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. 2009 Jul;104(1):143-60.
doi: 10.1093/aob/mcp105. Epub 2009 May 23.

Phylogenetics of Olea (Oleaceae) based on plastid and nuclear ribosomal DNA sequences: tertiary climatic shifts and lineage differentiation times

Guillaume Besnard  1 , Rafael Rubio de Casas, Pascal-Antoine Christin, Pablo Vargas
Affiliations

Phylogenetics of Olea (Oleaceae) based on plastid and nuclear ribosomal DNA sequences: tertiary climatic shifts and lineage differentiation times

Guillaume Besnard et al. Ann Bot. 2009 Jul.

Abstract

Background and aims: The genus Olea (Oleaceae) includes approx. 40 taxa of evergreen shrubs and trees classified in three subgenera, Olea, Paniculatae and Tetrapilus, the first of which has two sections (Olea and Ligustroides). Olive trees (the O. europaea complex) have been the subject of intensive research, whereas little is known about the phylogenetic relationships among the other species. To clarify the biogeographical history of this group, a molecular analysis of Olea and related genera of Oleaceae is thus necessary.

Methods: A phylogeny was built of Olea and related genera based on sequences of the nuclear ribosomal internal transcribed spacer-1 and four plastid regions. Lineage divergence and the evolution of abaxial peltate scales, the latter character linked to drought adaptation, were dated using a Bayesian method.

Key results: Olea is polyphyletic, with O. ambrensis and subgenus Tetrapilus not sharing a most recent common ancestor with the main Olea clade. Partial incongruence between nuclear and plastid phylogenetic reconstructions suggests a reticulation process in the evolution of subgenus Olea. Estimates of divergence times for major groups of Olea during the Tertiary were obtained.

Conclusions: This study indicates the necessity of revising current taxonomic boundaries in Olea. The results also suggest that main lines of evolution were promoted by major Tertiary climatic shifts: (1) the split between subgenera Olea and Paniculatae appears to have taken place at the Miocene-Oligocene boundary; (2) the separation of sections Ligustroides and Olea may have occurred during the Early Miocene following the Mi-1 glaciation; and (3) the diversification within these sections (and the origin of dense abaxial indumentum in section Olea) was concomitant with the aridification of Africa in the Late Miocene.

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Figures

Fig. 1.
Fig. 1.
Phylogenetic tree for Olea species based on four plastid DNA regions (trnT-trnL, trnL-trnF, trnS-trnG and matK). Majority-rule consensus tree of the Bayesian inference (BI) analysis. BI support values (posterior probability) are indicated on tree branches. Ligustrum vulgare served as the outgroup to root the tree. Numbers in bold below branches indicate maximum parsimony node support (bootstrap value). Abbreviations: O. c., Olea capensis; O. e., Olea europaea.
Fig. 2.
Fig. 2.
Majority-rule consensus tree of nuclear ribosomal DNA (ITS-1) sequences using Bayesian inference. Bayesian support values are indicated above branches. Numbers in bold below branches indicate maximum-parsimony node support (bootstrap value). Divergent haplotypes found in a single tree (from Tassili n'Ajjer and Tenerife) are numbered 1 and 2. The tree was rooted using Ligustrum vulgare and Syringa vulgaris. Abbreviations: O. c., Olea capensis; O. e., Olea europaea; MD, Madagascar.
Fig. 3.
Fig. 3.
Divergence time estimates based on both ITS-1 and plastid DNA sequences for major Olea lineages. The scale is in millions of years (Mya). Horizontal rectangles on nodes represent standard deviations of divergence times. Vertical dotted lines indicate major Tertiary bioclimatic events: (a) Oi-1 glacial maximum (34 Mya; Zachos et al., 2001); (b) Mi-1 glaciation at the Miocene–Oligocene boundary (24 Mya; Zachos et al., 2001); (c) marked global cooling and subsequent aridification of Africa (16–2·8 Mya; Zachos et al., 2001), increase of the East Antarctica Ice Sheet and the meridional temperature gradient (Flower and Kennett, 1994); (d) desertification of the Sahara (approx. 10–7 Mya; Flower and Kennett, 1994), establishment of the Benguela current and aridification of southern Africa (Linder, 2003). The appearance of scattered peltate scales (solid triangle 1) and indumenta with large lobed peltate scales (solid triangle 2) on the abaxial leaf surface is indicated on the corresponding branches. See Supplementary Data 3 for more details on the phylogenetic tree topology. *Olea europaea subspp. cerasiformis, europaea, guanchica and maroccana.
Fig. 4.
Fig. 4.
SEM photographs of the abaxial surface of several members of Olea and related taxa. Stomata protected by dense scales (4) are only observed in samples of subgenus Olea, section Olea, although scattered peltate trichomes (3) are observed in other species of Olea. Specimens of subgenus Tetrapilus and other genera do not have scales, although in some cases they possess glandular structures (2) and, in the case of O. rosea, linear trichomes (1). Detailed views of stomata are shown, except for O. europaea subsp. laperrinei, for which stomata could not be observed because of the density of the scales. The orifices (5) seen in this image are sectioned stems of missing trichomes. (A) Noronhia sp. (ANK1); (B) Noronhia sp. (ANK2); (C) Chionanthus ramiflorus; (D) Nestegis sandwicensis; (E–K) subgenus Tetrapilus: (E) Olea tsoongii, (F) O. neriifolia, (G) O. wightiana, (H) O. rosea, (I) O. hainanensis, (J) O. brachiata, (K) O. paniculata (subgenus Paniculatae); (L–R) subgenus Olea section Ligustroides: (L) O. schliebenii, (M) O. exasperata, (N) O. capensis subsp. capensis, (O) O. capensis subsp. macrocarpa, (P) O. welwitschii, (Q) O. lancea, (R) O. woodiana; (S–V) subgenus Olea section Olea: (S) O. europaea subsp. europaea, (T) O. europaea subsp. cuspidata, (U) O. europaea subsp. guanchica, (V) O. europaea subsp. laperrinei. Scale bars are 200 µm and 40 µm for the left-hand and right-hand images in each pair, respectively. The scale bar in (V) is 200 µm.
Fig. 4.
Fig. 4.
SEM photographs of the abaxial surface of several members of Olea and related taxa. Stomata protected by dense scales (4) are only observed in samples of subgenus Olea, section Olea, although scattered peltate trichomes (3) are observed in other species of Olea. Specimens of subgenus Tetrapilus and other genera do not have scales, although in some cases they possess glandular structures (2) and, in the case of O. rosea, linear trichomes (1). Detailed views of stomata are shown, except for O. europaea subsp. laperrinei, for which stomata could not be observed because of the density of the scales. The orifices (5) seen in this image are sectioned stems of missing trichomes. (A) Noronhia sp. (ANK1); (B) Noronhia sp. (ANK2); (C) Chionanthus ramiflorus; (D) Nestegis sandwicensis; (E–K) subgenus Tetrapilus: (E) Olea tsoongii, (F) O. neriifolia, (G) O. wightiana, (H) O. rosea, (I) O. hainanensis, (J) O. brachiata, (K) O. paniculata (subgenus Paniculatae); (L–R) subgenus Olea section Ligustroides: (L) O. schliebenii, (M) O. exasperata, (N) O. capensis subsp. capensis, (O) O. capensis subsp. macrocarpa, (P) O. welwitschii, (Q) O. lancea, (R) O. woodiana; (S–V) subgenus Olea section Olea: (S) O. europaea subsp. europaea, (T) O. europaea subsp. cuspidata, (U) O. europaea subsp. guanchica, (V) O. europaea subsp. laperrinei. Scale bars are 200 µm and 40 µm for the left-hand and right-hand images in each pair, respectively. The scale bar in (V) is 200 µm.
Fig. 4.
Fig. 4.
SEM photographs of the abaxial surface of several members of Olea and related taxa. Stomata protected by dense scales (4) are only observed in samples of subgenus Olea, section Olea, although scattered peltate trichomes (3) are observed in other species of Olea. Specimens of subgenus Tetrapilus and other genera do not have scales, although in some cases they possess glandular structures (2) and, in the case of O. rosea, linear trichomes (1). Detailed views of stomata are shown, except for O. europaea subsp. laperrinei, for which stomata could not be observed because of the density of the scales. The orifices (5) seen in this image are sectioned stems of missing trichomes. (A) Noronhia sp. (ANK1); (B) Noronhia sp. (ANK2); (C) Chionanthus ramiflorus; (D) Nestegis sandwicensis; (E–K) subgenus Tetrapilus: (E) Olea tsoongii, (F) O. neriifolia, (G) O. wightiana, (H) O. rosea, (I) O. hainanensis, (J) O. brachiata, (K) O. paniculata (subgenus Paniculatae); (L–R) subgenus Olea section Ligustroides: (L) O. schliebenii, (M) O. exasperata, (N) O. capensis subsp. capensis, (O) O. capensis subsp. macrocarpa, (P) O. welwitschii, (Q) O. lancea, (R) O. woodiana; (S–V) subgenus Olea section Olea: (S) O. europaea subsp. europaea, (T) O. europaea subsp. cuspidata, (U) O. europaea subsp. guanchica, (V) O. europaea subsp. laperrinei. Scale bars are 200 µm and 40 µm for the left-hand and right-hand images in each pair, respectively. The scale bar in (V) is 200 µm.
See this image and copyright information in PMC

References

    1. Álvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution. 2003;29:417–434. - PubMed
    1. Angiolillo A, Mencuccini M, Baldoni L. Olive genetic diversity assessed using amplified polymorphic fragment length polymorphisms. Theoretical and Applied Genetics. 1999;98:411–421.
    1. Baldoni L, Guerrero C, Sossey-Alaoui K, Abbott AG, Angiolillo A, Lumaret R. Phylogenetic relationships among Olea species based on nucleotide variation at a non-coding chloroplast DNA region. Plant Biology. 2002;4:346–351.
    1. Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ. The ITS region of nuclear ribosomal DNA. A valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden. 1995;82:247–277.
    1. Besnard G, Khadari B, Villemur P, Bervillé A. Cytoplasmic male sterility in the olive (Olea europaea L.) Theoretical and Applied Genetics. 2000;100:1018–1024.

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