The integration of multiple independent data reveals an unusual response to Pleistocene climatic changes in the hard tick Ixodes ricinus

In the last few years, improved analytical tools and the integration of genetic data with multiple sources of information have shown that temperate species exhibited more complex responses to ice ages than previously thought. In this study, we investigated how Pleistocene climatic changes affected the current distribution and genetic diversity of European populations of the tick Ixodes ricinus, an ectoparasite with high ecological plasticity. We first used mitochondrial and nuclear genetic markers to investigate the phylogeographic structure of the species and its Pleistocene history using coalescent‐based methods; then we used species distribution modelling to infer the climatic niche of the species at last glacial maximum; finally, we reviewed the literature on the I. ricinus hosts to identify the locations of their glacial refugia. Our results support the scenario that during the last glacial phase, I. ricinus never experienced a prolonged allopatric divergence in separate glacial refugia, but persisted with interconnected populations across Southern and Central Europe. The generalist behaviour in host choice of I. ricinus would have played a major role in maintaining connections between its populations. Although most of the hosts persisted in separate refugia, from the point of view of I. ricinus, they represented a continuity of ‘bridges’ among populations. Our study highlights the importance of species‐specific ecology in affecting responses to Pleistocene glacial–interglacial cycles. Together with other cases in Europe and elsewhere, it contributes to setting new hypotheses on how species with wide ecological plasticity coped with Pleistocene climatic changes.     

Holarctic phylogeography of the tundra shrew (Sorex tundrensis) based on mitochondrial genes

A range‐wide phylogeographic study of the tundra shrew (Sorex tundrensis) was performed using cytochrome b and cytochrome oxidase I (COI) mitochondrial genes. The results based on 121 specimens from 42 localities demonstrate that the tundra shrew is divided into five main mitochondrial DNA phylogenetic lineages with largely parapatric distribution. In addition to a single Nearctic clade (Alaska) four Palearctic clades are identified: Western (Northen Urals, Kazakhstan, South‐West Siberia), Eastern (from East Transbaikalia and the Middle Amur to Chukotka), South Central (Central Siberia, the Altai, the Dzhungarian Alatau) and North Central (Northern Siberia, Central Yakutia). Date estimates obtained by use of a molecular clock corrected for potential rate decay suggest Late Pleistocene age for the most recent common ancestor of all contemporary tundra shrew populations. Relatively high genetic divergence between phylogroups (0.95–1.6%) indicates that the observed phylogeographic structure was initiated by historical events that predated the Last Glacial Maximum. We assume that, being more cold‐ and arid‐tolerant, tundra shrew underwent expansion during an early cold phase of the Last Glacial and spread through its recent range earlier than most of other Siberian red‐toothed shrews. Comparative phylogeographic analysis of Siberian shrews and rodents suggests that evolutionary histories of species associated with azonal or open habitats show important differences compared to forest species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 721–746.     

Climate,physiological tolerance and sex‐biased dispersal shape genetic structure of Neotropical orchid bees

Understanding the impact of past climatic events on the demographic history of extant species is critical for predicting species' responses to future climate change. Palaeoclimatic instability is a major mechanism of lineage diversification in taxa with low dispersal and small geographical ranges in tropical ecosystems. However, the impact of these climatic events remains questionable for the diversification of species with high levels of gene flow and large geographical distributions. In this study, we investigate the impact of Pleistocene climate change on three Neotropical orchid bee species (Eulaema bombiformis, E. meriana and E. cingulata) with transcontinental distributions and different physiological tolerances. We first generated ecological niche models to identify species‐specific climatically stable areas during Pleistocene climatic oscillations. Using a combination of mitochondrial and nuclear markers, we inferred calibrated phylogenies and estimated historical demographic parameters to reconstruct the phylogeographical history of each species. Our results indicate species with narrower physiological tolerance experienced less suitable habitat during glaciations and currently exhibit strong population structure in the mitochondrial genome. However, nuclear markers with low and high mutation rates show lack of association with geography. These results combined with lower migration rate estimates from the mitochondrial than the nuclear genome suggest male‐biased dispersal. We conclude that despite large effective population sizes and capacity for long‐distance dispersal, climatic instability is an important mechanism of maternal lineage diversification in orchid bees. Thus, these Neotropical pollinators are susceptible to disruption of genetic connectivity in the event of large‐scale climatic changes.     

Range instability leads to cytonuclear discordance in a morphologically cryptic ground squirrel species complex

The processes responsible for cytonuclear discordance frequently remain unclear. Here, we employed an exon capture data set and demographic methods to test hypotheses generated by species distribution models to examine how contrasting histories of range stability vs. fluctuation have caused cytonuclear concordance and discordance in ground squirrel lineages from the Otospermophilus beecheyi species complex. Previous studies in O. beecheyi revealed three morphologically cryptic and highly divergent mitochondrial DNA lineages (named the Northern, Central and Southern lineages based on geography) with only the Northern lineage exhibiting concordant divergence for nuclear genes. Here, we showed that these mtDNA lineages likely formed in allopatry during the Pleistocene, but responded differentially to climatic changes that occurred since the last interglacial (~120,000 years ago). We find that the Northern lineage maintained a stable range throughout this period, correlating with genetic distinctiveness among all genetic markers and low migration rates with the other lineages. In contrast, our results suggested that the Southern lineage expanded from Baja California Sur during the Late Pleistocene to overlap and potentially swamp a contracting Central lineage. High rates of intraspecific gene flow between Southern lineage individuals among expansion origin and expansion edge populations largely eroded Central ancestry from autosomal markers. However, male‐biased dispersal in this system preserved signals of this past hybridization and introgression event in matrilineal‐biased X‐chromosome and mtDNA markers. Our results highlight the importance of range stability in maintaining the persistence of phylogeographic lineages, whereas unstable range dynamics can increase the tendency for lineages to merge upon secondary contact.     

Increased genetic structuring of isolated Salamandra salamandra populations (Caudata: Salamandridae) at the margins of the Carpathian Mountains

The traditional southern Pleistocene refugia hypothesis in Europe has lately been challenged for several animal and plant species. The Carpathian Basin, especially at the marginal regions, is one of the recently recognized biodiversity hotspots in Europe. Marginal populations are prone to have lower genetic diversity and higher genetic differentiation than central populations. Here, we examined one mitochondrial DNA fragment (D‐loop) and nine nuclear (microsatellite) loci to describe the genetic diversity and phylogeographical pattern of fire salamander (Salamandra salamandra) populations in the Carpathian Basin with focusing on the southern margins of the Western Carpathians, where isolated populations of this species are present. Analyses of microsatellites indicated reduced genetic diversity for most of the isolated populations. Based on the mitochondrial DNA, only two haplotypes were found, whereas the analyses with the nuclear markers revealed a more recent genetic split between Western (Alpine) and Eastern (Carpathian) populations, and separated the Apuseni Mountains population (part of the Western Carpathians). Using approximate Bayesian computation analyses, we identified the most probable colonization scenario for the isolated North Hungarian Carpathian Basin populations. The split between isolated salamander populations from the central populations in the Carpathian Mountains dates back to the beginning of the Late Pleistocene, while the split between most of the Hungarian populations can be associated with the Last Glacial Maximum. We found evidence for long‐time isolation between the marginal Carpathian Basin and central populations. Our results also show that S. salamandra survived glacial periods in the temperate forests of north‐east Pannonia (North Hungarian Mountains), confirming that the Carpathian Basin served as important northerly refugia during the Pleistocene climatic oscillations.     

Pleistocene diversification in Morocco and recent demographic expansion in the Mediterranean pond turtle Mauremys leprosa

Quaternary climatic oscillations and geographic barriers have strongly influenced the distribution and diversification of thermophilic species occurring in the Mediterranean Basin. The Western Mediterranean pond turtle, Mauremys leprosa, is widely distributed throughout the Iberian Peninsula, southern France and most of the Maghreb region, with two subspecies currently recognized. In this work, we used 566 samples, including 259 new individuals, across the species range, and sequenced two mitochondrial markers (cytochrome b gene and control region; 163 samples in a concatenated mtDNA dataset) and one nuclear intron (R35; 23 samples representing all identified sublineages) to study the evolutionary history of M. leprosa. We combined phylogenetic methods and phylogeographic continuous diffusion models with spatial analysis. Our results (1) show a high level of genetic structure in Morocco originated during the Pleistocene; (2) reveal two independent population expansion waves from Morocco to Tunisia and to southern Europe, which later expanded throughout the Iberian Peninsula, and (3) identify several secondary contact zones in Morocco. Our study also sheds new light on the role of geographical features (Moroccan mountains ranges and the Strait of Gibraltar) and Pleistocene climatic oscillations in shaping genetic diversity and structure of M. leprosa, and underlines the importance of the Maghreb as a differentiation centre harbouring distinct glacial refugia.     

Looking into the past – the reaction of three grouse species to climate change over the last million years using whole genome sequences

Tracking past population fluctuations can give insight into current levels of genetic variation present within species. Analysing population dynamics over larger timescales can be aligned to known climatic changes to determine the response of species to varying environments. Here, we applied the Pairwise Sequentially Markovian Coalescent (psmc ) model to infer past population dynamics of three widespread grouse species; black grouse, willow grouse and rock ptarmigan. This allowed the tracking of the effective population size (N_e) of all three species beyond 1 Mya, revealing that (i) early Pleistocene cooling (~2.5 Mya) caused an increase in the willow grouse and rock ptarmigan populations, (ii) the mid‐Brunhes event (~430 kya) and following climatic oscillations decreased the N_e of willow grouse and rock ptarmigan, but increased the N_e of black grouse and (iii) all three species reacted differently to the last glacial maximum (LGM) – black grouse increased prior to it, rock ptarmigan experienced a severe bottleneck and willow grouse was maintained at large population size. We postulate that the varying psmc signal throughout the LGM depicts only the local history of the species. Nevertheless, the large population fluctuations in willow grouse and rock ptarmigan indicate that both species are opportunistic breeders while black grouse tracks the climatic changes more slowly and is maintained at lower N_e. Our results highlight the usefulness of the psmc approach in investigating species’ reaction to climate change in the deep past, but also that caution should be taken in drawing general conclusions about the recent past.     

Molecular data and species distribution models reveal the Pleistocene history of the mayfly Ameletus inopinatus (Ephemeroptera: Siphlonuridae)1

1. We investigated the Pleistocene and Holocene history of the rare mayfly Ameletus inopinatus EATON 1887 (Ephemeroptera: Siphlonuridae) in Europe. We used A. inopinatus as a model species to explore the phylogeography of montane, cold‐tolerant aquatic insects with arctic–alpine distributions. 2. Using species distribution models, we developed hypotheses about the species demographic history in Central Europe and the recolonisation history of Fennoscandia. We tested these hypotheses using mitochondrial cytochrome oxidase I (mtCOI) sequence data and compared our genetic results with previously generated microsatellite data to explore genetic diversity distributions of A. inopinatus. 3. We observed old lineages, deep splits and almost complete lineage sorting of mtCOI sequences among mountain ranges. These results support a periglacial survival, i.e. persistence at the periphery of Pleistocene glaciers in Central Europe. 4. There was strong differentiation between the Fennoscandian and all other populations, indicating that Fennoscandia was recolonised from a refugium not accounted for in our sampling. High degrees of population genetic structure within the northern samples suggest that Fennoscandia was recolonised by more than one lineage. However, this structure was not apparent in previously published microsatellite data, consistent with secondary contact without sexual incompatibility or with sex‐biased dispersal. 5. Our demographic analyses indicate that (i) the separation of northern and Central European lineages occurred during the early Pleistocene; (ii) Central European populations have persisted independently throughout the Pleistocene and (iii) the species extended its range about 150 000 years ago.     

Lineage-specific late pleistocene expansion of an endemic subtropical gossamer-wing damselfly, Euphaea formosa, in Taiwan

Background  

Pleistocene glacial oscillations have significantly affected the historical population dynamics of temperate taxa. However, the general effects of recent climatic changes on the evolutionary history and genetic structure of extant subtropical species remain poorly understood. In the present study, phylogeographic and historical demographic analyses based on mitochondrial and nuclear DNA sequences were used. The aim was to investigate whether Pleistocene climatic cycles, paleo-drainages or mountain vicariance of Taiwan shaped the evolutionary diversification of a subtropical gossamer-wing damselfly, Euphaea formosa.     

Pleistocene glacial cycle effects on the phylogeography of the Chinese endemic bat species, <Emphasis Type="Italic">Myotis davidii</Emphasis>

Background  

Global climatic oscillations, glaciation cycles and the unique geographic topology of China have profoundly influenced species population distributions. In most species, contemporary distributions of populations cannot be fully understood, except in a historical context. Complex patterns of Pleistocene glaciations, as well as other physiographic changes have influenced the distribution of bat species in China. Until this study, there had been no phylogeographical research on Myotis davidii, an endemic Chinese bat. We used a combination of nuclear and mitochondrial DNA markers to investigate genetic diversity, population structure, and the demographic history of M. davidii. In particular, we compared patterns of genetic variation to glacial oscillations, topography, and environmental variation during the Pleistocene in an effort to explain current distributions in light of these historical processes.     

Testing for shared biogeographic history in the lower Central American freshwater fish assemblage using comparative phylogeography: concerted,independent, or multiple evolutionary responses?

A central goal of comparative phylogeography is determining whether codistributed species experienced (1) concerted evolutionary responses to past geological and climatic events, indicated by congruent spatial and temporal patterns (“concerted‐response hypothesis”); (2) independent responses, indicated by spatial incongruence (“independent‐response hypothesis”); or (3) multiple responses (“multiple‐response hypothesis”), indicated by spatial congruence but temporal incongruence (“pseudocongruence”) or spatial and temporal incongruence (“pseudoincongruence”). We tested these competing hypotheses using DNA sequence data from three livebearing fish species codistributed in the Nicaraguan depression of Central America (Alfaro cultratus, Poecilia gillii, and Xenophallus umbratilis) that we predicted might display congruent responses due to co‐occurrence in identical freshwater drainages. Spatial analyses recovered different subdivisions of genetic structure for each species, despite shared finer‐scale breaks in northwestern Costa Rica (also supported by phylogenetic results). Isolation‐with‐migration models estimated incongruent timelines of among‐region divergences, with A. cultratus and Xenophallus populations diverging over Miocene–mid‐Pleistocene while P. gillii populations diverged over mid‐late Pleistocene. Approximate Bayesian computation also lent substantial support to multiple discrete divergences over a model of simultaneous divergence across shared spatial breaks (e.g., Bayes factor [B₁₀] = 4.303 for Ψ [no. of divergences] > 1 vs. Ψ = 1). Thus, the data support phylogeographic pseudoincongruence consistent with the multiple‐response hypothesis. Model comparisons also indicated incongruence in historical demography, for example, support for intraspecific late Pleistocene population growth was unique to P. gillii, despite evidence for finer‐scale population expansions in the other taxa. Empirical tests for phylogeographic congruence indicate that multiple evolutionary responses to historical events have shaped the population structure of freshwater species codistributed within the complex landscapes in/around the Nicaraguan depression. Recent community assembly through different routes (i.e., different past distributions or colonization routes), and intrinsic ecological differences among species, has likely contributed to the unique phylogeographical patterns displayed by these Neotropical fishes.     

Phylogeography of the heavily poached African common pangolin (Pholidota,Manis tricuspis) reveals six cryptic lineages as traceable signatures of Pleistocene diversification

Knowledge on faunal diversification in African rainforests remains scarce. We used phylogeography to assess (i) the role of Pleistocene climatic oscillations in the diversification of the African common pangolin (Manis tricuspis) and (ii) the utility of our multilocus approach for taxonomic delineation and trade tracing of this heavily poached species. We sequenced 101 individuals for two mitochondrial DNA (mtDNA), two nuclear DNA and one Y‐borne gene fragments (totalizing 2602 bp). We used a time‐calibrated, Bayesian inference phylogenetic framework and conducted character‐based, genetic and phylogenetic delineation of species hypotheses within African common pangolins. We identified six geographic lineages partitioned into western Africa, Ghana, the Dahomey Gap, western central Africa, Gabon and central Africa, all diverging during the Middle to Late Pleistocene. MtDNA (cytochrome b + control region) was the sole locus to provide diagnostic characters for each of the six lineages. Tree‐based Bayesian delimitation methods using single‐ and multilocus approaches gave high support for ‘species’ level recognition of the six African common pangolin lineages. Although the diversification of African common pangolins occurred during Pleistocene cyclical glaciations, causative correlation with traditional rainforest refugia and riverine barriers in Africa was not straightforward. We conclude on the existence of six cryptic lineages within African common pangolins, which might be of major relevance for future conservation strategies. The high discriminative power of the mtDNA markers used in this study should allow an efficient molecular tracing of the regional origin of African common pangolin seizures.     

Congruent phylogeographical patterns of eight tree species in Atlantic Central Africa provide insights into the past dynamics of forest cover

Cycles of Quaternary climatic change are assumed to be major drivers of African rainforest dynamics and evolution. However, most hypotheses on past vegetation dynamics relied on palaeobotanical records, an approach lacking spatial resolution, and on current patterns of species diversity and endemism, an approach confounding history and environmental determinism. In this context, a comparative phylogeographical study of rainforest species represents a complementary approach because Pleistocene climatic fluctuations may have left interpretable signatures in the patterns of genetic diversity within species. Using 1274 plastid DNA sequences from eight tree species (Afrostyrax kamerunensis, A. lepidophyllus, Erythrophleum suaveolens, Greenwayodendron suaveolens, Milicia excelsa, Santiria trimera, Scorodophloeus zenkeri and Symphonia globulifera) sampled in 50 populations of Atlantic Central Africa (ACA), we averaged divergence across species to produce the first map of the region synthesizing genetic distinctiveness and standardized divergence within and among localities. Significant congruence in divergence was detected mostly among five of the eight species and was stronger in the northern ACA. This pattern is compatible with a scenario of past forest fragmentation and recolonization whereby forests from eastern Cameroon and northeastern Gabon would have been more affected by past climatic change than those of western Cameroon (where one or more refugia would have occurred). By contrast, southern ACA (Gabon) displayed low congruence among species that may reflect less drastic past forest fragmentation or a more complex history of vegetation changes. Finally, we also highlight the potential impact of current environmental barriers on spatial genetic structures.     

Species‐level phylogeographical history of the endemic species Calligonum roborovskii and its close relatives in Calligonum section Medusa (Polygonaceae) in arid north‐western China

Quaternary climatic oscillations appear to have influenced the genetic diversity and evolutionary history of arid‐adapted plants. To understand the processes involved and reveal evolutionary relationships, haplotypes were examined from Calligonum roborovskii, an endemic species occurring in the arid zones across the desert regions of north‐western China, and seven other species also from Calligonum section Medusa, including C. gobicum, C. mongolicum and the narrow endemic species C. ebi‐nuricum, C. pumilum, C. taklimakanense, C. trifarium and C. yengisaricum. Forty‐three haplotypes were identified in 422 individuals from 51 natural populations, from variation of two plastid DNA intergenic spacers (rpl32‐trnL and ycf6‐psbM). A high level of total genetic diversity was found across species for which more than two populations were examined, including C. gobicum, C. mongolicum, C. pumilum and C. roborovskii. A distinct isolation‐by‐distance pattern in each of these species was suggested by the Mantel test, indicating that restricted gene flow caused high genetic differentiation among populations. Three haplotypes were shared by two or three species each, but the other 40 haplotypes were species‐specific. The 43 haplotypes split into three major clades, but not species‐specific lineages; most of the Calligonum species were not reciprocally monophyletic, probably due to incomplete lineage sorting or introgression. The identified haplotypes were dated to 1.97 Mya (95% highest posterior density: 2.95–0.99 Mya) and diverged until the late Pleistocene, possibly linked to aridification and enlargement of deserts caused by climate changes. Variation of desert habitats during the Pleistocene might play a key role in causing the divergence.     

Spatial Patterns of Haplotype Variation in the Epiphytic Bromeliad Catopsis nutans

Identifying factors governing the origin, distribution, and maintenance of Neotropical plant diversity is an enduring challenge. To explore the complex and dynamic historical processes that shaped contemporary genetic patterns for a Central American plant species, we investigated the spatial distribution of chloroplast haplotypes of a geographically and environmentally widespread epiphytic bromeliad with wind‐dispersed seeds, Catopsis nutans, in Costa Rica. We hypothesized that genetic discontinuities occur between northwestern and southwestern Pacific slope populations, resembling patterns reported for other plant taxa in the region. Using non‐coding chloroplast DNA from 469 individuals and 23 populations, we assessed the influences of geographic and environmental distance as well as historical climatic variation on the genetic structure of populations spanning >1200 m in elevation. Catopsis nutans revealed seven haplotypes with low within‐population diversity (mean haplotype richness = 1.2) and moderate genetic structure (F_ST = 0.699). Pairwise F_ST was significantly correlated with both geographic and environmental distance. The frequency of dominant haplotypes was significantly correlated with elevation. A cluster of nine Pacific lowland populations exhibited a distinct haplotype profile and contained five of the seven haplotypes, suggesting historical isolation and limited seed‐mediated gene flow with other populations. Paleodistribution models indicated lowland and upland habitats in this region were contiguous through past climatic oscillations. Based on our paleodistribution analysis and comparable prior phylogeographic studies, the genetic signature of recent climatic oscillations are likely superimposed upon the distribution of anciently divergent lineages. Our study highlights the unique phylogeographic history of a Neotropical plant species spanning an elevation gradient.     

The influence of climate on morphometric traits of fossil populations of Microtus arvalis and M. agrestis from the Carpathian Basin,northern Hungary

In this study, we analysed morphometrically fossil populations of Microtus arvalis and M. agrestis from eight late Middle to Late Pleistocene archaeological and palaeontological sites in the Carpathian Basin, northern Hungary. The intra‐ and interspecific variations in both species can be related to climatic oscillations linked to the onset of the Eemian interglacial and the first phases of Marine Isotope Stage 5. The size of M. agrestis can be correlated with the presence/absence of relatively humid climatic and environmental conditions and of surface water resources (such as marshes and flooded areas). A possible immigration event of M. arvalis populations into the Carpathian Basin, also related to the Eemian interglacial, is also identified.     

Fossil evidence and phylogeography of temperate species: 'glacial refugia' and post-glacial recolonization

We present a short synthesis of the Pleistocene distribution dynamics and phylogeographic recolonization hypotheses for two temperate European mammal species, the red deer ( Cervus elaphus ) and the roe deer ( Capreolus capreolus ), for which high-resolution patterns of fossil evidence and genetic data sets are available. Such data are critical to an understanding of the role of hypothesized glacial refugia. Both species show a similar pattern: a relatively wide distribution in the southern part of Central Europe 60,000–25,000 years ago, and a strong restriction to areas in southern Europe for nearly 10,000 years during the Last Glacial Maximum (LGM) and the early Late Glacial (25,000–14,700 years ago). With the beginning of Greenland Interstadial 1 (Bølling/Allerød warming, c. 14,700–11,600 years ago) a sudden range expansion into Central Europe is visible, but the colonization of most of Central Europe, including the northern European Lowlands, only began in the early Holocene. In a European context, regions where the species were distributed during the LGM and early Late Glacial are most relevant as potential origins of recolonization processes, because during these c. 10,000 years distribution ranges were smaller than at any other time in the Late Quaternary. As far as the present distribution of temperate species and their genetic lineages is concerned, so-called 'cryptic refugia' are important only if the species are actually confirmed there during the LGM, as otherwise they could not possibly have contributed to the recolonization that eventually resulted in the present distribution ranges.     

Late Pleistocene climate change promoted divergence between Picea asperata and P. crassifolia on the Qinghai–Tibet Plateau through recent bottlenecks

Divergence during the early stage of speciation can be driven by a population bottleneck via reduced gene flow and enhanced lineage sorting. In this study, we aimed to examine whether such bottlenecks occurred during the initial speciation of two closely related spruce species Picea asperata and P. crassifolia occurring on the Qinghai–Tibet Plateau (QTP). We analyzed sequences of three chloroplast, two mitochondrial DNA fragments and a further 13 nuclear loci from 216 individuals of the two species. Both species showed a low level of genetic diversity in contrast to other congeners occurring in the QTP and adjacent regions. The estimated population sizes of P. asperata and P. crassifolia are less than the ancestral population size before splitting. These results together with multiple statistical tests (Tajima's D, Fu and Li's D* and F*) suggest that these two species underwent recent bottlenecks. Based on approximate Bayesian computation (ABC), we also determined that the period of the population shrinkage was consistent with the interspecific divergence during the late Pleistocene. The reduced population sizes and the divergent selection may together have triggered the initial divergence under high gene flow between these two species. Our results therefore highlight the importance of climatic oscillations during the late Pleistocene in promoting speciation through changing demographic sizes of the ancestral species on the QTP and in adjacent regions.     

The Pleistocene demography of an alpine juniper of the Qinghai‐Tibetan Plateau: tabula rasa,cryptic refugia or something else?

Aim Numerous palaeoecological and genetic studies have shown that different tree species responded in very different ways to Pleistocene climatic oscillations. Some were forced into small refugia far from their current range, while others were able to survive in small refugia close to, or even within, their current natural range. In this study we examine the Pleistocene demography of a juniper species (Juniperus przewalskii, Cupressaceae) from the Qinghai‐Tibetan Plateau. Location The Qinghai‐Tibetan Plateau (QTP). Methods Eight nuclear loci were sequenced in 141 individuals from 20 natural populations distributed across the entire natural range of J. przewalskii, and coalescent analysis was used to test demographic hypotheses. Results The overall nucleotide diversity in the sample was low (π_sil = 0.0029), with few rare alleles and pronounced population genetic structure (F_ST = 0.181). We detected a division previously found using chloroplast DNA markers: all segregating sites in populations from the central part of the QTP appear to be a subset of those found around the edge of the plateau, confirming the relatively young age of the former. In contrast to the middle Pleistocene bottlenecks detected in boreal tree species, the coalescent‐based analyses failed to reject the standard neutral model for the juniper species considered here. Main conclusions Juniperus przewalskii did not undergo marked changes in population sizes during the Pleistocene, although this species seems to have experienced recent, post‐glacial expansion. This finding is largely consistent with the limited number of previous studies on conifer species of the QTP, but contradicts findings of studies on boreal species. These findings have wide implications for understanding plant species’ responses to past climatic oscillations on the high‐elevation QTP.     

The ancient Britons: groundwater fauna survived extreme climate change over tens of millions of years across NW Europe

Global climate changes during the Cenozoic (65.5–0 Ma) caused major biological range shifts and extinctions. In northern Europe, for example, a pattern of few endemics and the dominance of wide‐ranging species is thought to have been determined by the Pleistocene (2.59–0.01 Ma) glaciations. This study, in contrast, reveals an ancient subsurface fauna endemic to Britain and Ireland. Using a Bayesian phylogenetic approach, we found that two species of stygobitic invertebrates (genus Niphargus) have not only survived the entire Pleistocene in refugia but have persisted for at least 19.5 million years. Other Niphargus species form distinct cryptic taxa that diverged from their nearest continental relative between 5.6 and 1.0 Ma. The study also reveals an unusual biogeographical pattern in the Niphargus genus. It originated in north‐west Europe approximately 87 Ma and underwent a gradual range expansion. Phylogenetic diversity and species age are highest in north‐west Europe, suggesting resilience to extreme climate change and strongly contrasting the patterns seen in surface fauna. However, species diversity is highest in south‐east Europe, indicating that once the genus spread to these areas (approximately 25 Ma), geomorphological and climatic conditions enabled much higher diversification. Our study highlights that groundwater ecosystems provide an important contribution to biodiversity and offers insight into the interactions between biological and climatic processes.