciadanthus expanded in Eurasia and Africa (6), (d) followed by the divergence of the Asian section Fraxinus (7) and the migration of a lineage leading to F. nigra in North America (8). More recently, the differentiation of F. mandshurica in Asia and transcontinental expansion of the lineage towards Europe (9) resulted in the observed geographical diversity of the section Fraxinus throughout Eurasia.
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References

    1. Jaramillo-Correa JP, Beaulieu J, Khasa DP, Bousquet J (2009) Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 39: 286–307.
    1. Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends in Ecology and Evolution 17: 361–369.
    1. Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forests 6: 95–124.
    1. Wallander E (2008) Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Systematics and Evolution 273: 25–49.
    1. Morand-Prieur M-E, Raquin C, Shykoff JA, Frascaria-Lacoste N (2003) Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae). American Journal of Botany 90: 949–953. - PubMed

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