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1.  The ancient tropical rainforest tree Symphonia globulifera L. f. (Clusiaceae) was not restricted to postulated Pleistocene refugia in Atlantic Equatorial Africa 
Heredity  2013;111(1):66-76.
Understanding the history of forests and their species' demographic responses to past disturbances is important for predicting impacts of future environmental changes. Tropical rainforests of the Guineo-Congolian region in Central Africa are believed to have survived the Pleistocene glacial periods in a few major refugia, essentially centred on mountainous regions close to the Atlantic Ocean. We tested this hypothesis by investigating the phylogeographic structure of a widespread, ancient rainforest tree species, Symphonia globulifera L. f. (Clusiaceae), using plastid DNA sequences (chloroplast DNA [cpDNA], psbA-trnH intergenic spacer) and nuclear microsatellites (simple sequence repeats, SSRs). SSRs identified four gene pools located in Benin, West Cameroon, South Cameroon and Gabon, and São Tomé. This structure was also apparent at cpDNA. Approximate Bayesian Computation detected recent bottlenecks approximately dated to the last glacial maximum in Benin, West Cameroon and São Tomé, and an older bottleneck in South Cameroon and Gabon, suggesting a genetic effect of Pleistocene cycles of forest contraction. CpDNA haplotype distribution indicated wide-ranging long-term persistence of S. globulifera both inside and outside of postulated forest refugia. Pollen flow was four times greater than that of seed in South Cameroon and Gabon, which probably enabled rapid population recovery after bottlenecks. Furthermore, our study suggested ecotypic differentiation—coastal or swamp vs terra firme—in S. globulifera. Comparison with other tree phylogeographic studies in Central Africa highlighted the relevance of species-specific responses to environmental change in forest trees.
PMCID: PMC3692313  PMID: 23572126
forest refuge theory; phylogeography; psbA-trnH; SSR; tropical Africa; approximate bayesian computation
2.  Genetic and palaeo-climatic evidence for widespread persistence of the coastal tree species Eucalyptus gomphocephala (Myrtaceae) during the Last Glacial Maximum 
Annals of Botany  2013;113(1):55-67.
Background and Aims
Few phylogeographic studies have been undertaken of species confined to narrow, linear coastal systems where past sea level and geomorphological changes may have had a profound effect on species population sizes and distributions. In this study, a phylogeographic analysis was conducted of Eucalyptus gomphocephala (tuart), a tree species restricted to a 400 × 10 km band of coastal sand-plain in south west Australia. Here, there is little known about the response of coastal vegetation to glacial/interglacial climate change, and a test was made as to whether this species was likely to have persisted widely through the Last Glacial Maximum (LGM), or conforms to a post-LGM dispersal model of recovery from few refugia.
The genetic structure over the entire range of tuart was assessed using seven nuclear (21 populations; n = 595) and four chloroplast (24 populations; n = 238) microsatellite markers designed for eucalypt species. Correlative palaeodistribution modelling was also conducted based on five climatic variables, within two LGM models.
Key Results
The chloroplast markers generated six haplotypes, which were strongly geographically structured (GST = 0·86 and RST = 0·75). Nuclear microsatellite diversity was high (overall mean HE 0·75) and uniformly distributed (FST = 0·05), with a strong pattern of isolation by distance (r2 = 0·362, P = 0·001). Distribution models of E. gomphocephala during the LGM showed a wide distribution that extended at least 30 km westward from the current distribution to the palaeo-coastline.
The chloroplast and nuclear data suggest wide persistence of E. gomphocephala during the LGM. Palaeodistribution modelling supports the conclusions drawn from genetic data and indicates a widespread westward shift of E. gomphocephala onto the exposed continental shelf during the LGM. This study highlights the importance of the inclusion of complementary, non-genetic data (information on geomorphology and palaeoclimate) to interpret phylogeographic patterns.
PMCID: PMC3864724  PMID: 24284819
Australian biogeography; climate change; coastal geomorphology; Eucalyptus gomphocephala; founder effects; Last Glacial Maximum; LGM; microsatellites; Myrtaceae; palaeodistribution modelling; phylogeography; southern hemisphere; south-western Australia; tuart
3.  Comparative molecular cytogenetics of major repetitive sequence families of three Dendrobium species (Orchidaceae) from Bangladesh 
Annals of Botany  2009;104(5):863-872.
Background and Aims
Dendrobium species show tremendous morphological diversity and have broad geographical distribution. As repetitive sequence analysis is a useful tool to investigate the evolution of chromosomes and genomes, the aim of the present study was the characterization of repetitive sequences from Dendrobium moschatum for comparative molecular and cytogenetic studies in the related species Dendrobium aphyllum, Dendrobium aggregatum and representatives from other orchid genera.
In order to isolate highly repetitive sequences, a c0t-1 DNA plasmid library was established. Repeats were sequenced and used as probes for Southern hybridization. Sequence divergence was analysed using bioinformatic tools. Repetitive sequences were localized along orchid chromosomes by fluorescence in situ hybridization (FISH).
Key Results
Characterization of the c0t-1 library resulted in the detection of repetitive sequences including the (GA)n dinucleotide DmoO11, numerous Arabidopsis-like telomeric repeats and the highly amplified dispersed repeat DmoF14. The DmoF14 repeat is conserved in six Dendrobium species but diversified in representative species of three other orchid genera. FISH analyses showed the genome-wide distribution of DmoF14 in D. moschatum, D. aphyllum and D. aggregatum. Hybridization with the telomeric repeats demonstrated Arabidopsis-like telomeres at the chromosome ends of Dendrobium species. However, FISH using the telomeric probe revealed two pairs of chromosomes with strong intercalary signals in D. aphyllum. FISH showed the terminal position of 5S and 18S–5·8S–25S rRNA genes and a characteristic number of rDNA sites in the three Dendrobium species.
The repeated sequences isolated from D. moschatum c0t-1 DNA constitute major DNA families of the D. moschatum, D. aphyllum and D. aggregatum genomes with DmoF14 representing an ancient component of orchid genomes. Large intercalary telomere-like arrays suggest chromosomal rearrangements in D. aphyllum while the number and localization of rRNA genes as well as the species-specific distribution pattern of an abundant microsatellite reflect the genomic diversity of the three Dendrobium species.
PMCID: PMC2749531  PMID: 19635741
Orchidaceae; Dendrobium moschatum; Dendrobium aphyllum; Dendrobium aggregatum; repetitive DNA; FISH; c0t-1 DNA
4.  Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor 
At the last glacial maximum, Fennoscandia was covered by an ice sheet while the tundra occupied most of the rest of northern Eurasia. More or less disjunct refugial populations of plants were dispersed in southern Europe, often trapped between mountain ranges and seas. Genetic and paleobotanical evidences indicate that these populations have contributed much to Holocene recolonization of more northern latitudes. Less supportive evidence has been found for the existence of glacial populations located closer to the ice margin. Scots pine (Pinus sylvestris L.) is a nordic conifer with a wide natural range covering much of Eurasia. Fractures in its extant genetic structure might be indicative of glacial vicariance and how different refugia contributed to the current distribution at the continental level. The population structure of Scots pine was investigated on much of its Eurasian natural range using maternally inherited mitochondrial DNA polymorphisms.
A novel polymorphic region of the Scots pine mitochondrial genome has been identified, the intron 1 of nad7, with three variants caused by insertions-deletions. From 986 trees distributed among 54 populations, four distinct multi-locus mitochondrial haplotypes (mitotypes) were detected based on the three nad7 intron 1 haplotypes and two previously reported size variants for nad1 intron B/C. Population differentiation was high (GST = 0.657) and the distribution of the mitotypes was geographically highly structured, suggesting at least four genetically distinct ancestral lineages. A cosmopolitan lineage was widely distributed in much of Europe throughout eastern Asia. A previously reported lineage limited to the Iberian Peninsula was confirmed. A new geographically restricted lineage was found confined to Asia Minor. A new lineage was restricted to more northern latitudes in northeastern Europe and the Baltic region.
The contribution of the various ancestral lineages to the current distribution of Scots pine was asymmetric and extant endemism reflected the presence of large geographic barriers to migration. The results suggest a complex biogeographical history with glacial refugia shared with temperate plant species in southern European Peninsulas and Asia Minor, and a genetically distinct glacial population located more North. These results confirm recent observations for cold tolerant species about the possible existence of refugial populations at mid-northern latitudes contributing significantly to the recolonization of northern Europe. Thus, Eurasian populations of nordic plant species might not be as genetically homogenous as assumed by simply considering them as offsets of glacial populations located in southern peninsulas. As such, they might have evolved distinctive genetic adaptations during glacial vicariance, worth evaluating and considering for conservation.
PMCID: PMC2222255  PMID: 18034901
5.  Pushed to the limit: consequences of climate change for the Araucariaceae: a relictual rain forest family 
Annals of Botany  2011;108(2):347-357.
Background and Aims
Under predicted climate change scenarios, increased temperatures are likely to predispose trees to leaf and other tissue damage, resulting in plant death and contraction of already narrow distribution ranges in many relictual species. The effects of predicted upward temperatures may be further exacerbated by changes in rainfall patterns and damage caused by frosts on trees that have been insufficiently cold-hardened. The Araucariaceae is a relictual family and the seven species found in Australia have limited natural distributions characterized by low frost intensity and frequency, and warm summer temperatures. The temperature limits for these species were determined in order to help understand how such species will fare in a changing climate.
Experiments were conducted using samples from representative trees of the Araucariaceae species occurring in Australia, Agathis (A. atropurpurea, A. microstachya and A. robusta), Arauacaria (A. bidwilli, A. cunninghamii and A. heterophylla) and Wollemia nobilis. Samples were collected from plants grown in a common garden environment. Lower and higher temperature limits were determined by subjecting detached winter-hardened leaves to temperatures from 0 to –17 °C and summer-exposed leaves to 25 to 63 °C, then measuring the efficiency of photosystem II (Fv/Fm) and visually rating leaf damage. The exotherm, a sharp rise in temperature indicating the point of ice nucleation within the cells of the leaf, was measured on detached leaves of winter-hardened and summer temperature-exposed leaves.
Key Results
Lower temperature limits (indicated by FT50, the temperature at which PSII efficiency is 50 %, and LT50 the temperature at which 50 % visual leaf damage occurred) were approx. –5·5 to –7·5 °C for A. atropurpurea, A. microstachya and A. heterophylla, approx. –7 to –9 °C for A. robusta, A. bidwillii and A. cunninghamii, and –10·5 to –11 °C for W. nobilis. High temperature damage began at 47·5 °C for W. nobilis, and occurred in the range 48·5–52 °C for A. bidwillii and A. cunninghamii, and in the range 50·5–53·5 °C for A. robusta, A. microstachya and A. heterophylla. Winter-hardened leaves had ice nucleation temperatures of –5·5 °C or lower, with W. nobilis the lowest at –6·8 °C. All species had significantly higher ice nucleation temperatures in summer, with A. atropurpurea and A. heterophylla forming ice in the leaf at temperatures >3 °C higher in summer than in winter. Wollemia nobilis had lower FT50 and LT50 values than its ice nucleation temperature, indicating that the species has a degree of ice tolerance.
While lower temperature limits in the Australian Araucariaceae are generally unlikely to affect their survival in wild populations during normal winters, unseasonal frosts may have devastating effects on tree survival. Extreme high temperatures are not common in the areas of natural occurrence, but upward temperature shifts, in combination with localized radiant heating, may increase the heat experienced within a canopy by at least 10 °C and impact on tree survival, and may contribute to range contraction. Heat stress may explain why many landscape plantings of W. nobilis have failed in hotter areas of Australia.
PMCID: PMC3143045  PMID: 21727080
Hardiness; frost; high temperature; climate change; Araucariaceae; rain forest
6.  Landscape Patterns in Rainforest Phylogenetic Signal: Isolated Islands of Refugia or Structured Continental Distributions? 
PLoS ONE  2013;8(12):e80685.
Identify patterns of change in species distributions, diversity, concentrations of evolutionary history, and assembly of Australian rainforests.
We used the distribution records of all known rainforest woody species in Australia across their full continental extent. These were analysed using measures of species richness, phylogenetic diversity (PD), phylogenetic endemism (PE) and phylogenetic structure (net relatedness index; NRI). Phylogenetic structure was assessed using both continental and regional species pools. To test the influence of growth-form, freestanding and climbing plants were analysed independently, and in combination.
Species richness decreased along two generally orthogonal continental axes, corresponding with wet to seasonally dry and tropical to temperate habitats. The PE analyses identified four main areas of substantially restricted phylogenetic diversity, including parts of Cape York, Wet Tropics, Border Ranges, and Tasmania. The continental pool NRI results showed evenness (species less related than expected by chance) in groups of grid cells in coastally aligned areas of species rich tropical and sub-tropical rainforest, and in low diversity moist forest areas in the south-east of the Great Dividing Range and in Tasmania. Monsoon and drier vine forests, and moist forests inland from upland refugia showed phylogenetic clustering, reflecting lower diversity and more relatedness. Signals for evenness in Tasmania and clustering in northern monsoon forests weakened in analyses using regional species pools. For climbing plants, values for NRI by grid cell showed strong spatial structuring, with high diversity and PE concentrated in moist tropical and subtropical regions.
Concentrations of rainforest evolutionary history (phylo-diversity) were patchily distributed within a continuum of species distributions. Contrasting with previous concepts of rainforest community distribution, our findings of continuous distributions and continental connectivity have significant implications for interpreting rainforest evolutionary history and current day ecological processes, and for managing rainforest diversity in changing circumstances.
PMCID: PMC3846590  PMID: 24312493
7.  The impact of Pleistocene climate change on an ancient arctic–alpine plant: multiple lineages of disparate history in Oxyria digyna 
Ecology and Evolution  2012;2(3):649-665.
The ranges of arctic–alpine species have shifted extensively with Pleistocene climate changes and glaciations. Using sequence data from the trnH-psbA and trnT-trnL chloroplast DNA spacer regions, we investigated the phylogeography of the widespread, ancient (>3 million years) arctic–alpine plant Oxyria digyna (Polygonaceae). We identified 45 haplotypes and six highly divergent major lineages; estimated ages of these lineages (time to most recent common ancestor, TMRCA) ranged from ∼0.5 to 2.5 million years. One lineage is widespread in the arctic, a second is restricted to the southern Rocky Mountains of the western United States, and a third was found only in the Himalayan and Altai regions of Asia. Three other lineages are widespread in western North America, where they overlap extensively. The high genetic diversity and the presence of divergent major cpDNA lineages within Oxyria digyna reflect its age and suggest that it was widespread during much of its history. The distributions of individual lineages indicate repeated spread of Oxyria digyna through North America over multiple glacial cycles. During the Last Glacial Maximum it persisted in multiple refugia in western North America, including Beringia, south of the continental ice, and within the northern limits of the Cordilleran ice sheet. Our data contribute to a growing body of evidence that arctic–alpine species have migrated from different source regions over multiple glacial cycles and that cryptic refugia contributed to persistence through the Last Glacial Maximum.
PMCID: PMC3399151  PMID: 22822441
Arctic-alpine plants; cpDNA; phylogeography; Pleistocene glaciations; refugia
8.  Comparative phylogeography of two related plant species with overlapping ranges in Europe, and the potential effects of climate change on their intraspecific genetic diversity 
The aim of the present study was to use a combined phylogeographic and species distribution modelling approach to compare the glacial histories of two plant species with overlapping distributions, Orthilia secunda (one-sided wintergreen) and Monotropa hypopitys (yellow bird's nest). Phylogeographic analysis was carried out to determine the distribution of genetic variation across the range of each species and to test whether both correspond to the "classic" model of high diversity in the south, with decreasing diversity at higher latitudes, or whether the cold-adapted O. secunda might retain more genetic variation in northern populations. In addition, projected species distributions based on a future climate scenario were modelled to assess how changes in the species ranges might impact on total intraspecific diversity in both cases.
Palaeodistribution modelling and phylogeographic analysis using multiple genetic markers (chloroplast trnS-trnG region, nuclear ITS and microsatellites for O. secunda; chloroplast rps2, nuclear ITS and microsatellites for M. hypopitys) indicated that both species persisted throughout the Last Glacial Maximum in southern refugia. For both species, the majority of the genetic diversity was concentrated in these southerly populations, whereas those in recolonized areas generally exhibited lower levels of diversity, particularly in M. hypopitys. Species distribution modelling based on projected future climate indicated substantial changes in the ranges of both species, with a loss of southern and central populations, and a potential northward expansion for the temperate M. hypopitys.
Both Orthilia secunda and Monotropa hypopitys appear to have persisted through the LGM in Europe in southern refugia. The boreal O. secunda, however, has retained a larger proportion of its genetic diversity in more northerly populations outside these refugial areas than the temperate M. hypopitys. Given that future species distribution modelling suggests northern range shifts and loss of suitable habitat in the southern parts of the species' current distributions, extinction of genetically diverse rear edge populations could have a significant effect in the rangewide intraspecific diversity of both species, but particularly in M. hypopitys.
PMCID: PMC3038166  PMID: 21272309
9.  Past climate changes explain the phylogeography of Vitellaria paradoxa over Africa 
Heredity  2011;107(2):174-186.
The evolution of the savanna biome has been deeply marked by repeated contraction/expansion phases due to climate perturbations during the Quaternary period. In this study, we investigated the impact of the last glacial maximum (LGM) on the present genetic pattern of Vitellaria paradoxa (shea tree), a major African savanna tree. A range-wide sampling of the species enabled us to sample 374 individuals from 71 populations distributed throughout sub-Sahelian Africa. Trees were genotyped using 3 chloroplasts and 12 nuclear microsatellites, and were sequenced for 2 polymorphic chloroplast intergenic spacers. Analyses of genetic diversity and structure were based on frequency-based and Bayesian methods. Potential distributions of V. paradoxa at present, during the LGM and the last interglacial period, were examined using DIVA-GIS ecological niche modelling (ENM). Haplotypic and allelic richness varied significantly across the range according to chloroplast and nuclear microsatellites, which pointed to higher diversity in West Africa. A high but contrasted level of differentiation was revealed among populations with a clear phylogeographic signal, with both nuclear (FST=0.21; RST=0.28; RST>RST (permuted)) and chloroplast simple sequence repeats (SSRs) (GST=0.81; NST=0.90; NST>NST (permuted)). We identified a strong geographically related structure separating western and eastern populations, and a substructure in the eastern part of the area consistent with subspecies distinction. Using ENM, we deduced that perturbations during the LGM fragmented the potential eastern distribution of shea tree, but not its distribution in West Africa. Our main results suggest that climate variations are the major factor explaining the genetic pattern of V. paradoxa.
PMCID: PMC3178399  PMID: 21407253
intergenic spacers; microsatellite markers; last glacial maximum; phylogeography; sub-Sahelian Africa; Vitellaria paradoxa
10.  Nuclear DNA Microsatellites Reveal Genetic Variation but a Lack of Phylogeographical Structure in an Endangered Species, Fraxinus mandshurica, Across North-east China 
Annals of Botany  2008;102(2):195-205.
Background and Aims
The widely accepted paradigm that the modern genetic structure of plant species in the northern hemisphere has been largely determined by recolonization from refugia after the last glacial maximum fails to explain the presence of cold-tolerant species at intermediate latitudes. Another generally accepted paradigm is that mountain ridges act as important barriers causing genetic isolation of species, but this too has been challenged in recent studies. The aims of the work reported here were to determine the genetic diversity and distribution patterns of extant natural populations of an endangered cool temperate species, Faxinus mandshurica, and to examine whether these two paradigms are appropriate when applied to this species over a wide geographical scale.
1435 adult individuals were sampled from 30 natural populations across the main and central range of the species, covering major mountain ranges across North-east China (NEC). Genetic variation was estimated based on nine polymorphic nuclear microsatellite loci. Phylogeographical analyses were employed using various approaches, including Bayesian clustering, spatial analysis of molecular variance, Monmonier's algorithm, neighbor-joining trees, principal co-ordinate analysis and isolation by distance.
Key Results
Genetic diversity within populations was relatively high, and no significant recent bottlenecks were detected in any of the populations. A significant negative correlation between intra-population genetic diversity and latitude was identified. In contrast, genetic differentiation among all the populations examined was extremely low and no clear geographic genetic structure was identified, with the exception of one distinct population.
The modern genetic structure in this species can be explained by extensive gene flow, an absence of mountains acting as barriers, and the presence of a wide refuge across NEC rather than multiple small refugia. Intra-population genetic variation along latitudes is probably associated with the systematically northward shifts of forest biomes in eastern China during the mid-Holocene. To determine important genetic patterns and identify resources for conservation, however, it will be necessary to examine differentially inherited genetic markers exposed to selection pressures (e.g. chloroplast DNA) and to investigate different generations.
PMCID: PMC2712365  PMID: 18477559
Fraxinus mandshurica; nuclear microsatellites; latitude variation; historical migration; fossil pollen; spatial genetic structure; genetic barriers
11.  Integrative taxonomy resolves the cryptic and pseudo-cryptic Radula buccinifera complex (Porellales, Jungermanniopsida), including two reinstated and five new species 
PhytoKeys  2013;1-113.
Molecular data from three chloroplast markers resolve individuals attributable to Radula buccinifera in six lineages belonging to two subgenera, indicating the species is polyphyletic as currently circumscribed. All lineages are morphologically diagnosable, but one pair exhibits such morphological overlap that they can be considered cryptic. Molecular and morphological data justify the re-instatement of a broadly circumscribed ecologically variable R. strangulata, of R. mittenii, and the description of five new species. Two species Radula mittenii Steph. and R. notabilis sp. nov. are endemic to the Wet Tropics Bioregion of north-east Queensland, suggesting high diversity and high endemism might characterise the bryoflora of this relatively isolated wet-tropical region. Radula demissa sp. nov. is endemic to southern temperate Australasia, and like R. strangulata occurs on both sides of the Tasman Sea. Radula imposita sp. nov. is a twig and leaf epiphyte found in association with waterways in New South Wales and Queensland. Another species, R. pugioniformis sp. nov., has been confused with Radula buccinifera but was not included in the molecular phylogeny. Morphological data suggest it may belong to subg. Odontoradula. Radula buccinifera is endemic to Australia including Western Australia and Tasmania, and to date is known from south of the Clarence River on the north coast of New South Wales. Nested within R. buccinifera is a morphologically distinct plant from Norfolk Island described as R. anisotoma sp. nov. Radula australiana is resolved as monophyletic, sister to a species occurring in east coast Australian rainforests, and nesting among the R. buccinifera lineages with strong support. The molecular phylogeny suggests several long-distance dispersal events may have occurred. These include two east-west dispersal events from New Zealand to Tasmania and south-east Australia in R. strangulata, one east-west dispersal event from Tasmania to Western Australia in R. buccinifera, and at least one west-east dispersal from Australia to New Zealand in R. australiana. Another west-east dispersal event from Australia to Norfolk Island may have led to the budding speciation of R. anisotoma. In contrast, Radula demissa is phylogeographically subdivided into strongly supported clades either side of the Tasman Sea, suggesting long distance dispersal is infrequent in this species.
PMCID: PMC3821098  PMID: 24223490
Radulaceae; Radula subg. Metaradula; Radula anisotoma; Radula australiana; Radula buccinifera; Radula demissa; Radula imposita; Radula mittenii; Radula notabilis; Radula pugioniformis; Radula strangulata; sp. nov.; morphology; DNA sequence data; Australia; New Zealand; Flora; liverwort; dispersal; biogeography; cryptic species
12.  A strong ‘filter’ effect of the East China Sea land bridge for East Asia’s temperate plant species: inferences from molecular phylogeography and ecological niche modelling of Platycrater arguta (Hydrangeaceae) 
In East Asia, an increasing number of studies on temperate forest tree species find evidence for migration and gene exchange across the East China Sea (ECS) land bridge up until the last glacial maximum (LGM). However, it is less clear when and how lineages diverged in this region, whether in full isolation or in the face of post-divergence gene flow. Here, we investigate the effects of Quaternary changes in climate and sea level on the evolutionary and demographic history of Platycrater arguta, a rare temperate understorey shrub with disjunct distributions in East China (var. sinensis) and South Japan (var. arguta). Molecular data were obtained from 14 P. arguta populations to infer current patterns of molecular structure and diversity in relation to past (Last Interglacial and Last Glacial Maximum) and present distributions based on ecological niche modelling (ENM). A coalescent-based isolation-with-migration (IM) model was used to estimate lineage divergence times and population demographic parameters.
Combining information from nuclear/chloroplast sequence data with nuclear microsatellites, our IM analyses identify the two varieties as genetically distinct units that evolved in strict allopatry since the mid-Pleistocene, c. 0.89 (0.51–1.2) Ma. Together with Bayesian Skyeline Plots, our data further suggest that both lineages experienced post-divergence demographic growth, followed by refugial isolation, divergence, and in the case of var. arguta post-glacial admixture. However, past species distribution modelling indicates that the species’ overall distribution has not greatly changed over the last glacial cycles.
Our findings highlight the important influence of ancient sea-level changes on the diversification of East Asia’s temperate flora. Implicitly, they challenge the notion of general temperate forest expansion across the ECS land bridge, demonstrating instead its ‘filter’ effect owing to an unsuitable environment for certain species and their biological (e.g., recruitment) properties.
PMCID: PMC4015774  PMID: 24593236
13.  Evolutionary history of a widespread tree species Acer mono in East Asia 
Ecology and Evolution  2014;4(22):4332-4345.
East Asia has the most diverse temperate flora in the world primarily due to the lack of Pleistocene glaciation and the geographic heterogeneity. Although increasing phylogeography studies in this region provided more proofs in this issue, discrepancies and uncertainty still exist, especially in northern temperate deciduous broad-leaved and coniferous mixed forest region (II). And a widespread plant species could reduce the complexity to infer the relationship between diversity and physiographical pattern. Hence, we studied the evolution history of a widespread temperate tree, Acer mono, populations in region II and the influence of physiographic patterns on intraspecific genetic diversity. Analyses of chloroplast sequences and nuclear microsatellites indicated high levels of genetic diversity. The diversity distribution was spatially heterogeneous and a latitudinal cline existed in both markers. The spatial distribution pattern between genetic diversity within A. mono and the diversity at species level was generally consistent. Western subtropical evergreen broad-leaved forest subregion (IVb) had a unique ancient chloroplast clade (CP3) and a nuclear gene pool (GP5) with dominance indicating the critical role of this area in species diversification. Genetic data and ecological niche model results both suggested that populations in region II disappeared during the last glacial maximum (LGM) and recovered from south of Changbai Mt. and the Korean Peninsula. Two distribution centers were likely during the LGM, one in the north edge of warm temperate deciduous broad-leaved forest region (III) and another in the south edge of region III. This was reflected by the genetic pattern with two spatially independent genetic groups. This study highlights the key role of region III in sustaining genetic diversity in the northern range and connecting diversity between southern and northern range. We elucidated the diversity relationship between vegetation regions which could facilitate the understanding of biodiversity origin and maintenance in East Asia.
PMCID: PMC4267871  PMID: 25540694
Acer mono; community assemblage; phylogeography; temperate mixed forests
14.  Phylogeography and palaeodistribution modelling of Nassauvia subgenus Strongyloma (Asteraceae): exploring phylogeographical scenarios in the Patagonian steppe 
Ecology and Evolution  2014;4(22):4270-4286.
The Patagonian steppe is an immense, cold, arid region, yet phylogeographically understudied. Nassauvia subgen. Strongyloma is a characteristic element of the steppe, exhibiting a continuum of morphological variation. This taxon provides a relevant phylogeographical model not only to understand how past environmental changes shaped the genetic structure of its populations, but also to explore phylogeographical scenarios at the large geographical scale of the Patagonian steppe. Here, we (1) assess demographic processes and historical events that shaped current geographic patterns of haplotypic diversity; (2) analyze hypotheses of isolation in refugia, fragmentation of populations, and/or colonization of available areas during Pleistocene glaciations; and (3) model extant and palaeoclimatic distributions to support inferred phylogeographical patterns. Chloroplast intergenic spacers, rpl32–trnL and trnQ–5′rps16, were sequenced for 372 individuals from 63 populations. Nested clade analysis, analyses of molecular variance, and neutrality tests were performed to assess genetic structure and range expansion. The present potential distribution was modelled and projected onto a last glacial maximum (LGM) model. Of 41 haplotypes observed, ten were shared among populations associated with different morphological variants. Populations with highest haplotype diversity and private haplotypes were found in central-western and south-eastern Patagonia, consistent with long-term persistence in refugia during Pleistocene. Palaeomodelling suggested a shift toward the palaeoseashore during LGM; new available areas over the exposed Atlantic submarine platform were colonized during glaciations with postglacial retraction of populations. A scenario of fragmentation and posterior range expansion may explain the observed patterns in the center of the steppe, which is supported by palaeomodelling. Northern Patagonian populations were isolated from southern populations by the Chubut and the Deseado river basins during glaciations. Pleistocene glaciations indirectly impacted the distribution, demography, and diversification of subgen. Strongyloma through decreased winter temperatures and water availability in different areas of its range.
PMCID: PMC4267866  PMID: 25540689
Colonization; fragmentation; glacial refugia; Patagonian steppe; plant phylogeography; Pleistocene glaciations; range expansion; species distribution modelling
15.  Phylogeography of Quercus variabilis Based on Chloroplast DNA Sequence in East Asia: Multiple Glacial Refugia and Mainland-Migrated Island Populations 
PLoS ONE  2012;7(10):e47268.
The biogeographical relationships between far-separated populations, in particular, those in the mainland and islands, remain unclear for widespread species in eastern Asia where the current distribution of plants was greatly influenced by the Quaternary climate. Deciduous Oriental oak (Quercus variabilis) is one of the most widely distributed species in eastern Asia. In this study, leaf material of 528 Q. variabilis trees from 50 populations across the whole distribution (Mainland China, Korea Peninsular as well as Japan, Zhoushan and Taiwan Islands) was collected, and three cpDNA intergenic spacer fragments were sequenced using universal primers. A total of 26 haplotypes were detected, and it showed a weak phylogeographical structure in eastern Asia populations at species level, however, in the central-eastern region of Mainland China, the populations had more haplotypes than those in other regions, with a significant phylogeographical structure (NST = 0.751> GST = 0.690, P<0.05). Q. variabilis displayed high interpopulation and low intrapopulation genetic diversity across the distribution range. Both unimodal mismatch distribution and significant negative Fu’s FS indicated a demographic expansion of Q. variabilis populations in East Asia. A fossil calibrated phylogenetic tree showed a rapid speciation during Pleistocene, with a population augment occurred in Middle Pleistocene. Both diversity patterns and ecological niche modelling indicated there could be multiple glacial refugia and possible bottleneck or founder effects occurred in the southern Japan. We dated major spatial expansion of Q. variabilis population in eastern Asia to the last glacial cycle(s), a period with sea-level fluctuations and land bridges in East China Sea as possible dispersal corridors. This study showed that geographical heterogeneity combined with climate and sea-level changes have shaped the genetic structure of this wide-ranging tree species in East Asia.
PMCID: PMC3480369  PMID: 23115642
16.  Phylogeographic Evidence for a Link of Species Divergence of Ephedra in the Qinghai-Tibetan Plateau and Adjacent Regions to the Miocene Asian Aridification 
PLoS ONE  2013;8(2):e56243.
The Qinghai-Tibetan Plateau (QTP) has become one of the hotspots for phylogeographical studies due to its high species diversity. However, most previous studies have focused on the effects of the Quaternary glaciations on phylogeographical structures and the locations of glacial refugia, and little is known about the effects of the aridization of interior Asia on plant population structure and speciation. Here the chloroplast DNA (cpDNA) trnT-trnF and trnS-trnfM sequences were used to investigate the differentiation and phylogeographical history of 14 Ephedra species from the QTP and northern China, based on a sampling of 107 populations. The phylogeographical analysis, together with phylogenetic reconstruction based on combined four cpDNA fragments (rbcL, rpl16, rps4, and trnS-trnfM), supports three main lineages (eastern QTP, southern QTP, and northern China) of these Ephedra species. Divergence of each lineage could be dated to the Middle or Late Miocene, and was very likely linked to the uplift of the QTP and the Asian aridification, given the high drought and/or cold tolerance of Ephedra. Most of the Ephedra species had low intraspecific variation and lacked a strong phylogeographical structure, which could be partially attributed to clonal reproduction and a relatively recent origin. In addition, ten of the detected 25 cpDNA haplotypes are shared among species, suggesting that a wide sampling of species is helpful to investigate the origin of observed haplotypes and make reliable phylogeographical inference. Moreover, the systematic positions of some Ephedra species are discussed.
PMCID: PMC3571962  PMID: 23418542
17.  Phylogeographic divergence in the widespread delicate skink (Lampropholis delicata) corresponds to dry habitat barriers in eastern Australia 
The mesic habitats of eastern Australia harbour a highly diverse fauna. We examined the impact of climatic oscillations and recognised biogeographic barriers on the evolutionary history of the delicate skink (Lampropholis delicata), a species that occurs in moist habitats throughout eastern Australia. The delicate skink is a common and widespread species whose distribution spans 26° of latitude and nine major biogeographic barriers in eastern Australia. Sequence data were obtained from four mitochondrial genes (ND2, ND4, 12SrRNA, 16SrRNA) for 238 individuals from 120 populations across the entire native distribution of the species. The evolutionary history and diversification of the delicate skink was investigated using a range of phylogenetic (Maximum Likelihood, Bayesian) and phylogeographic analyses (genetic diversity, ΦST, AMOVA, Tajima's D, Fu's F statistic).
Nine geographically structured, genetically divergent clades were identified within the delicate skink. The main clades diverged during the late Miocene-Pliocene, coinciding with the decline and fragmentation of rainforest and other wet forest habitats in eastern Australia. Most of the phylogeographic breaks within the delicate skink were concordant with dry habitat or high elevation barriers, including several recognised biogeographic barriers in eastern Australia (Burdekin Gap, St Lawrence Gap, McPherson Range, Hunter Valley, southern New South Wales). Genetically divergent populations were also located in high elevation topographic isolates inland from the main range of L. delicata (Kroombit Tops, Blackdown Tablelands, Coolah Tops). The species colonised South Australia from southern New South Wales via an inland route, possibly along the Murray River system. There is evidence for recent expansion of the species range across eastern Victoria and into Tasmania, via the Bassian Isthmus, during the late Pleistocene.
The delicate skink is a single widespread, but genetically variable, species. This study provides the first detailed phylogeographic investigation of a widespread species whose distribution spans virtually all of the major biogeographic barriers in eastern Australia.
PMCID: PMC3141439  PMID: 21726459
18.  Comparative phylogeography of eight herbs and lianas (Marantaceae) in central African rainforests 
Frontiers in Genetics  2014;5:403.
Vegetation history in tropical Africa is still to date hardly known and the drivers of population differentiation and speciation processes are little documented. It has often been postulated that population fragmentations following climate changes have played a key role in shaping the geographic distribution patterns of genetic diversity and in driving speciation. Here we analyzed phylogeographic patterns (chloroplast-DNA sequences) within and between eight (sister) species of widespread rainforest herbs and lianas from four genera of Marantaceae (Halopegia, Haumania, Marantochloa, Megaphrynium), searching for concordant patterns across species and concordance with the Pleistocene refuge hypothesis. Using 1146 plastid DNA sequences sampled across African tropical lowland rainforest, particularly in the Lower Guinean (LG) phytogeographic region, we analyzed intra- and interspecific patterns of genetic diversity, endemism and distinctiveness. Intraspecific patterns of haplotype diversity were concordant among most species as well as with the species-level diversity pattern of Marantaceae. Highest values were found in the hilly areas of Cameroon and Gabon. However, the spatial distribution of endemic haplotypes, an indicator for refuge areas in general, was not congruent across species. Each proposed refuge exhibited high values of endemism for one or a few species indicating their potential role as area of retraction for the respective species only. Thus, evolutionary histories seem to be diverse across species. In fact, areas of high diversity might have been both refuge and/or crossing zone of recolonization routes i.e., secondary contact zone. We hypothesize that retraction of species into one or the other refuge happened by chance depending on the species' distribution range at the time of climate deterioration. The idiosyncratic patterns found in Marantaceae species are similar to those found among tropical tree species, especially in southern LG.
PMCID: PMC4237126  PMID: 25477901
endemism; distinctiveness; genetic diversity; trnC-petN1r; refugia; Lower Guinea
19.  Phylogeography and Post-Glacial Recolonization in Wolverines (Gulo gulo) from across Their Circumpolar Distribution 
PLoS ONE  2013;8(12):e83837.
Interglacial-glacial cycles of the Quaternary are widely recognized in shaping phylogeographic structure. Patterns from cold adapted species can be especially informative - in particular, uncovering additional glacial refugia, identifying likely recolonization patterns, and increasing our understanding of species’ responses to climate change. We investigated phylogenetic structure of the wolverine, a wide-ranging cold adapted carnivore, using a 318 bp of the mitochondrial DNA control region for 983 wolverines (n = 209 this study, n = 774 from GenBank) from across their full Holarctic distribution. Bayesian phylogenetic tree reconstruction and the distribution of observed pairwise haplotype differences (mismatch distribution) provided evidence of a single rapid population expansion across the wolverine’s Holarctic range. Even though molecular evidence corroborated a single refugium, significant subdivisions of population genetic structure (0.01< ΦST <0.99, P<0.05) were detected. Pairwise ΦST estimates separated Scandinavia from Russia and Mongolia, and identified five main divisions within North America - the Central Arctic, a western region, an eastern region consisting of Ontario and Quebec/Labrador, Manitoba, and California. These data are in contrast to the nearly panmictic structure observed in northwestern North America using nuclear microsatellites, but largely support the nuclear DNA separation of contemporary Manitoba and Ontario wolverines from northern populations. Historic samples (c. 1900) from the functionally extirpated eastern population of Quebec/Labrador displayed genetic similarities to contemporary Ontario wolverines. To understand these divergence patterns, four hypotheses were tested using Approximate Bayesian Computation (ABC). The most supported hypothesis was a single Beringia incursion during the last glacial maximum that established the northwestern population, followed by a west-to-east colonization during the Holocene. This pattern is suggestive of colonization occurring in accordance with glacial retreat, and supports expansion from a single refugium. These data are significant relative to current discussions on the conservation status of this species across its range.
PMCID: PMC3875487  PMID: 24386287
20.  Population dynamics and genetic changes of Picea abies in the South Carpathians revealed by pollen and ancient DNA analyses 
Studies on allele length polymorphism designate several glacial refugia for Norway spruce (Picea abies) in the South Carpathian Mountains, but infer only limited expansion from these refugia after the last glaciation. To better understand the genetic dynamics of a South Carpathian spruce lineage, we compared ancient DNA from 10,700 and 11,000-year-old spruce pollen and macrofossils retrieved from Holocene lake sediment in the Retezat Mountains with DNA extracted from extant material from the same site. We used eight primer pairs that amplified short and variable regions of the spruce cpDNA. In addition, from the same lake sediment we obtained a 15,000-years-long pollen accumulation rate (PAR) record for spruce that helped us to infer changes in population size at this site.
We obtained successful amplifications for Norway spruce from 17 out of 462 pollen grains tested, while the macrofossil material provided 22 DNA sequences. Two fossil sequences were found to be unique to the ancient material. Population genetic statistics showed higher genetic diversity in the ancient individuals compared to the extant ones. Similarly, statistically significant Ks and Kst values showed a considerable level of differentiation between extant and ancient populations at the same loci.
Lateglacial and Holocene PAR values suggested that population size of the ancient population was small, in the range of 1/10 or 1/5 of the extant population. PAR analysis also detected two periods of rapid population growths (from ca. 11,100 and 3900 calibrated years before present (cal yr BP)) and three bottlenecks (around 9180, 7200 and 2200 cal yr BP), likely triggered by climatic change and human impact.
Our results suggest that the paternal lineages observed today in the Retezat Mountains persisted at this site at least since the early Holocene. Combination of the results from the genetic and the PAR analyses furthermore suggests that the higher level of genetic variation found in the ancient populations and the loss of ancient allele types detected in the extant individuals were likely due to the repeated bottlenecks during the Holocene; however our limited sample size did not allow us to exclude sampling effect.
This study demonstrates how past population size changes inferred from PAR records can be efficiently used in combination with ancient DNA studies. The joint application of palaeoecological and population genetics analyses proved to be a powerful tool to understand the influence of past population demographic changes on the haplotype diversity and genetic composition of forest tree species.
PMCID: PMC3068097  PMID: 21392386
21.  Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. 
Tasmania is a natural laboratory for investigating the evolutionary processes of the Quaternary. It is a large island lying 40-44 degrees S, which was repeatedly glaciated and linked to southeastern continental Australia during the Quaternary. Climate change promoted both the isolation of species in glacial refugia, and an exchange between Tasmanian and mainland floras. Eucalyptus is a complex and diverse genus, which has increased in abundance in Australia over the past 100 kyr, probably in response to higher fire frequency. Morphological evidence suggests that gene flow may have occurred between many eucalypt species after changes in their distribution during the Quaternary. This paper summarizes recent genetic evidence for migration and introgressive hybridization in Tasmanian Eucalyptus. Maternally inherited chloroplast DNA reveals a long-term persistence of eucalypts in southeastern Tasmanian refugia, coupled with introgressive hybridization involving many species. Detailed analysis of the widespread species Eucalyptus globulus suggests that migration from mainland Australia was followed by introgression involving a rare Tasmanian endemic. The data support the hypothesis that changes in distribution of interfertile species during the Quaternary have promoted reticulate evolution in Eucalyptus.
PMCID: PMC1693314  PMID: 15101583
22.  Phylogeography sheds light on the central–marginal hypothesis in a Mediterranean narrow endemic plant 
Annals of Botany  2013;112(7):1409-1420.
Background and Aims
Understanding the factors that shape variation in genetic diversity across the geographic ranges of species is an important challenge in the effort to conserve evolutionary processes sustaining biodiversity. The historical influences leading to a central–marginal organization of genetic diversity have been explored for species whose range is known to have expanded from refugia after glacial events. However, this question has rarely been addressed for Mediterranean endemic plants of azonal habitats such as rocky slopes or screes. In this context, this comprehensive study examined molecular and field data from Arenaria provincialis (Caryophyllaceae), a narrow endemic plant of south-eastern France.
Across the whole geographic range, an investigation was made of whether high levels of abundance and genetic diversity (estimated from amplified fragment length polymorphism markers) are centrally distributed, to evaluate the relevance of the central–marginal hypothesis. Phylogeographic patterns inferred from chloroplast DNA (cpDNA) were used, applying Bayesian methods to test the influence of past biogeographic events. Multivariate analysis combining phylogeographic and ecological data was used to reveal the historical and ecological distinctiveness of populations.
Key Results
Despite the narrow distribution of A. provincialis, a high level of nucleotide variation is found within cpDNA loci, supporting its persistence throughout the Pleistocene period. The area characterized by the highest genetic diversity is centrally located. Structured phylogeography and Bayesian factor analysis supported the hypothesis that the central area of the distribution was the source of both westward and eastward migrations, probably during arid periods of the Pleistocene, and more recently was a crossroads of backward migrations. By contrast, the two areas located today at the range limits are younger, have reduced genetic diversity and are marginal in the ecological gradients.
This study highlights a case of strong population distinctiveness within a narrow range. Phylogeography sheds light on the historical role of the areas centrally situated in the distribution. The current range size and abundance patterns are not sufficient to predict the organization of genetic diversity.
PMCID: PMC3806523  PMID: 23962409
Arenaria provincialis; Caryophyllaceae; central–marginal hypothesis; genetic diversity; geographic range; ecological niche; Pleistocene; Provence; conservation; migration; population distinctiveness
23.  Phylogeography of Pinus subsection Australes in the Caribbean Basin 
Annals of Botany  2010;107(2):229-241.
Background and Aims
Four species of Pinus subsection Australes occur in the Caribbean Basin: P. caribaea, P. cubensis, P. maestrensis and P. occidentalis. This study analyses the phylogeography of these species to assess possible colonization events from Central America to the islands and subsequent population expansions during glacial periods driven by both drier climate and larger emerged land areas.
Allele size data were obtained for plastid microsatellites for 314 individuals from 24 populations, covering the distribution range of subsection Australes in the Caribbean Basin.
Key Results
In total, 113 plastid haplotypes were identified. The highest genetic diversity was found in populations of P. caribaea. Overall, Caribbean Basin populations fit the isolation by distance model. Significant phylogeographical structure was found (RST = 0·671 > permuted RST = 0·101; P < 0·0001). The haplotype network and a Bayesian analysis of population structure (BAPS) indicated different Central American origins for P. caribaea var. bahamensis and P. caribaea var. caribaea plastids, with Central America populations in northern and south-eastern groups. Sudden expansion times for BAPS clusters were close to three glacial maxima.
Central America contains ancestral plastid haplotypes. Population expansion has played a major role in the distribution of genetic diversity in P. caribaea var. hondurensis. Two colonization events gave rise to the P. caribaea var. bahamensis and P. caribaea var. caribaea lineages. Plastid variation in the eastern species (P. cubensis, P. maestrensis and P. occidentalis) evolved independently from that in P. caribaea var. caribaea. Incomplete lineage sorting between P. cubensis and P. maestrensis is apparent. Inferred expansion times for P. caribaea var. bahamensis and for the eastern lineages correspond to glacial maxima, whereas those for P. caribaea var. hondurensis correspond to the beginning of the temperature decrease that led to Marine Isotope Stage 8.
PMCID: PMC3025731  PMID: 21118838
Caribbean Basin; historical demography; phylogeography; Pinus; plastid microsatellites; population genetics; subsection Australes
24.  Phylogeography of Liquidambar styraciflua (Altingiaceae) in Mesoamerica: survivors of a Neogene widespread temperate forest (or cloud forest) in North America? 
Ecology and Evolution  2014;4(4):311-328.
We investigate the genetic variation between populations of the American sweetgum (Liquidambar styraciflua), a tree species with a disjunct distribution between northeastern Texas and Mexico, by analyzing sequences of two chloroplast DNA plastid regions in Mesoamerica. Our results revealed phylogeographical structure, with private haplotypes distributed in unique environmental space at either side of the Trans-Mexican Volcanic Belt, and a split in the absence of gene flow dating back ca. 4.2–1.4 million years ago (MYA). Species distribution modeling results fit a model of refugia along the Gulf and Atlantic coasts but the present ranges of US and Mesoamerican populations persisted disjunct during glacial/interglacial cycles. Divergence between the US and Mesoamerican (ca. 8.4–2.8 MYA) populations of L. styraciflua and asymmetrical gene flow patterns support the hypothesis of a long-distance dispersal during the Pliocene, with fragmentation since the most recent glacial advance (120,000 years BP) according to coalescent simulations and high effective migration rates from Mesoamerica to the USA and close to zero in the opposite direction. Our findings implicate the Trans-Mexican Volcanic Belt as a porous barrier driving genetic divergence of L. styraciflua, corresponding with environmental niche differences, during the Pliocene to Quaternary volcanic arc episode 3.6 MYA, and a Mesoamerican origin of populations in the USA.
PMCID: PMC3936380  PMID: 24634718
Altingiaceae; cloud forests; Liquidambar; Mesoamerica; Mexico; Pleistocene; Trans-Mexican Volcanic Belt
25.  Three divergent lineages within an Australian marsupial (Petrogale penicillata) suggest multiple major refugia for mesic taxa in southeast Australia 
Ecology and Evolution  2014;4(7):1102-1116.
Mesic southeastern Australia represents the continent's ancestral biome and is highly biodiverse, yet its phylogeographic history remains poorly understood. Here, we examine mitochondrial DNA (mtDNA) control region and microsatellite diversity in the brush-tailed rock-wallaby (Petrogale penicillata;n = 279 from 31 sites), to assess historic evolutionary and biogeographic processes in southeastern Australia. Our results (mtDNA, microsatellites) confirmed three geographically discrete and genetically divergent lineages within brush-tailed rock-wallabies, whose divergence appears to date to the mid-Pleistocene. These three lineages had been hypothesized previously but data were limited. While the Northern and Central lineages were separated by a known biogeographic barrier (Hunter Valley), the boundary between the Central and Southern lineages was not. We propose that during particularly cool glacial cycles, the high peaks of the Great Dividing Range and the narrow adjacent coastal plain resulted in a more significant north–south barrier for mesic taxa in southeastern Australia than has been previously appreciated. Similarly, located phylogeographic breaks in codistributed species highlight the importance of these regions in shaping the distribution of biodiversity in southeastern Australia and suggest the existence of three major refuge areas during the Pleistocene. Substructuring within the northern lineage also suggests the occurrence of multiple local refugia during some glacial cycles. Within the three major lineages, most brush-tailed rock-wallaby populations were locally highly structured, indicating limited dispersal by both sexes. The three identified lineages represent evolutionarily significant units and should be managed to maximize the retention of genetic diversity within this threatened species.
PMCID: PMC3997325  PMID: 24772286
Great Dividing Range; Hunter Valley; phylogeography; rock-wallaby; southeast Australia

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