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1.  Niche Conservatism and the Future Potential Range of Epipactis helleborine (Orchidaceae) 
PLoS ONE  2013;8(10):e77352.
The aim of the present study was to evaluate the current distribution of suitable niches for the invasive orchid species, Epipactis helleborine, and to estimate the possibility of its further expansion. Moreover, niche modeling tools were used to explain its rapid expansion in North America and to test the niche conservatism of the species. The maximum entropy method was used to create models of the suitable niche distribution. A database of E. helleborine localities was prepared based on the examination of herbarium specimens, information from electronic databases as well as data gathered during field works. The differences between the niches occupied by native and invasive populations were evaluated using the niche overlap and niche identity test indexes. Moreover, the coverage of the most suitable habitats for the species was measured for three future scenarios as well as for the present time model. Populations of E. helleborine occupy North American west coast habitats very similar to those preferred by native, Eurasian populations, while the expansion in the east coast is related to the niche shift. The created models of suitable niche distribution indicate that the species does not realize its potential niche in the native range. The total surface of the habitats potentially available for E. helleborine will decrease in all climate change scenarios created for 2080.
PMCID: PMC3797094  PMID: 24143222
2.  Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard 
Pleistocene climatic oscillations have played a major role in structuring present-day biodiversity. The southern Mediterranean peninsulas have long been recognized as major glacial refugia, from where Northern Europe was post-glacially colonized. However, recent studies have unravelled numerous additional refugia also in northern regions. We investigated the phylogeographic pattern of the widespread Western Palaearctic lizard Podarcis muralis, using a range-wide multilocus approach, to evaluate whether it is concordant with a recent expansion from southern glacial refugia or alternatively from a combination of Mediterranean and northern refugia.
We analyzed DNA sequences of two mitochondrial (cytb and nd4) and three nuclear (acm4, mc1r, and pdc) gene fragments in individuals from 52 localities across the species range, using phylogenetic and phylogeographic methods. The complex phylogeographic pattern observed, with 23 reciprocally monophyletic allo- parapatric lineages having a Pleistocene divergence, suggests a scenario of long-term isolation in multiple ice-age refugia across the species distribution range. Multiple lineages were identified within the three Mediterranean peninsulas – Iberia, Italy and the Balkans - where the highest genetic diversity was observed. Such an unprecedented phylogeographic pattern - here called “refugia within all refugia” – compasses the classical scenario of multiple southern refugia. However, unlike the southern refugia model, various distinct lineages were also found in northern regions, suggesting that additional refugia in France, Northern Italy, Eastern Alps and Central Balkans allowed the long-term persistence of this species throughout Pleistocene glaciations.
The phylogeography of Podarcis muralis provides a paradigm of temperate species survival in Mediterranean and extra-Mediterranean glacial refugia. Such refugia acted as independent biogeographic compartments for the long-term persistence of this species, for the differentiation of its genetic lineages, and for the short-distance post-glacial re-colonization of neighbouring areas. This finding echoes previous findings from recent phylogeographic studies on species from temperate ecoregions, thus suggesting the need for a reappraisal of the role of northern refugia for glacial persistence and post-glacial assembly of Holarctic biota.
PMCID: PMC3711914  PMID: 23841475
Podarcis muralis; Phylogeography; Western Palaearctic; Glacial refugia; Mediterranean peninsulas; Genetic diversity; Temperate species
3.  Phylogeography and postglacial expansion of the endangered semi-aquatic mammal Galemys pyrenaicus 
Species with strict ecological requirements may provide new insights into the forces that shaped the geographic variation of genetic diversity. The Pyrenean desman, Galemys pyrenaicus, is a small semi-aquatic mammal that inhabits clean streams of the northern half of the Iberian Peninsula and is endangered in most of its geographic range, but its genetic structure is currently unknown. While the stringent ecological demands derived from its aquatic habitat might have caused a partition of the genetic diversity among river basins, Pleistocene glaciations would have generated a genetic pattern related to glacial refugia.
To study the relative importance of historical and ecological factors in the genetic structure of G. pyrenaicus, we used mitochondrial and intronic sequences of specimens covering most of the species range. We show, first, that the Pyrenean desman has very low levels of genetic diversity compared to other mammals. In addition, phylogenetic and dating analyses of the mitochondrial sequences reveal a strong phylogeographic structure of a Middle Pleistocene origin, suggesting that the main lineages arose during periods of glacial isolation. Furthermore, both the spatial distribution of nuclear and mitochondrial diversity and the results of species distribution modeling suggest the existence of a major glacial refugium in the northwestern part of the Iberian Peninsula. Finally, the main mitochondrial lineages show a striking parapatric distribution without any apparent exchange of mitochondrial haplotypes between the lineages that came into secondary contact (although with certain permeability to nuclear genes), indicating incomplete mixing after the post-glacial recolonization. On the other hand, when we analyzed the partition of the genetic diversity among river basins, the Pyrenean desman showed a lower than expected genetic differentiation among main rivers.
The analysis of mitochondrial and intronic markers in G. pyrenaicus showed the predominant effects of Pleistocene glaciations on the genetic structure of this species, while the distribution of the genetic diversity was not greatly influenced by the main river systems. These results and, particularly, the discovery of a marked phylogeographic structure, may have important implications for the conservation of the Pyrenean desman.
PMCID: PMC3682870  PMID: 23738626
Conservation genetics; Introns; Mammals; Mitochondrial genes; Nuclear genes; Pyrenean desman; Niche modeling; Iberian Peninsula; Endemism
4.  Genetically Depauperate in the Continent but Rich in Oceanic Islands: Cistus monspeliensis (Cistaceae) in the Canary Islands 
PLoS ONE  2011;6(2):e17172.
Population genetic theory holds that oceanic island populations are expected to have lower levels of genetic variation than their mainland counterparts, due to founder effect after island colonization from the continent. Cistus monspeliensis (Cistaceae) is distributed in both the Canary Islands and the Mediterranean region. Numerous phylogenetic results obtained in the last years allow performing further phylogeographic analyses in Cistus.
Methodology/Principal Findings
We analyzed sequences from multiple plastid DNA regions in 47 populations of Cistus monspeliensis from the Canary Islands (21 populations) and the Mediterranean basin (26 populations). The time-calibrated phylogeny and phylogeographic analyses yielded the following results: (1) a single, ancestral haplotype is distributed across the Mediterranean, whereas 10 haplotypes in the Canary Islands; (2) four haplotype lineages are present in the Canarian Islands; (3) multiple colonization events across the archipelago are inferred; (4) the earliest split of intraspecific lineages occurred in the Early to Middle Pleistocene (<930,000 years BP).
The contrasting pattern of cpDNA variation is best explained by genetic bottlenecks in the Mediterranean during Quaternary glaciations, while the Canarian archipelago acted as a refugium of high levels of genetic diversity. Active colonization across the Canarian islands is supported not only by the distribution of C. monspeliensis in five of the seven islands, but also by our phylogeographic reconstruction in which unrelated haplotypes are present on the same island. Widespread distribution of thermophilous habitats on every island, as those found throughout the Mediterranean, has likely been responsible for the successful colonization of C. monspeliensis, despite the absence of a long-distance dispersal mechanism. This is the first example of a plant species with higher genetic variation among oceanic island populations than among those of the continent.
PMCID: PMC3038934  PMID: 21347265
5.  Phylogeography of Supralittoral Rocky Intertidal Ligia Isopods in the Pacific Region from Central California to Central Mexico 
PLoS ONE  2010;5(7):e11633.
Ligia isopods are widely distributed in the Pacific rocky intertidal shores from central California to central Mexico, including the Gulf of California. Yet, their biological characteristics restrict them to complete their life cycles in a very narrow range of the rocky intertidal supralittoral. Herein, we examine phylogeographic patterns of Ligia isopods from 122 localities between central California and central Mexico. We expect to find high levels of allopatric diversity. In addition, we expect the phylogeographic patterns to show signatures of past vicariant events that occurred in this geologically dynamic region.
Methodology/Principal Findings
We sequenced two mitochondrial genes (Cytochrome Oxidase I and 16S ribosomal DNA). We conducted Maximum Likelihood and Bayesian phylogenetic analyses. We found many divergent clades that, in general, group according to geography. Some of the most striking features of the Ligia phylogeographic pattern include: (1) deep mid-peninsular phylogeographic breaks on the Pacific and Gulf sides of Baja peninsula; (2) within the Gulf lineages, the northern peninsula is most closely related to the northern mainland, while the southern peninsula is most closely related to the central-southern mainland; and, (3) the southernmost portion of the peninsula (Cape Region) is most closely related to the southernmost portion of mainland.
Our results shed light on the phylogenetic relationships of Ligia populations in the study area. This study probably represents the finest-scale phylogeographic examination for any organism to date in this region. Presence of highly divergent lineages suggests multiple Ligia species exist in this region. The phylogeographic patterns of Ligia in the Gulf of California and Baja peninsula are incongruent with a widely accepted vicariant scenario among phylogeographers, but consistent with aspects of alternative geological hypotheses and phylo- and biogeographic patterns of several other taxa. Our findings contribute to the ongoing debate regarding the geological origin of this important biogeographic region.
PMCID: PMC2908127  PMID: 20657776
6.  One Species, Three Pleistocene Evolutionary Histories: Phylogeography of the Italian Crested Newt, Triturus carnifex 
PLoS ONE  2012;7(7):e41754.
Phylogeographic patterns of temperate species from the Mediterranean peninsulas have been investigated intensively. Nevertheless, as more phylogeographies become available, either unique patterns or new lines of concordance continue to emerge, providing new insights on the evolution of regional biotas. Here, we investigated the phylogeography and evolutionary history of the Italian crested newt, Triturus carnifex, through phylogenetic, molecular dating and population structure analyses of two mitochondrial gene fragments (ND2 and ND4; overall 1273 bp). We found three main mtDNA lineages having parapatric distribution and estimated divergence times between Late Pliocene and Early Pleistocene. One lineage (S) was widespread south of the northern Apennine chain and was further geographically structured into five sublineages, likely of Middle Pleistocene origin. The second lineage (C) was widespread throughout the Padano–Venetian plain and did not show a clear phylogeographic structure. The third lineage (N) was observed in only two populations located on western Croatia/Slovenia. Results of analysis of molecular variance suggested that partitioning populations according to the geographic distribution of these lineages and sublineages explains 76% of the observed genetic variation. The phylogeographic structure observed within T. carnifex and divergence time estimates among its lineages, suggest that responses to Pleistocene environmental changes in this single species have been as diverse as those found previously among several codistributed temperate species combined. Consistent with the landscape heterogeneity, physiographic features, and palaeogeographical evolution of its distribution range, these responses encompass multiple refugia along the Apennine chain, lowland refugia in large peri-coastal plains, and a ‘cryptic’ northern refugium.
PMCID: PMC3406094  PMID: 22848590
7.  The importance of Anatolian mountains as the cradle of global diversity in Arabis alpina, a key arctic–alpine species 
Annals of Botany  2011;108(2):241-252.
Background and Aims
Anatolia is a biologically diverse, but phylogeographically under-explored region. It is described as either a centre of origin and long-term Pleistocene refugium, or as a centre for genetic amalgamation, fed from distinct neighbouring refugia. These contrasting hypotheses are tested through a global phylogeographic analysis of the arctic–alpine herb, Arabis alpina.
Herbarium and field collections were used to sample comprehensively the entire global range, with special focus on Anatolia and Levant. Sequence variation in the chloroplast DNA trnL-trnF region was examined in 483 accessions. A haplotype genealogy was constructed and phylogeographic methods, demographic analysis and divergence time estimations were used to identify the centres of diversity and to infer colonization history.
Key Results
Fifty-seven haplotypes were recovered, belonging to three haplogroups with non-overlapping distributions in (1) North America/Europe/northern Africa, (2) the Caucuses/Iranian Plateau/Arabian Peninsula and (3) Ethiopia–eastern Africa. All haplogroups occur within Anatolia, and all intermediate haplotypes linking the three haplogroups are endemic to central Anatolia and Levant, where haplotypic and nucleotide diversities exceeded all other regions. The local pattern of haplotype distribution strongly resembles the global pattern, and the haplotypes began to diverge approx. 2·7 Mya, coinciding with the climate cooling of the early Middle Pleistocene.
The phylogeographic structure of Arabis alpina is consistent with Anatolia being the cradle of origin for global genetic diversification. The highly structured landscape in combination with the Pleistocene climate fluctuations has created a network of mountain refugia and the accumulation of spatially arranged genotypes. This local Pleistocene population history has subsequently left a genetic imprint at the global scale, through four range expansions from the Anatolian diversity centre into Europe, the Near East, Arabia and Africa. Hence this study also illustrates the importance of sampling and scaling effects when translating global from local diversity patterns during phylogeographic analyses.
PMCID: PMC3143044  PMID: 21712298
Anatolia; centre of origin; Pleistocene glaciations; chloroplast trnL-F; divergence times; alpine plants; Arabis alpina
8.  Historical biogeography of the land snail Cornu aspersum: a new scenario inferred from haplotype distribution in the Western Mediterranean basin 
Despite its key location between the rest of the continent and Europe, research on the phylogeography of north African species remains very limited compared to European and North American taxa. The Mediterranean land mollusc Cornu aspersum (= Helix aspersa) is part of the few species widely sampled in north Africa for biogeographical analysis. It then provides an excellent biological model to understand phylogeographical patterns across the Mediterranean basin, and to evaluate hypotheses of population differentiation. We investigated here the phylogeography of this land snail to reassess the evolutionary scenario we previously considered for explaining its scattered distribution in the western Mediterranean, and to help to resolve the question of the direction of its range expansion (from north Africa to Europe or vice versa). By analysing simultaneously individuals from 73 sites sampled in its putative native range, the present work provides the first broad-scale screening of mitochondrial variation (cyt b and 16S rRNA genes) of C. aspersum.
Phylogeographical structure mirrored previous patterns inferred from anatomy and nuclear data, since all haplotypes could be ascribed to a B (West) or a C (East) lineage. Alternative migration models tested confirmed that C. aspersum most likely spread from north Africa to Europe. In addition to Kabylia in Algeria, which would have been successively a centre of dispersal and a zone of secondary contacts, we identified an area in Galicia where genetically distinct west and east type populations would have regained contact.
Vicariant and dispersal processes are reviewed and discussed in the light of signatures left in the geographical distribution of the genetic variation. In referring to Mediterranean taxa which show similar phylogeographical patterns, we proposed a parsimonious scenario to account for the "east-west" genetic splitting and the northward expansion of the western (B) clade which roughly involves (i) the dispersal of ancestral (eastern) types through Oligocene terranes in the Western Mediterranean (ii) the Tell Atlas orogenesis as gene flow barrier between future west and east populations, (iii) the impact of recurrent climatic fluctuations from mid-Pliocene to the last ice age, (iv) the loss of the eastern lineage during Pleistocene northwards expansion phases.
PMCID: PMC2826328  PMID: 20089175
9.  When the Rule Becomes the Exception. No Evidence of Gene Flow between Two Zerynthia Cryptic Butterflies Suggests the Emergence of a New Model Group 
PLoS ONE  2013;8(6):e65746.
There is increasing evidence that most parapatric cryptic/sister taxa are reproductively compatible across their areas of contact. Consequently, the biological species concept, which assumes absence of interbreeding, is becoming a not so effective criterion in evolutionary ecology. Nevertheless, the few parapatric sister taxa showing complete reproductive barriers represent interesting models to study speciation processes and the evolution of reproductive isolation. In this study, we examined contact populations in northwestern Italy of two butterfly species, Zerynthia polyxena and Z. cassandra, characterized by different genitalic morphotypes. We studied levels of divergence among 21 populations distributed from Sicily to France using three genetic markers (the mitochondrial COI and ND1 genes and the nuclear wingless gene) and genitalic geometric morphometrics. Moreover, we performed species distribution modelling to estimate different climatic requirements of Z. polyxena and Z. cassandra. We projected climatic data into glacial maximum scenarios in order to verify if and to which extent glacial cycles could have contributed to speciation processes. Genetic and morphometric analyses identified two main groups. All specimens showed a concordant pattern of diversification, including those individuals sampled in the contact area. Haplotype distribution and climatic models showed that during glacial maxima both species experienced a strong range contraction and presumably remained separated into different microrefugia in southern France, in the Italian Peninsula and on the islands of Elba and Sicily. Long term separation was probably favoured by reduced dispersal ability and high phylopatry, while genitalic diversification probably favoured interbreeding avoidance. Conversely, the aposematic wing pattern remained almost identical. We compared our results with those obtained in other species and concluded that Z. polyxena and Z. cassandra represent a valuable model in the study of speciation.
PMCID: PMC3675026  PMID: 23755277
10.  A phylogenetic study of Laeliinae (Orchidaceae) based on combined nuclear and plastid DNA sequences 
Annals of Botany  2009;104(3):417-430.
Background and Aims
Laeliinae are a neotropical orchid subtribe with approx. 1500 species in 50 genera. In this study, an attempt is made to assess generic alliances based on molecular phylogenetic analysis of DNA sequence data.
Six DNA datasets were gathered: plastid trnL intron, trnL-F spacer, matK gene and trnK introns upstream and dowstream from matK and nuclear ITS rDNA. Data were analysed with maximum parsimony (MP) and Bayesian analysis with mixed models (BA).
Key Results
Although relationships between Laeliinae and outgroups are well supported, within the subtribe sequence variation is low considering the broad taxonomic range covered. Localized incongruence between the ITS and plastid trees was found. A combined tree followed the ITS trees more closely, but the levels of support obtained with MP were low. The Bayesian analysis recovered more well-supported nodes. The trees from combined MP and BA allowed eight generic alliances to be recognized within Laeliinae, all of which show trends in morphological characters but lack unambiguous synapomorphies.
By using combined plastid and nuclear DNA data in conjunction with mixed-models Bayesian inference, it is possible to delimit smaller groups within Laeliinae and discuss general patterns of pollination and hybridization compatibility. Furthermore, these small groups can now be used for further detailed studies to explain morphological evolution and diversification patterns within the subtribe.
PMCID: PMC2720643  PMID: 19423551
Laeliinae; Orchidaceae; ITS; trnL intron; trnL-F spacer; matK
11.  Paleoclimatic modeling and phylogeography of least killifish, Heterandria formosa: insights into Pleistocene expansion-contraction dynamics and evolutionary history of North American Coastal Plain freshwater biota 
Climatic and sea-level fluctuations throughout the last Pleistocene glacial cycle (~130-0 ka) profoundly influenced present-day distributions and genetic diversity of Northern Hemisphere biotas by forcing range contractions in many species during the glacial advance and allowing expansion following glacial retreat ('expansion-contraction’ model). Evidence for such range dynamics and refugia in the unglaciated Gulf-Atlantic Coastal Plain stems largely from terrestrial species, and aquatic species Pleistocene responses remain relatively uninvestigated. Heterandria formosa, a wide-ranging regional endemic, presents an ideal system to test the expansion-contraction model within this biota. By integrating ecological niche modeling and phylogeography, we infer the Pleistocene history of this livebearing fish (Poeciliidae) and test for several predicted distributional and genetic effects of the last glaciation.
Paleoclimatic models predicted range contraction to a single southwest Florida peninsula refugium during the Last Glacial Maximum, followed by northward expansion. We inferred spatial-population subdivision into four groups that reflect genetic barriers outside this refuge. Several other features of the genetic data were consistent with predictions derived from an expansion-contraction model: limited intraspecific divergence (e.g. mean mtDNA p-distance = 0.66%); a pattern of mtDNA diversity (mean Hd = 0.934; mean π = 0.007) consistent with rapid, recent population expansion; a lack of mtDNA isolation-by-distance; and clinal variation in allozyme diversity with higher diversity at lower latitudes near the predicted refugium. Statistical tests of mismatch distributions and coalescent simulations of the gene tree lent greater support to a scenario of post-glacial expansion and diversification from a single refugium than to any other model examined (e.g. multiple-refugia scenarios).
Congruent results from diverse data indicate H. formosa fits the classic Pleistocene expansion-contraction model, even as the genetic data suggest additional ecological influences on population structure. While evidence for Plio-Pleistocene Gulf Coast vicariance is well described for many freshwater species presently codistributed with H. formosa, this species demography and diversification departs notably from this pattern. Species-specific expansion-contraction dynamics may therefore have figured more prominently in shaping Coastal Plain evolutionary history than previously thought. Our findings bolster growing appreciation for the complexity of phylogeographical structuring within North America’s southern refugia, including responses of Coastal Plain freshwater biota to Pleistocene climatic fluctuations.
PMCID: PMC3851817  PMID: 24107245
12.  The evolution of floral deception in Epipactis veratrifolia (Orchidaceae): from indirect defense to pollination 
BMC Plant Biology  2014;14:63.
It is estimated that floral deception has evolved in at least 7500 species of angiosperms, of which two thirds are orchids. Epipactis veratrifolia (Orchidaceae) is a model system of aphid mimicry as aphidophagous hoverflies lay eggs on false brood sites on their flowers. To understand the evolutionary ecology of floral deception, we investigated the pollination biology of E. veratrifolia across 10 populations in the Eastern Himalayas. We reconstructed the phylogeny of Epipactis and mapped the known pollination systems of previously studied species onto the tree.
Some inflorescences of E. veratrifolia were so infested with aphids while they were still in bud that the some larvae of hoverflies developed to the third instar while flower buds opened. This indicated that adult female hoverflies were partly rewarded for oviposition. Although flowers failed to secrete nectar, they mimicked both alarm pheromones and aphid coloring of to attract female hoverflies as their exclusive pollinators. Phylogenetic mapping indicate that pollination by aphidophagous hoverflies is likely an ancestral condition in the genus Epipactis. We suggest that the biological interaction of aphid (prey), orchid (primary producer) and hoverfly (predator) may represent an intermediate stage between mutualism and deception in the evolution of pollination-by-deceit in E. veratrifolia.
Our analyses indicate that this intermediate stage may be used as a model system to interpret the origin of oviposition (brood site) mimicry in Epipactis. We propose the hypothesis that some deceptive pollination systems evolved directly from earlier (partly) mutualistic systems that maintained the fidelity of the original pollinator(s) even though rewards (nectar/ brood site) were lost.
PMCID: PMC4007573  PMID: 24621377
Anther cap; Aphids; Floral mimicry; Hoverflies; Intermediate stage; Pollinator
13.  Evolutionary Origin and Phylogeography of the Diploid Obligate Parthenogen Artemia parthenogenetica (Branchiopoda: Anostraca) 
PLoS ONE  2010;5(8):e11932.
Understanding the evolutionary origin and the phylogeographic patterns of asexual taxa can shed light on the origin and maintenance of sexual reproduction. We assessed the geographic origin, genetic diversity, and phylogeographic history of obligate parthenogen diploid Artemia parthenogenetica populations, a widespread halophilic crustacean.
Methodology/Principal Findings
We analysed a partial sequence of the Cytochrome c Oxidase Subunit I mitochondrial gene from an extensive set of localities (including Eurasia, Africa, and Australia), and examined their phylogeographic patterns and the phylogenetic relationships of diploid A. parthenogenetica and its closest sexual relatives. Populations displayed an extremely low level of mitochondrial genetic diversity, with one widespread haplotype shared by over 79% of individuals analysed. Phylogenetic and phylogeographic analyses indicated a multiple and recent evolutionary origin of diploid A. parthenogenetica, and strongly suggested that the geographic origin of parthenogenesis in Artemia was in Central Asia. Our results indicate that the maternal sexual ancestors of diploid A. parthenogenetica were an undescribed species from Kazakhstan and A. urmiana.
We found evidence for multiple origin of parthenogenesis in Central Asia. Our results indicated that, shortly after its origin, diploid A. parthenogenetica populations underwent a rapid range expansion from Central Asia towards the Mediterranean region, and probably to the rest of its current geographic distribution. This contrasts with the restricted geographic distribution, strong genetic structure, and regional endemism of sexual Artemia lineages and other passively dispersed sexual continental aquatic invertebrates. We hypothesize that diploid parthenogens might have reached their current distribution in historical times, with a range expansion possibly facilitated by an increased availability of suitable habitat provided by anthropogenic activities, such as the spread of solar saltworks, aided by their natural dispersal vectors (i.e., waterbirds).
PMCID: PMC2915914  PMID: 20694140
14.  Phylogeography of Rhodiola kirilowii (Crassulaceae): A Story of Miocene Divergence and Quaternary Expansion 
PLoS ONE  2014;9(11):e112923.
The evolution and current distribution of the Sino-Tibetan flora have been greatly affected by historical geological events, such as the uplift of the Qinghai-Tibetan Plateau (QTP), and Quaternary climatic oscillations. Rhodiola kirilowii, a perennial herb with its distribution ranging from the southeastern QTP and the Hengduan Mountains (HM) to adjacent northern China and central Asia, provides an excellent model to examine and disentangle the effect of both geological orogeny and climatic oscillation on the evolutionary history of species with such distribution patterns. We here conducted a phylogeographic study using sequences of two chloroplast fragments (trnL-F and trnS-G) and internal transcribed spacers in 29 populations of R. kirilowii. A total of 25 plastid haplotypes and 12 ITS ribotypes were found. Molecular clock estimation revealed deep divergence between the central Asian populations and other populations from the HM and northern China; this split occurred ca. 2.84 million year ago. The majority of populations from the mountains of northern China were dominated by a single haplotype or ribotype, while populations of the HM harbored both high genetic diversity and high haplotype diversity. This distribution pattern indicates that HM was either a diversification center or a refugium for R. kirilowii during the Quaternary climatic oscillations. The present distribution of this species on mountains in northern China may have resulted from a rapid glacial population expansion from the HM. This expansion was confirmed by the mismatch distribution analysis and negative Tajima's D and Fu's FS values, and was dated to ca. 168 thousand years ago. High genetic diversity and population differentiation in both plastid and ITS sequences were revealed; these imply restricted gene flow between populations. A distinct isolation-by-distance pattern was suggested by the Mantel test. Our results show that in old lineages, populations may harbour divergent genetic forms that are sufficient to maintain or even increase overall genetic diversity despite fragmentation and low within-population variation.
PMCID: PMC4229298  PMID: 25389750
15.  Molecular biogeography of Europe: Pleistocene cycles and postglacial trends 
Frontiers in Zoology  2007;4:11.
The climatic cycles with subsequent glacial and intergalcial periods have had a great impact on the distribution and evolution of species. Using genetic analytical tools considerably increased our understanding of these processes. In this review I therefore give an overview of the molecular biogeography of Europe. For means of simplification, I distinguish between three major biogeographical entities: (i) "Mediterranean" with Mediterranean differentiation and dispersal centres, (ii) "Continental" with extra-Mediterranean centres and (iii) "Alpine" and/or "Arctic" with recent alpine and/or arctic distribution patterns. These different molecular biogeographical patterns are presented using actual examples.
Many "Mediterranean" species are differentiated into three major European genetic lineages, which are due to glacial isolation in the three major Mediterranean peninsulas. Postglacial expansion in this group of species is mostly influenced by the barriers of the Pyrenees and the Alps with four resulting main patterns of postglacial range expansions. However, some cases are known with less than one genetic lineage per Mediterranean peninsula on the one hand, and others with a considerable genetic substructure within each of the Mediterranean peninsulas, Asia Minor and the Maghreb. These structures within the Mediterranean sub-centres are often rather strong and in several cases even predate the Pleistocene.
For the "Continental" species, it could be shown that the formerly supposed postglacial spread from eastern Palearctic expansion centres is mostly not applicable. Quite the contrary, most of these species apparently had extra-Mediterranean centres of survival in Europe with special importance of the perialpine regions, the Carpathian Basin and parts of the Balkan Peninsula.
In the group of "Alpine" and/or "Arctic" species, several molecular biogeographical patterns have been found, which support and improve the postulates based on distribution patterns and pollen records. Thus, genetic studies support the strong linkage between southwestern Alps and Pyrenees, northeastern Alps and Carpathians as well as southeastern Alps and the Dinaric mountain systems, hereby allowing conclusions on the glacial distribution patterns of these species. Furthermore, genetic analyses of arctic-alpine disjunct species support their broad distribution in the periglacial areas at least during the last glacial period.
The detailed understanding of the different phylogeographical structures is essential for the management of the different evolutionary significant units of species and the conservation of their entire genetic diversity. Furthermore, the distribution of genetic diversity due to biogeographical reasons helps understanding the differing regional vulnerabilities of extant populations.
PMCID: PMC1868914  PMID: 17439649
16.  The Colonization History of Juniperus brevifolia (Cupressaceae) in the Azores Islands 
PLoS ONE  2011;6(11):e27697.
A central aim of island biogeography is to understand the colonization history of insular species using current distributions, fossil records and genetic diversity. Here, we analyze five plastid DNA regions of the endangered Juniperus brevifolia, which is endemic to the Azores archipelago.
Methodology/Principal Findings
The phylogeny of the section Juniperus and the phylogeographic analyses of J. brevifolia based on the coalescence theory of allele (plastid) diversity suggest that: (1) a single introduction event likely occurred from Europe; (2) genetic diversification and inter-island dispersal postdated the emergence of the oldest island (Santa Maria, 8.12 Ma); (3) the genetic differentiation found in populations on the islands with higher age and smaller distance to the continent is significantly higher than that on the younger, more remote ones; (4) the high number of haplotypes observed (16), and the widespread distribution of the most frequent and ancestral ones across the archipelago, are indicating early diversification, demographic expansion, and recurrent dispersal. In contrast, restriction of six of the seven derived haplotypes to single islands is construed as reflecting significant isolation time prior to colonization.
Our phylogeographic reconstruction points to the sequence of island emergence as the key factor to explain the distribution of plastid DNA variation. The reproductive traits of this juniper species (anemophily, ornithochory, multi-seeded cones), together with its broad ecological range, appear to be largely responsible for recurrent inter-island colonization of ancestral haplotypes. In contrast, certain delay in colonization of new haplotypes may reflect intraspecific habitat competition on islands where this juniper was already present.
PMCID: PMC3218011  PMID: 22110727
17.  Phylogeography of the Tree Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) and the Influence of Quaternary Climate Changes in the Brazilian Cerrado 
Annals of Botany  2007;100(6):1219-1228.
Background and Aims
Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) is an endemic tree from the Brazilian cerrado (savanna vegetation), a biome classified as a hotspot for conservation priority. This study investigates the phylogeographic structure of H. stigonocarpa, in order to understand the processes that have led to its current spatial genetic pattern.
The polymorphism level and spatial distribution of variants of the plastid non-coding region between the genes psbC and trnS were investigated in 175 individuals from 17 populations, covering the greater part of the total distribution of the species. Molecular diversity indices were calculated and intra-specific relationships were inferred by the construction of haplotype networks using the median-joining method. Genetic differentiation among populations and main geographical groups was evaluated using spatial analysis of molecular variance (SAMOVA).
Key Results
Twenty-three different haplotypes were identified. The level of differentiation among the populations analysed was relatively high (FST = 0·692). Phylogeographic analyses showed a clear association between the haplotype network and geographic distribution of populations, revealing three main geographical groups: western, central and eastern. SAMOVA corroborated this finding, indicating that most of the variation can be attributed to differences among these three groups (58·8 %), with little difference among populations within groups (FSC = 0·252).
The subdivision of the geographic distribution of H. stigonocarpa populations into three genetically differentiated groups can be associated with Quaternary climatic changes. The data suggest that during glacial times H. stigonocarpa populations became extinct in most parts of the southern present-day cerrado area. Milder climatic conditions in the north and eastern portions of the cerrado resulted in maintenance of populations in these regions. Thus it is inferred that the most southern part of the present-day cerrado was re-colonized by different lineages from northern parts of this biome, after postglacial climate amelioration.
PMCID: PMC2759258  PMID: 17881340
Biogeography; cerrado; genetic structure; Quaternary climate changes; Fabaceae; Leguminosae; Hymenaea stigonocarpa; neotropical savannas; Pleistocene; phylogeography; psbC-trnS
18.  Phylogeography and historical demography of the Lusitanian snail Elona quimperiana reveal survival in unexpected separate glacial refugia 
Present day distributions of Palearctic taxa in northern latitudes mainly result from populations having survived in local patches during the Late Pleistocene and/or from recolonizing populations from southern temperate refugia. If well-studied Mediterranean and eastern European refugia are widely accepted, some recent biogeographical assumptions still remain unclear, such as the occurrence of multiple glacial refugia in Iberia and cryptic refugia in northern Europe during the last glaciations. The Lusitanian snail Elona quimperiana has a remarkably disjunct distribution, limited to northwestern France (Brittany), northwestern Spain and the Basque Country. By describing the phylogeographical structure of this species across its entire range, the present study attempts to identify refugia and subsequent recolonization routes.
Results based on 16S and COI gene sequences showed that the low genetic diversity observed in the Brittany populations should be associated with a recent demographic expansion. By contrast, populations from Spain exhibit several differentiated lineages and are characterized by demographic equilibrium, while the Basque populations are the only ones harboring typical distinct haplotypes. The center of the star-like networks of both gene sequences is occupied by a common ancestral-like haplotype found in Brittany and Spain, which might have originated from the middle of Northern Spain (i.e. Asturias, eastern Lugo and western Cantabria). Estimates of the divergence time between the Spain-Brittany and Basque lineages strongly suggest that E. quimperiana survived the Pleistocene glaciations in distinct refugia on the Iberian Peninsula, one of which is situated in Picos de Europa, and the other in the Basque Country. The occurrence of a northern refugium in France cannot be rejected as of yet.
Present results confirm the Iberian origin of the land snail E. quimperiana and strongly support the emerging phylogeographic hypothesis of multiple refugia in Iberia during the last glaciations. The scenario of a spatial expansion of E. quimperiana from an Iberian refuge located in Asturias to northern areas provides the most probable explanation for the present distribution of this land snail. By harboring distinct haplotypes, the Basque Country populations appear to be of great importance in terms of potential adaptation, long term persistence and hence, the conservation of E. quimperiana.
PMCID: PMC2652461  PMID: 19099565
19.  Alpine Crossroads or Origin of Genetic Diversity? Comparative Phylogeography of Two Sympatric Microgastropod Species 
PLoS ONE  2012;7(5):e37089.
The Alpine Region, constituting the Alps and the Dinaric Alps, has played a major role in the formation of current patterns of biodiversity either as a contact zone of postglacial expanding lineages or as the origin of genetic diversity. In our study, we tested these hypotheses for two widespread, sympatric microgastropod taxa – Carychium minimum O.F. Müller, 1774 and Carychium tridentatum (Risso, 1826) (Gastropoda, Eupulmonata, Carychiidae) – by using COI sequence data and species potential distribution models analyzed in a statistical phylogeographical framework. Additionally, we examined disjunct transatlantic populations of those taxa from the Azores and North America. In general, both Carychium taxa demonstrate a genetic structure composed of several differentiated haplotype lineages most likely resulting from allopatric diversification in isolated refugial areas during the Pleistocene glacial periods. However, the genetic structure of Carychium minimum is more pronounced, which can be attributed to ecological constraints relating to habitat proximity to permanent bodies of water. For most of the Carychium lineages, the broader Alpine Region was identified as the likely origin of genetic diversity. Several lineages are endemic to the broader Alpine Region whereas a single lineage per species underwent a postglacial expansion to (re)colonize previously unsuitable habitats, e.g. in Northern Europe. The source populations of those expanding lineages can be traced back to the Eastern and Western Alps. Consequently, we identify the Alpine Region as a significant ‘hot-spot’ for the formation of genetic diversity within European Carychium lineages. Passive dispersal via anthropogenic means best explains the presence of transatlantic European Carychium populations on the Azores and in North America. We conclude that passive (anthropogenic) transport could mislead the interpretation of observed phylogeographical patterns in general.
PMCID: PMC3351404  PMID: 22606334
20.  Microbial diversity in the floral nectar of seven Epipactis (Orchidaceae) species 
MicrobiologyOpen  2013;2(4):644-658.
Floral nectar of animal-pollinated plants is commonly infested with microorganisms, yet little is known about the microorganisms inhabiting the floral nectar of orchids. In this study, we investigated microbial communities occurring in the floral nectar of seven Epipactis (Orchidaceae) species. Culturable bacteria and yeasts were isolated and identified by partially sequencing the small subunit (SSU) ribosomal RNA (rRNA) gene and the D1/D2 domains of the large subunit (LSU) rRNA gene, respectively. Using three different culture media, we found that bacteria were common inhabitants of the floral nectar of Epipactis. The most widely distributed bacterial operational taxonomic units (OTUs) in nectar of Epipactis were representatives of the family of Enterobacteriaceae, with an unspecified Enterobacteriaceae bacterium as the most common. In contrast to previous studies investigating microbial communities in floral nectar, very few yeast species (mainly of the genus Cryptococcus) were observed, and most of them occurred in very low densities. Total OTU richness (i.e., the number of bacterial and yeast OTUs per orchid species) varied between 4 and 20. Cluster analysis revealed that microbial communities of allogamous species differed from those of autogamous and facultatively autogamous species. This study extends previous efforts to identify microbial communities in floral nectar and indicates that the floral nectar of the orchids investigated mainly contained bacterial communities with moderate phylogenetic diversity.
PMCID: PMC3948608  PMID: 23836678
Bacteria; floral nectar; microbial communities; orchids; yeasts.
21.  Phylogeography and regional endemism of a passively dispersing zooplankter: mitochondrial DNA variation in rotifer resting egg banks. 
We investigated the phylogeography of the salt water rotifer Brachionus plicatilis, a cyclical parthenogen with passive dispersal mechanisms, using resting eggs recovered from saline lake sediments. Individual resting eggs were obtained from a large selection of lakes which were representative of five endorheic basins and the chain of coastal ponds in the Iberian Peninsula. The novel use of resting eggs allows the integration of seasonal and annual variations as well as the impact of stochastic effects such as drift and local extinction. A 653 bp fragment of the mitochondrial cytochrome oxidase subunit I (COI) gene was sequenced from 98 eggs. Our results revealed a deep phylogeographical structure in this species, with a division into two main lineages with distinct geographical distributions, which probably diverged at the beginning of the Pleistocene period. Most of the mitochondrial DNA haplotypes were restricted to single lakes. Nested clade analysis supported Early Pleistocene fragmentation of populations, low gene flow and some long-distance colonization. These conclusions contrast strongly with previous ideas on rotifer biogeography and this pattern is consistent with a recolonization of the Iberian Peninsula from two glacial refugia. The results provide new insights into the processes responsible for the genetic diversification of passive dispersers, a life-history trait typical of zooplanktonic biotas.
PMCID: PMC1690794  PMID: 11413632
22.  DNA Barcoding the Canadian Arctic Flora: Core Plastid Barcodes (rbcL + matK) for 490 Vascular Plant Species 
PLoS ONE  2013;8(10):e77982.
Accurate identification of Arctic plant species is critical for understanding potential climate-induced changes in their diversity and distributions. To facilitate rapid identification we generated DNA barcodes for the core plastid barcode loci (rbcL and matK) for 490 vascular plant species, representing nearly half of the Canadian Arctic flora and 93% of the flora of the Canadian Arctic Archipelago. Sequence recovery was higher for rbcL than matK (93% and 81%), and rbcL was easier to recover than matK from herbarium specimens (92% and 77%). Distance-based and sequence-similarity analyses of combined rbcL + matK data discriminate 97% of genera, 56% of species, and 7% of infraspecific taxa. There is a significant negative correlation between the number of species sampled per genus and the percent species resolution per genus. We characterize barcode variation in detail in the ten largest genera sampled (Carex, Draba, Festuca, Pedicularis, Poa, Potentilla, Puccinellia, Ranunculus, Salix, and Saxifraga) in the context of their phylogenetic relationships and taxonomy. Discrimination with the core barcode loci in these genera ranges from 0% in Salix to 85% in Carex. Haplotype variation in multiple genera does not correspond to species boundaries, including Taraxacum, in which the distribution of plastid haplotypes among Arctic species is consistent with plastid variation documented in non-Arctic species. Introgression of Poa glauca plastid DNA into multiple individuals of P. hartzii is problematic for identification of these species with DNA barcodes. Of three supplementary barcode loci (psbA–trnH, psbK–psbI, atpF–atpH) collected for a subset of Poa and Puccinellia species, only atpF–atpH improved discrimination in Puccinellia, compared with rbcL and matK. Variation in matK in Vaccinium uliginosum and rbcL in Saxifraga oppositifolia corresponds to variation in other loci used to characterize the phylogeographic histories of these Arctic-alpine species.
PMCID: PMC3865322  PMID: 24348895
23.  The evolutionary history of Antirrhinum in the Pyrenees inferred from phylogeographic analyses 
The origin and colonisation history after the Quaternary ice ages remain largely unresolved for many plant lineages, mainly owing to a lack of fine-scale studies. Here, we present a molecular phylogeny and a phylogeographic analysis of Antirrhinum, an important model system in plant biology, in the Pyrenees range. Our goal was to reconstruct the evolutionary and colonisation history of four taxa endemic to this region (A. majus subsp. majus, A. majus. subsp. striatum, A. molle, and A. sempervirens) by using a dense sampling strategy, with a total of 452 individuals from 99 populations whose collective distribution spans nearly the entirety of the Pyrenees and adjacent mountains.
Phylogenetic and phylogeographic analyses of the sequences of two plastid (trnS-trnG and trnK-matK) regions revealed the following: (i) historical relationship between the Pyrenees and Iberia (but not with the Alps); (ii) the long persistence of populations in the Pyrenees, at least since the Late Pleistocene; (iii) three different colonisation histories for populations from the Western, Central, and Eastern Pyrenees; (iv) the deep phylogeographic separation of the eastern and western populations; and (v) the colonisation of southern France from the Eastern Pyrenees.
The present study underlines the enormous influence of the glacial history of the mountain ranges on the current configuration of intra- and inter-specific genetic diversity in Antirrhinum, as well as the importance of periglacial areas for the survival of species during glacial periods of the Quaternary.
PMCID: PMC4099501  PMID: 24970688
Antirrhinum; Phylogeny; Phylogeography; Pyrenees; Quaternary
24.  Phylogeography and demographic history of Lacerta lepida in the Iberian Peninsula: multiple refugia, range expansions and secondary contact zones 
The Iberian Peninsula is recognized as an important refugial area for species survival and diversification during the climatic cycles of the Quaternary. Recent phylogeographic studies have revealed Iberia as a complex of multiple refugia. However, most of these studies have focused either on species with narrow distributions within the region or species groups that, although widely distributed, generally have a genetic structure that relates to pre-Quaternary cladogenetic events. In this study we undertake a detailed phylogeographic analysis of the lizard species, Lacerta lepida, whose distribution encompasses the entire Iberian Peninsula. We attempt to identify refugial areas, recolonization routes, zones of secondary contact and date demographic events within this species.
Results support the existence of 6 evolutionary lineages (phylogroups) with a strong association between genetic variation and geography, suggesting a history of allopatric divergence in different refugia. Diversification within phylogroups is concordant with the onset of the Pleistocene climatic oscillations. The southern regions of several phylogroups show a high incidence of ancestral alleles in contrast with high incidence of recently derived alleles in northern regions. All phylogroups show signs of recent demographic and spatial expansions. We have further identified several zones of secondary contact, with divergent mitochondrial haplotypes occurring in narrow zones of sympatry.
The concordant patterns of spatial and demographic expansions detected within phylogroups, together with the high incidence of ancestral haplotypes in southern regions of several phylogroups, suggests a pattern of contraction of populations into southern refugia during adverse climatic conditions from which subsequent northern expansions occurred. This study supports the emergent pattern of multiple refugia within Iberia but adds to it by identifying a pattern of refugia coincident with the southern distribution limits of individual evolutionary lineages. These areas are important in terms of long-term species persistence and therefore important areas for conservation.
PMCID: PMC3141430  PMID: 21682856
25.  Phylogeographical Studies of Ascaris spp. Based on Ribosomal and Mitochondrial DNA Sequences 
The taxonomic distinctiveness of Ascaris lumbricoides and A. suum, two of the world's most significant nematodes, still represents a much-debated scientific issue. Previous studies have described two different scenarios in transmission patterns, explained by two hypotheses: (1) separated host-specific transmission cycles in highly endemic regions, (2) a single pool of infection shared by humans and pigs in non-endemic regions. Recently, A. suum has been suggested as an important cause of human ascariasis in endemic areas such as China, where cross-infections and hybridization have also been reported. The main aims of the present study were to investigate the molecular epidemiology of human and pig Ascaris from non-endemic regions and, with reference to existing data, to infer the phylogenetic and phylogeographic relationships among the samples.
151 Ascaris worms from pigs and humans were characterized using PCR-RFLP on nuclear ITS rDNA. Representative geographical sub-samples were also analysed by sequencing a portion of the mitochondrial cox1 gene, to infer the extent of variability at population level. Sequence data were compared to GenBank sequences from endemic and non-endemic regions.
Principal Findings
No fixed differences between human and pig Ascaris were evident, with the exception of the Slovak population, which displays significant genetic differentiation. The RFLP analysis confirmed pig as a source of human infection in non-endemic regions and as a corridor for the promulgation of hybrid genotypes. Epidemiology and host-affiliation seem not to be relevant in shaping molecular variance. Phylogenetic and phylogeographical analyses described a complex scenario, involving multiple hosts, sporadic contact between forms and an ancestral taxon referable to A. suum.
These results suggest the existence of homogenizing gene flow between the two taxa, which appear to be variants of a single polytypic species. This conclusion has implications on the systematics, transmission and control programs relating to ascariasis.
Author Summary
Ascaris lumbricoides, the world's most common human nematode, and A. suum, the pig roundworm, are two of the most important soil-transmitted helminthes of public health and socio-economic concern. However, previously documented similarities at the morphological and genetic level, coupled with evidence for hybridization and gene flow, have clouded the taxonomic distinctiveness of these two nematodes. To date, molecular epidemiological studies have been carried out, mostly in highly endemic regions, where two different transmission cycles have been described. Recently, pigs have been recognized as an important source of human ascariasis in China, opening questions about the zoonotic potential and the efficiency of control programs. Here, samples from non-endemic regions have been analysed using a nuclear marker to identify nematodes to species level plus a mitochondrial marker to investigate the phylogeographic relationships among individuals of the two species from both endemic and non-endemic regions. Results obtained suggested that A. suum and A. lumbricoides may be variants of the same species, with the lack of fixed genetic differences and considerable phylogeographic admixture confirming an extremely close evolutionary relationship among these nematodes. This study highlights the need to further explore the evolutionary affinities of the two taxa to help shed light on the epidemiology of ascariasis.
PMCID: PMC3623706  PMID: 23593529

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