Figure 1 - uploaded by Roberta Piredda
Content may be subject to copyright.
ML tree of the investigated oak accessions. ML tree of plastid accessions; tentatively rooted with the Notholithocarpus-Chrysolepis subtree. Stars indicate subtrees comprising accessions of Mediterranean members of Quercus Group Ilex. Colouration refers to the taxonomic affiliations and main clades of specimens. Number at branches indicate non-parametric bootstrap support under maximum likelihood using two different implementations and posterior probabilities calculated using Bayesian inference.
Source publication
Nucleotide sequences from the plastome are currently the main source for assessing taxonomic and phylogenetic relationships in flowering plants and their historical biogeography at all hierarchical levels. One exception is the large and economically important genus Quercus (oaks). Whereas differentiation patterns of the nuclear genome are in agreem...
Contexts in source publication
Context 1
... of the Mediterranean species of Quercus Group Ilex cluster in three well supported clades (Fig. 1). The first clade ('Euro-Med') accommodates most accessions of Q. ilex and Q. coccifera. In the second clade ('Cerris-Ilex'), accessions of Q. ilex, Q. coccifera, and one of the five samples of Q. aucheri group together with all representatives of Quercus Group Cerris and two Himalayan-East Asian species of Group Ilex. Sister to this ...
Context 2
... polyphyletic is Quercus Group Ilex? Figure 4 highlights the incongruence of the plastid genealogy tree with the current understanding of the evolution of Fagaceae and oaks based on molecular sequence data from Figure 4 Map of chloroplast evolution in oaks. Mapping of chloroplast evolution in oaks (using the same rooting scenario as in Fig. 1) on current evolutionary synopsis (based on nuclear sequence data, morphology, and the fossil record; modified after Grímsson et al. (2015, Fig. 16). Colouring of the plas- tid lineages refers to branches/subclades in Fig. 1: bluish, common (ancestral) and 'New World' oak/cas- tanoids plastid haplotype lineages; green, lineages of the ...
Context 3
... polyphyletic is Quercus Group Ilex? Figure 4 highlights the incongruence of the plastid genealogy tree with the current understanding of the evolution of Fagaceae and oaks based on molecular sequence data from Figure 4 Map of chloroplast evolution in oaks. Mapping of chloroplast evolution in oaks (using the same rooting scenario as in Fig. 1) on current evolutionary synopsis (based on nuclear sequence data, morphology, and the fossil record; modified after Grímsson et al. (2015, Fig. 16). Colouring of the plas- tid lineages refers to branches/subclades in Fig. 1: bluish, common (ancestral) and 'New World' oak/cas- tanoids plastid haplotype lineages; green, lineages of the unique 'Euro-Med' plastid haplotype found only in Mediterranean members of Group Ilex; reddish, lineages of 'Old World' oaks and Eurasian castanoids. ...
Context 4
... 4 Map of chloroplast evolution in oaks. Mapping of chloroplast evolution in oaks (using the same rooting scenario as in Fig. 1) on current evolutionary synopsis (based on nuclear sequence data, morphology, and the fossil record; modified after Grímsson et al. (2015, Fig. 16). Colouring of the plas- tid lineages refers to branches/subclades in Fig. 1: bluish, common (ancestral) and 'New World' oak/cas- tanoids plastid haplotype lineages; green, lineages of the unique 'Euro-Med' plastid haplotype found only in Mediterranean members of Group Ilex; reddish, lineages of 'Old World' oaks and Eurasian castanoids. Note that members of Group Ilex keep plastid haplotypes of five different ...
Context 5
... polyphyletic origin of Quercus Group Ilex or its Mediterranean members is unlikely. Nuclear data covering the entire range of Q. ilex and Q. coccifera in the Mediterranean region unambiguously resolved the two species as close, but mutually monophyletic sister taxa (Denk & Grimm, 2010). The 'non-monophyly' of Group Ilex plastomes seen in the tree (Fig. 1), including haplotypes shared with Group Cerris or closely related to Group Cyclobalanopsis therefore reflects either incomplete lineage sorting or introgression or both. In the absence of nucleome data for all here included individuals, it is impossible to infer to which degree introgression and incomplete lineage sorting contributed ...
Context 6
... the high diversity of haplotypes in Group Ilex as compared to other major oak lineages (or other genera in the Fagales; see Table 3; File S2) it can be hypothesized that the geographical disruptions in the plastome of the ancestors of Group Ilex and interacting lineages predate the manifestation of modern taxa (species and infrageneric groups; Fig. 1). Haplotypes shared between members of Group Ilex and its sister lineages Group Cerris and Group Cyclobalanopsis may indicate the same geographic origin or may be the result of secondary contact and asymmetrical ...
Context 7
... from the actual position of the plastid root (note the scattered placement of putative outgroups in Fig. 1), the divergence of the 'Euro-Med' haplotype must have coincided with the initial differentiation in Quercus (Fig. 1). Oaks had achieved a wide northern hemispheric range by the Eocene. Unequivocal fossils are known from high latitudes (North America, Greenland, North Europe;Crepet & Nixon, 1989;Manchester, 1994;Grímsson et al., 2015) ...
Context 8
... from the actual position of the plastid root (note the scattered placement of putative outgroups in Fig. 1), the divergence of the 'Euro-Med' haplotype must have coincided with the initial differentiation in Quercus (Fig. 1). Oaks had achieved a wide northern hemispheric range by the Eocene. Unequivocal fossils are known from high latitudes (North America, Greenland, North Europe;Crepet & Nixon, 1989;Manchester, 1994;Grímsson et al., 2015) and mid-latitudes (Central Europe, South East Asia; Kvaček & Walther, 1989;Hofmann, 2010). All major lineages of oaks ...
Context 9
... the fossil record and molecular dating using eight nuclear gene regions (Bouchal et al., 2014: Fig. 14;Hubert et al., 2014;Grímsson et al., 2015). During this time, one fraction of oaks, represented by the 'Euro-Med' plastids, must have been geographically and reproductively isolated which would have caused a major split in the plastid gene pool (Fig. 1). Today, the 'Euro-Med' haplotype within Quercus Group Ilex is the only one exclusively shared by just two, but widespread Mediterranean species of Group Ilex, Q. ilex and Q. coccifera. This haplotype is markedly distinct from haplotypes in other oaks or Fagaceae (Fig. 1). Two evolutionary hypotheses could explain the establishment of ...
Context 10
... isolated which would have caused a major split in the plastid gene pool (Fig. 1). Today, the 'Euro-Med' haplotype within Quercus Group Ilex is the only one exclusively shared by just two, but widespread Mediterranean species of Group Ilex, Q. ilex and Q. coccifera. This haplotype is markedly distinct from haplotypes in other oaks or Fagaceae (Fig. 1). Two evolutionary hypotheses could explain the establishment of this unique haplotype in Q. ilex-Q. coccifera (Fig. 5): (i) The 'Euro-Med' haplotype is the remnant of an extinct oak lineage that was intrograded (invaded) and consumed by Figure 5 Origin of the 'Euro-Med' haplotype. Eocene set-up and the origin of the 'Euro-Med' haplo- ...
Context 11
... members of Group Cerris have a much wider range in north-eastern Asia; Menitsky, 2005). Regarding its phylogenetic position, the emergence of the 'Cerris-Ilex' haplotype appears to have been linked with a major taxonomic sorting event in Eurasian Fagaceae, resulting in distinct haplotypes restricted to genera and intrageneric groups of Quercus (Fig. 1). Based on the palaeobotanical record, these lineages (Castanopsis, Castanea, Quercus Group Ilex, Quercus Group Cyclobalanopsis) were well established at least by the Eocene (Table 4 and Fig. 5; Grímsson et al., 2015); a deep divergence is reflected by their distinctly different nuclear genomes Denk & Grimm, 2010;Hubert et al., 2014). ...
Context 12
... The decoupled evolutionary signals in plastomes and the nucleome/morphology as documented for Nothofagus (Acosta & Premoli, 2010;Premoli et al., 2012) and Quercus Group Ilex (this study) suggest that the traditional placeholder sampling strategy is not ideal. Signals from few-marker/many-samples data sets are likely to be complex or even puzzling (Figs. 1-4), but at the same time provide entirely new perspectives on plant evolution worth exploring. For Quercus Group Ilex, our pilot study focussing on Mediterranean species reveals a crucial aspect of oak evolution not seen in the combined nuclear, morphological, and fossil data: large-scale introgression and/or incomplete lineage sorting ...
Context 13
... within modern members of Group Cerris, a wide spectrum of leaf traits is found from pseudo-evergreen in Q. suber, to semi-evergreen in Q. brantii, Q. ithaburensis, Q. trojana (partly) and fully deciduous in Q. acutissima, Q. castaneifolia, Q. cerris, Q. libani and Q. variabilis. The conspicuous plastid diversity in the Mediterranean species of Group Ilex and the lineage in general ( Figs. 1 and 2; Table 2) can only be interpreted as reflecting the highly complex geographical history of this group, due to growing geographic isolation between clades from the Oligocene onwards. The 'Euro-Med' haplotype evidences an initial phase of geographic differentiation predating the formation of modern lineages, but its origin and evolutionary significance remain enigmatic (Fig. 5). ...
Citations
... Species of section Ilex are widely distributed in Eurasian low-middle latitude habitats comprising ca. 35-36 species (Denk and Grimm, 2010;Simeone et al., 2016). Unfortunately, the wide range of EBLFs in East Asia is now greatly diminished as a result of intensified human activities (Cao and Zhang, 1997;Tang, 2010). ...
... In this study, various cpDNA haplotypes exist within a species and some of these haplotypes are shared interspecifically. Recent phylogeographic studies of the section Ilex from the Himalayas (Feng et al., 2016;Meng et al., 2017) and the pan-Mediterranean (Simeone et al., 2016;Vitelli et al., 2017) also showed similar scenario. Moreover, even using the complete plastid genome sequences for phylogenetic reconstruction, the monophyletic status of species was still rare in section Quercus (Pham et al., 2017). ...
... We found that the evolutionary history of the chloroplast genome is net-like rather than dichotomous, which hinders the discriminatory ability to infer the species tree using these maternal markers, especially in a frequent-hybridized taxa (Hollingsworth et al., 2011;Coissac et al., 2016). Moreover, driven by the peculiar paleogeographical histories of the studied regions, plastid genome may reveal geographic differentiation or distribution range of the ancestral lineage instead of the true species phylogeny (Petit et al., 2002;Gugger and Cavender-Bares, 2013;Simeone et al., 2016;Pham et al., 2017;Vitelli et al., 2017). Eurasian evergreen oaks also have strong cpDNA genetic differentiation across different geographical regions instead of species taxonomy. ...
The East Asian subtropics mostly occupied by evergreen broad-leaved forests (EBLFs), is one of the global diversity centers for evergreen oaks. Evergreen oaks are keystone canopy trees in EBLFs with important ecosystem function and crucial significance for regional biodiversity conservation. However, the species composition and diversity of Asian evergreen oaks are poorly understood. Here, we test whether the four chloroplast markers atpI-atpH, matK, psbA-trnH, and ycf1, can discriminate the two evergreen oak sections in Asia – Cyclobalanopsis and Ilex. Two hundred and seventy-two individuals representing 57 species were scanned and 17 species from other oaks sections were included for phylogenetic reconstruction. The genetic diversity of the Quercus sections was also compared. Overall, we found that universal chloroplast DNA (cpDNA) barcoding markers could resolve two clades in Quercus, i.e., subgenus Cerris (Old World Clade) and subgenus Quercus (New World Clade). The chloroplast markers distinguished the main sections, with few exceptions. Each cpDNA region showed no barcoding gap and none of them provided good resolution at the species level. The best species resolution (27.78%) was obtained when three or four markers were combined and analyzed using BLAST. The high conservation of the cpDNA and complicated evolutionary patterns, due to incomplete lineage sorting, interspecific hybridization and introgressions may hinder the ability of cpDNA markers to discriminate different species. When comparing diversification pattern across Quercus sections (Cyclobalanopsis, Ilex, Cerris, Quercus, and Protobalanus), we found that section Ilex was the most genetically diverse, and section Cyclobalanopsis was lower genetically diverse. This diversification pattern may have resulted from the interplay of the Eurasia Cenozoic tectonic movements, climate changes and different niches of their ancestral lineages.
... Similarity in the biparentally-inherited nucleome is taken as indication that two or more taxa are closely related in an evolutionary sense, and have not been isolated for a long time. It has been shown that in densely sampled, sympatric oak species speciation processes directly affect the nucleome, but not the plastome[51][52][53][54][55]. Two closely related species are more likely to hybridize and introgress, which will eventually lead to a homogenization of the nucleome but not necessarily of the plastome. ...
... Quercus coccifera and Q. ilex[54,56]). Thus, nuclear data will more likely reflect the (current) systematic affinity of an individual or species, whereas plastid data may reflect the provenance of the (mother) population (e.g.[55,56]for oaks, and[57,58]for Nothofagaceae). The simplest explanation for the geographic distribution of nuclear and plastid lineages (Fig. 4) is that an originally South Asian-Indomalayan sister lineage (orange) of the exclusively Philippine lineage (red), migrated or expanded into the southern Pacific area, possibly in response to the expansion of earlier diverged other Ixora in that region (green and purple members of the African-Asian clade). ...
Background
The Philippine archipelago is globally one of the most important model island systems for studying evolutionary processes. However, most plant species on this archipelago have not yet been studied in sufficient detail. The main aim of this study is to unravel the evolutionary history and biogeographic relationships of the Philippine members of the pantropical genus Ixora.
Results
The complex plastid and nuclear divergence patterns in Philippine Ixora, documented using tree and network approaches, reveal a highly dynamic evolution in Ixora, involving several phases of radiation and recolonization. Philippine Ixora comprises at least five lineages, of which one is most closely related to species from Wallacea, and the remaining four to species from Asia.
Conclusions
Our study highlights the importance of Philippine species for understanding phytogeographic patterns in the Indomalayan-Australasian eco-region. The overall genetic differentiation, as well as the incongruence between genealogies based on the biparentally inherited nucleome and the maternally inherited plastome in Ixora, reflect the complex tectonic history of the Philippine archipelago. The Ixora lineage related to Wallacean species supports the delimitation of different ecozones along Huxley’s line, because it is absent from Palawan. The remaining four lineages are all allied with Asian taxa, reflecting several waves of colonization. Close relationships between some widespread Philippine species and locally adapted narrow endemics suggest that the widespread, genetically diverse species act as pools for the formation of new species in a process of ongoing speciation. Our results suggest that the species concepts of some of the more widespread taxa need to be revised.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-017-0974-3) contains supplementary material, which is available to authorized users.
... Thus, further efforts to standardize the current terminology of leaf epidermal features in oaks are essential for comparing the published data. Quercus Group Ilex, also known as Eurasian sclerophyllous oaks, with about 30–37 species (Simeone et al., 2016), has been treated as subgenus Heterobalanus in Menitsky's (1984) classification system. Its distribution displays a more or less continuous range in Eurasia with higher ecological and taxonomic diversity in the Himalayas and adjacent areas (Zhou, 1992; Denk and Grimm, 2010). ...
... Quercus spinosa and Q. floribunda have both capitate and branched uniseriate trichomes. The phylogenetic reconstruction based on chloroplast DNA sequences indicates that Q. spinosa clusters with Mediterranean species while Q. floribunda clusters with Himalayan species (Simeone et al., 2016). The co-existence of the two trichome types might suggest a possible ancestral status. ...
... Further efforts to supplement the leaf epidermal features of fossils are crucial to improve the accuracy of assigning them to extant closely related species. The widely shared cpDNA haplotypes among the Eurasian forms of Group Ilex did not reveal species identity, but these cpDNA haplotypes show a strong phylogeographical structure, which suggests that possible ancient hybridization and genetic assimilation occurred in ancestral lineages (Simeone et al., 2016). Hipp et al.'s (2015works inferred the phylogenetic framework of Group Ilex, but still about half of the species in Group Ilex have not yet been investigated . ...
Leaf epidermal features are useful for elucidating the taxonomy and systematics of oak species. Quercus Group Ilex has a wide distribution mainly in subtropical areas of Eurasia with rich fossil records since the Oligocene, but no comprehensive study has ever been conducted on its diversity of leaf epidermal features. We compared the leaf epidermal features of 37 species of Quercus Group Ilex and Q. suber from Group Cerris using light microscopy (LM) and scanning electron microscopy (SEM). A total of five trichome types (including three glandular and two non-glandular types) and two trichome base types were found. Leaf epidermal features of Group Ilex show typical xeromorphic features. The stomatal complexes are stephanocytic. The leaf trichome types and trichome base types are stable at inter- and intra-species levels. The trichomes, stomatal sizes and density and the ray arm lengths show a wide variation during developing stages within species. The leaf epidermal features show a highly convergent pattern in the genus Quercus based on tree-mapping analysis, except for the multiple epidermal layers on the adaxial surface supports the monophyletic origin of section Heterobalanus. Cluster analysis of leaf epidermal characters infers two morphological subgroups within Group Ilex: (1) the capitate and (2) the branched uniseriate. The trichomes and trichome base types, and their density are useful for species identification, which can improve the accuracy of assigning fossil leaves to their nearest living relatives in Group Ilex.
... Our results indicated that the haplotypes N2, N3, and N5 shared among species are ancient and have disjunctive distribution (Figure S1B), and shared haplotypes C2, C4, C6, C20, and N6 between sympatric species (Figure 1and Figure S1B) as expected for incomplete lineage sorting (Maddison and Knowles, 2006) and introgressive hybridization, respectively. Generally, numerous studies have revealed shared DNA polymorphisms between closely related species or species complex (e.g., Du et al., 2009; Simeone et al., 2016). This situation can be divided into two categories: firstly, retention of ancestral polymorphisms which caused by incomplete lineage sorting during and following speciation (Heckman et al., 2007; Wilyard et al., 2009); secondly, introgression or introgressive hybridization which caused by genetic exchange after secondary contact between previously geographically separated species (Liston et al., 1999; Gay et al., 2007). ...
The East Himalaya-Hengduan Mountains (EH-HM) region has a high biodiversity and harbors numerous endemic alpine plants. This is probably the result of combined orographic and climate oscillations occurring since late Tertiary. Here, we determined the genetic structure and evolutionary history of alpine oak species (including Quercus spinosa, Quercus aquifolioides, and Quercus rehderiana) using both cytoplasmic-nuclear markers and ecological niche models (ENMs), and elucidated the impacts of climate oscillations and environmental heterogeneity on their population demography. Our results indicate there were mixed genetic structure and asymmetric contemporary gene flow within them. The ENMs revealed a similar demographic history for the three species expanded their ranges from the last interglacial (LIG) to the last glacial maximum (LGM), which was consistent with effective population sizes changes. Effects of genetic drift and fragmentation of habitats were responsible for the high differentiation and the lack of phylogeographic structure. Our results support that geological and climatic factors since Miocene triggered the differentiation, evolutionary origin and range shifts of the three oak species in the studied area and also emphasize that a multidisciplinary approach combining molecular markers, ENMs and population genetics can yield deep insights into diversification and evolutionary dynamics of species.
Shared ancestral polymorphism and introgression are two main causes of chloroplast DNA (cpDNA) haplotype sharing among closely related angiosperms. In this study, we explored the roles of these two processes in shaping the phylogeographic patterns of East Asian Cerris oaks by examining the geographic distributions of randomly and locally distributed shared haplotypes, which coincide with the expectations of shared ancestry and introgression, respectively. We sequenced 1340 bp of non-coding cpDNA from Quercus acutissima (n = 418) and Q. chenii (n = 183) and compiled previously published sequence data of Q. variabilis (n = 439). The phylogenetic relationships among haplotypes were examined using a median-joining network. The geographic patterns of interspecifically shared haplotypes were assessed to test whether nearby populations have a higher degree of interspecific cpDNA sharing than distant ones. We identified a total of 27 haplotypes that were grouped into three non-species-specific lineages with overlapping distributions. Ancestral haplotypes were extensively shared and randomly distributed across populations of the three species. Some young haplotypes were locally shared in mountainous areas that may have been shared refugia. The local exchange of cpDNA resulted in an excess of similar haplotypes between nearby populations. Our study demonstrated that the haplotype sharing pattern among East Asian Cerris oaks reflected the imprints of both shared ancestral polymorphism and introgression. This pattern was also associated with the relatively stable climates and complex landscapes in East Asia, which not only allowed the long-term persistence of ancestral lineages but also connected the survived populations across refugia.
Japanese oak wilt disease is caused by fungi, which are brought by Platypus quercivorus into the trunk, hinder water supply by filling vessels with its hyphae and then weaken/kill trees. To evaluate the regeneration of Quercus phillyraeoides stands damaged by Japanese oak wilt disease by cutting survived trees, we investigated the effects of infection and gallery formation by P. quercivorus on sprouting success of Q. phillyraeoides. We investigated gallery density and the proportion of xylem discoloration of stumps, and evaluated the sprouting success 1 year and more than 5 years after cutting in two stands in Wakayama Prefecture, Japan. Although there were no significant effects of gallery formation on individual-level mortality rates both 1 or more than 5 years after cutting, the individual-level mortality rate more than 5 years after cutting was larger than that 1 year after cutting. Moreover, there were no significant effects of gallery formation on number and size of sprouts both 1 or more than 5 years after cutting. The number of sprouts 1 year after cutting decreased as increasing in the gallery density. However, gallery density and the ratio of xylem discoloration were positively correlated with stump diameter, which is known to be one of the factors decreasing the sprouting success of Q. phillyraeoides. Therefore, we were not be able to quantify the net effect of the gallery formation on sprouting success of Q. phillyraeoides. In summary, cutting of survived trees of Q. phillyraeoides after attacks of P. quercivorus contributes to regeneration of the stand by sprouting, because most individuals can survive and generate sprouts.
