Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis

The level of genetic differentiation within and between evolutionary lineages of the common vole (Microtus arvalis) in Europe was examined by analyzing mitochondrial sequences from the control region (mtDNA) and 12 nuclear microsatellite loci (nucDNA) for 338 voles from 18 populations. The distribution of evolutionary lineages and the affinity of populations to lineages were determined with additional sequence data from the mitochondrial cytochrome b gene. Our analyses demonstrated very high levels of differentiation between populations (overall FST: mtDNA 70%; nucDNA 17%). The affinity of populations to evolutionary lineages was strongly reflected in mtDNA but not in nucDNA variation. Patterns of genetic structure for both markers visualized in synthetic genetic maps suggest a postglacial range expansion of the species into the Alps, as well as a potentially more ancient colonization from the northeast to the southwest of Europe. This expansion is supported by estimates for the divergence times between evolutionary lineages and within the western European lineage, which predate the last glacial maximum (LGM). Furthermore, all measures of genetic diversity within populations increased significantly with longitude and showed a trend toward increase with latitude. We conclude that the detected patterns are difficult to explain only by range expansions from separate LGM refugia close to the Mediterranean. This suggests that some M. arvalis populations persisted during the LGM in suitable habitat further north and that the gradients in genetic diversity may represent traces of a more ancient colonization of Europe by the species.     

The divergence of two independent lineages of an endemic Chinese gecko,Gekko swinhonis,launched by the Qinling orogenic belt

The genetic structure and demographic history of an endemic Chinese gecko, Gekko swinhonis, were investigated by analysing the mitochondrial cytochrome b gene and 10 microsatellite loci for samples collected from 27 localities. Mitochondrial DNA data provided a detailed distribution of two highly divergent evolutionary lineages, between which the average pairwise distance achieved was 0.14. The geographic division of the two lineages coincided with a plate boundary consisting of the Qinling and Taihang Mts, suggesting a historical vicariant pattern. The orogeny of the Qinling Mts, a dispersal and major climatic barrier of the region, may have launched the independent lineage divergence. Both lineages have experienced recent expansion, and the current sympatric localities comprised the region of contact between the lineages. Individual‐based phylogenetic analyses of nucDNA and Bayesian‐clustering approaches revealed a deep genetic structure analogous to mtDNA. Incongruence between nucDNA and mtDNA at the individual level at localities outside of the contact region can be explained by the different inheritance patterns and male‐biased dispersal in this species. High genetic divergence, long‐term isolation and ecological adaptation, as well as the morphological differences, suggest the presence of a cryptic species.     

Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations

The phylogeography of the common vole (Microtus arvalis) was examined by analysing mitochondrial DNA (mtDNA) sequence variation in 1044 base pairs (bp) of the cytochrome b (cytb) gene and in 322 bp of the control region (ctr) among 106 individuals from 58 locations. The geographical distribution of four previously recognized cytb evolutionary lineages in Europe was refined and a new lineage was found in southern Germany. All lineages were distributed allopatrically, except in one sample that was probably located in a contact zone. The occurrence of several lineages in the Alps is in keeping with their recent recolonization from distinct sources. The translation of 84 cytb DNA sequences produced 33 distinct proteins with relationships that differed from those of the DNA haplotypes, suggesting that the mtDNA lineages did not diverge in response to selection. In comparison with M. agrestis, a neutrality test detected no overall evidence for selection in the cytb gene, but a closer examination of a structural model showed that evolutionarily conserved and functionally important positions were often affected. A new phylogeographical test of random accumulation of nonsynonymous mutations generated significant results in three lineages. We therefore conclude that the molecular diversity of cytb in M. arvalis is overall the result of the demographic history of the populations, but that there have been several episodes of local adaptation to peculiar environments.     

Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes

A species-wide phylogeographical study of the root vole (Microtus oeconomus) was performed using the whole 1140 base pair mitochondrial (mt) cytochrome b gene. We examined 83 specimens from 52 localities resulting in 65 unique haplotypes. Our results demonstrate that the root vole is divided into four main mtDNA phylogenetic lineages that seem to have largely allopatric distributions. Net divergence estimates (2.0-3.5%) between phylogroups, as well as relatively high nucleotide diversity estimates within phylogroups, indicate that the distinct phylogeographical structure was initiated by historical events that predated the latest glaciation. European root voles are divided into a Northern and a Central mtDNA phylogroup. The mtDNA data in concert with fossil records imply that root voles remained north of the classical refugial areas in southern Europe during the last glacial period. The currently fragmented populations in central Europe belong to a single mtDNA phylogroup. The Central Asian and the North European lineages are separated by the Ural Mountains, a phylogeographical split also found in collared lemmings (Dicrostonyx) and the common vole (M. arvalis). The Beringian lineage occurs from eastern Russia through Alaska to northwestern Canada. This distribution is congruent with the traditional boundaries of the Beringian refugium and with phylogeographical work on other organisms. In conclusion, similarities between the phylogeographical patterns in the root vole and other rodents, such as Arctic and subarctic lemmings, as well as more temperate vole species, indicate that late Quaternary geological and climatic events played a strong role in structuring northern biotic communities.     

Mitochondrial diversity and phylogeographic structure of Chinese domestic goats

China has numerous native domestic goat breeds, but so far there has been no extensive study on genetic diversity, population demographic history, and origin of Chinese goats. Here, we examined the genetic diversity and phylogeographic structure of Chinese domestic goats by determining a 481-bp fragment of the first hypervariable region of mitochondrial DNA (mtDNA) control region from 368 individuals representing 18 indigenous breeds. Phylogenetic analyses revealed that there were four mtDNA lineages (A-D) identified in Chinese goats, in which lineage A was predominant, lineage B was moderate, and lineages C and D were at low frequency. These results further support the multiple maternal origins of domestic goats. The pattern of genetic variation in goat mtDNA sequences indicated that the two larger lineages A and B had undergone population expansion events. In a combined analysis of previously reported sequences and our sequences belonging to lineage B, we detected two subclades, in which one was unique to eastern Asia and another was shared between eastern and southern Asia. A larger genetic variation in eastern Asia than southern Asia and the pattern of phylogeographic variation in lineage B suggest that at least one subclade of lineage B originated from eastern Asia. There was no significant geographical structuring in Chinese goat populations, which suggested that there existed strong gene flow among goat populations caused by extensive transportation of goats in history.     

Mitochondrial diversity of Opsariichthys bidens (Teleostei, Cyprinidae) in three Chinese drainages

We describe the phylogeographic structure of 28 Chinese populations of the cyprinid Opsariichthys bidens across three main Chinese river drainages. Our study is based on the phylogenetic analysis of the complete mitochondrial cytochrome b gene (1140 bp). We combined this analysis with population processes inferred from nested clade analysis (NCA) and mismatch distributions. Both analyses showed that Chinese O. bidens consists of five mtDNA lineages (Opsariichthys 1-5) with high genetic divergence among them. Molecular divergences (TrN+G) higher than 20% among the Opsariichthys 1-5 mtDNA lineages suggest a taxonomic underestimation at the species level. About 92% of the genetic variance among samples was explained by differences among Opsariichthys mtDNA lineages. Drainage-restricted haplotypes with high frequencies and moderate nucleotide diversity show that Opsariichthys populations have evolved independently. NCA results were congruent with the phylogeny, and unimodal mismatch distributions with negative Tajima's D values suggest population expansions in some Opsariichthys lineages. The phylogeographic structure of the Opsariichthys 1-5 mtDNA lineages appears to be related to their long-term interruption of gene flow (theta(ST)>0.97). Our results suggested that fragmentation of ancestral ranges might have caused Opsariichthys diversification in Chinese waters. However, current distribution of common haplotypes across the Yangtze and Pearl drainages suggests a recent river connection that could have favoured gene flow across drainages. Overall, the results indicated that the richness of current Asian widespread species might have been underestimated, and that the cyprinid populations of O. bidens in the Yangtze, Pearl and Hai He drainages may correspond to five species.     

Deep mitochondrial introgression and hybridization among ecologically divergent vole species

The completion of speciation is typically difficult to ascertain in rapidly diverging taxa but the amount of hybridization and gene flow in sympatry or parapatry contains important information about the level of reproductive isolation achieved. Here, we examined the progress in speciation between the Mediterranean (Microtus duodecimcostatus) and the Lusitanian pine vole (M. lusitanicus), which are part of the most rapid radiation of species known in mammals. These two Iberian pine voles are classified as separate species because of differences in morphology and ecology, but relatively many ambiguous individuals can be found in sympatric conditions. Our phylogenetic analyses of rangewide data from the mitochondrial cytochrome b gene (mtDNA) demonstrated high levels of diversity and a basal separation in two parapatric lineages. However, mtDNA affiliation was at odds with morphological classification or geographical distribution of the taxa. In contrast, statistical analyses of microsatellites (nucDNA) showed two clear genetic clusters in allopatry and sympatry generally matching morphological classification. This cytonuclear discordance over a large geographic area suggests historical introgression of mtDNA from M. duodecimcostatus to M. lusitanicus. There was statistical evidence for at least two recent hybrids in the sympatry zone but gene flow is apparently low given clear‐cut differences in nucDNA. Our results indicate a relatively advanced speciation process in these Iberian pine voles without fully established reproductive isolation. This situation enables use of combined population genomic and experimental approaches for the separation of patterns and mechanisms in the ongoing explosive diversification of these and other Arvicoline rodents in the future.     

Microsatellite markers confirm extensive population fragmentation of the endangered Balkan palaeoendemic Martino’s vole (<Emphasis Type="Italic">Dinaromys bogdanovi</Emphasis>)

The Martino’s vole is an endangered rodent endemic to the western Balkan Peninsula. Its range is fragmented, and populations are small due to high habitat specificity. The level of genetic variation within such populations is often low, and genetic differentiation between patchily dispersed populations is high. By scoring eight microsatellite loci in 110 individual Martino’s voles originating from 27 locations throughout the species range, we analysed genetic variation at both the intra- and interpopulation level. Factorial correspondence analysis, Bayesian analyses, and allele sharing distances divided individuals into three phylogroups (Northwestern, Central, and Southeastern), thus providing independent support for phylogeographic structuring, a pattern that has been described in previous studies based on mitochondrial DNA. Spatial genetic analyses showed that populations are highly fragmented, even in those areas with the highest population densities. The highest intrapopulation genetic variability and stable effective population sizes were found in Mount Zelengora (Bosnia and Herzegovina), which harbours a relatively large population of Martino’s voles. Populations in the Central and Southeastern lineages exhibited a significant isolation-by-distance pattern, indicating limited gene flow between them. Contrary to previous opinion, low effective population size and very limited gene flow between remaining populations suggest that the long-term existence of the Martino’s vole might not be secure, even in populations that live in optimal habitats. The only threat to the Martino’s vole identified thus far is competitive exclusion by the European snow vole. However, our results suggest that conservation problems associated with this paleoendemic rodent are more complex.     

Novel patterns of historical isolation, dispersal, and secondary contact across Baja California in the Rosy Boa (Lichanura trivirgata)

Mitochondrial DNA (mtDNA) sequence variation was examined in 131 individuals of the Rosy Boa (Lichanura trivirgata) from across the species range in southwestern North America. Bayesian inference and nested clade phylogeographic analyses (NCPA) were used to estimate relationships and infer evolutionary processes. These patterns were evaluated as they relate to previously hypothesized vicariant events and new insights are provided into the biogeographic and evolutionary processes important in Baja California and surrounding North American deserts. Three major lineages (Lineages A, B, and C) are revealed with very little overlap. Lineage A and B are predominately separated along the Colorado River and are found primarily within California and Arizona (respectively), while Lineage C consists of disjunct groups distributed along the Baja California peninsula as well as south-central Arizona, southward along the coastal regions of Sonora, Mexico. Estimated divergence time points (using a Bayesian relaxed molecular clock) and geographic congruence with postulated vicariant events suggest early extensions of the Gulf of California and subsequent development of the Colorado River during the Late Miocene-Pliocene led to the formation of these mtDNA lineages. Our results also suggest that vicariance hypotheses alone do not fully explain patterns of genetic variation. Therefore, we highlight the importance of dispersal to explain these patterns and current distribution of populations. We also compare the mtDNA lineages with those based on morphological variation and evaluate their implications for taxonomy.     

Isolation‐driven divergence: speciation in a widespread North American songbird (Aves: Certhiidae)

Lineage, or true ‘species’, trees may differ from gene trees because of stochastic processes in molecular evolution leading to gene‐tree heterogeneity. Problems with inferring species trees because of excessive incomplete lineage sorting may be exacerbated in lineages with rapid diversification or recent divergences necessitating the use of multiple loci and individuals. Many recent multilocus studies that investigate divergence times identify lineage splitting to be more recent than single‐locus studies, forcing the revision of biogeographic scenarios driving divergence. Here, we use 21 nuclear loci from regional populations to re‐evaluate hypotheses identified in an mtDNA phylogeographic study of the Brown Creeper (Certhia americana), as well as identify processes driving divergence. Nuclear phylogeographic analyses identified hierarchical genetic structure, supporting a basal split at approximately 32°N latitude, splitting northern and southern populations, with mixed patterns of genealogical concordance and discordance between data sets within the major lineages. Coalescent‐based analyses identify isolation, with little to no gene flow, as the primary driver of divergence between lineages. Recent isolation appears to have caused genetic bottlenecks in populations in the Sierra Madre Oriental and coastal mountain ranges of California, which may be targets for conservation concerns.     

Widespread secondary contact and new glacial refugia in the halophilic rotifer Brachionus plicatilis in the Iberian Peninsula

Small aquatic organisms harbour deep phylogeographic patterns and highly structured populations even at local scales. These patterns indicate restricted gene flow, despite these organisms' high dispersal abilities, and have been explained by a combination of (1) strong founder effects due to rapidly growing populations and very large population sizes, and (2) the development of diapausing egg banks and local adaptation, resulting in low effective gene flow, what is known as the Monopolization hypothesis. In this study, we build up on our understanding of the mitochondrial phylogeography of the halophilic rotifer Brachionus plicatilis in the Iberian Peninsula by both increasing the number of sampled ponds in areas where secondary contact is likely and doubling sample sizes. We analyzed partial mitochondrial sequences of 252 individuals. We found two deep mitochondrial DNA lineages differing in both their genetic diversity and the complexity of their phylogeographic structure. Our analyses suggest that several events of secondary contact between clades occurred after their expansion from glacial refugia. We found a pattern of isolation-by-distance, which we interpret as being the result of historical colonization events. We propose the existence of at least one glacial refugium in the SE of the Iberian Peninsula. Our findings challenge predictions of the Monopolization hypothesis, since coexistence (i.e., secondary contact) of divergent lineages in some ponds in the Iberian Peninsula is common. Our results indicate that phylogeographic structures in small organisms can be very complex and that gene flow between diverse lineages after population establishment can indeed occur.     

Parallel evolution and vicariance in the guppy (Poecilia reticulata) over multiple spatial and temporal scales

Well-studied model systems present ideal opportunities to understand the relative roles of contemporary selection versus historical processes in determining population differentiation and speciation. Although guppy populations in Trinidad have been a model for studies of evolutionary ecology and sexual selection for more than 50 years, this work has been conducted with little understanding of the phylogenetic history of this species. We used variation in nuclear (X-src) and mitochondrial DNA (mtDNA) sequences to examine the phylogeographic history of Poecilia reticulata Peters (the guppy) across its entire natural range, and to test whether patterns of morphological divergence are a consequence of parallel evolution. Phylogenetic, nested clade, population genetic, and demographic analyses were conducted to investigate patterns of genetic structure at several temporal scales and are discussed in relation to vicariant events, such as tectonic activity and glacial cycles, shaping northeast South American river drainages. The mtDNA phylogeny defined five major lineages, each associated with one or more river drainages, and analysis of molecular variance also detected geographic structuring among these river drainages in an evolutionarily conserved nuclear (X-src) locus. Nested clade and other demographic analyses suggest that the eastern Venezuela/ western Trinidad region is likely the center of origin of P. reticulata. Mantel tests show that the divergence of morphological characters, known to differentiate on a local scale in response to natural and sexual selection pressures, is not associated with mtDNA genetic distance; however, TreeScan analysis identified several significant associations of these characters with the haplotype tree. Parallel upstream/downstream patterns of morphological adaptation in response to selection pressures reported in P. reticulata within Trinidad rivers appears to persist across the natural range. Our results together with previous studies suggest that, although morphological variation in P. reticulata is primarily attributed to selection, phylogeographic history may also play a role.     

Specialist and generalist symbionts show counterintuitive levels of genetic diversity and discordant demographic histories along the Florida Reef Tract

Specialist and generalist life histories are expected to result in contrasting levels of genetic diversity at the population level, and symbioses are expected to lead to patterns that reflect a shared biogeographic history and co-diversification. We test these assumptions using mtDNA sequencing and a comparative phylogeographic approach for six co-occurring crustacean species that are symbiotic with sea anemones on western Atlantic coral reefs, yet vary in their host specificities: four are host specialists and two are host generalists. We first conducted species discovery analyses to delimit cryptic lineages, followed by classic population genetic diversity analyses for each delimited taxon, and then reconstructed the demographic history for each taxon using traditional summary statistics, Bayesian skyline plots, and approximate Bayesian computation to test for signatures of recent and concerted population expansion. The genetic diversity values recovered here contravene the expectations of the specialist–generalist variation hypothesis and classic population genetics theory; all specialist lineages had greater genetic diversity than generalists. Demography suggests recent population expansions in all taxa, although Bayesian skyline plots and approximate Bayesian computation suggest the timing and magnitude of these events were idiosyncratic. These results do not meet the a priori expectation of concordance among symbiotic taxa and suggest that intrinsic aspects of species biology may contribute more to phylogeographic history than extrinsic forces that shape whole communities. The recovery of two cryptic specialist lineages adds an additional layer of biodiversity to this symbiosis and contributes to an emerging pattern of cryptic speciation in the specialist taxa. Our results underscore the differences in the evolutionary processes acting on marine systems from the terrestrial processes that often drive theory. Finally, we continue to highlight the Florida Reef Tract as an important biodiversity hotspot.

     

Identifying shared genetic structure patterns among Pacific Northwest forest taxa: insights from use of visualization tools and computer simulations

Background

Identifying causal relationships in phylogeographic and landscape genetic investigations is notoriously difficult, but can be facilitated by use of multispecies comparisons.

Methodology/Principal Findings

We used data visualizations to identify common spatial patterns within single lineages of four taxa inhabiting Pacific Northwest forests (northern spotted owl: Strix occidentalis caurina; red tree vole: Arborimus longicaudus; southern torrent salamander: Rhyacotriton variegatus; and western white pine: Pinus monticola). Visualizations suggested that, despite occupying the same geographical region and habitats, species responded differently to prevailing historical processes. S. o. caurina and P. monticola demonstrated directional patterns of spatial genetic structure where genetic distances and diversity were greater in southern versus northern locales. A. longicaudus and R. variegatus displayed opposite patterns where genetic distances were greater in northern versus southern regions. Statistical analyses of directional patterns subsequently confirmed observations from visualizations. Based upon regional climatological history, we hypothesized that observed latitudinal patterns may have been produced by range expansions. Subsequent computer simulations confirmed that directional patterns can be produced by expansion events.

Conclusions/Significance

We discuss phylogeographic hypotheses regarding historical processes that may have produced observed patterns. Inferential methods used here may become increasingly powerful as detailed simulations of organisms and historical scenarios become plausible. We further suggest that inter-specific comparisons of historical patterns take place prior to drawing conclusions regarding effects of current anthropogenic change within landscapes.     

Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the Coral Triangle

The Indonesian-Australian Archipelago is the center of the world's marine biodiversity. Although many biogeographers have suggested that this region is a "center of origin," criticism of this theory has focused on the absence of processes promoting lineage diversification in the center. In this study we compare patterns of phylogeographic structure and gene flow in three codistributed, ecologically similar Indo-West Pacific stomatopod (mantis shrimp) species. All three taxa show evidence for limited gene flow across the Maluku Sea with deep genetic breaks between populations from Papua and Northern Indonesia, suggesting that limited water transport across the Maluku Sea may limit larval dispersal and gene flow across this region. All three taxa also show moderate to strong genetic structure between populations from Northern and Southern Indonesia, indicating limited gene flow across the Flores and Java Seas. Despite the similarities in phylogeographic structure, results indicate varied ages of the genetic discontinuities, ranging from the middle Pleistocene to the Pliocene. Concordance of genetic structure across multiple taxa combined with temporal discordance suggests that regional genetic structures have arisen from the action of common physical processes operating over extended time periods. The presence in all three species of both intraspecific genetic structure as well as deeply divergent lineages that likely represent cryptic species suggests that these processes may promote lineage diversification within the Indonesian-Australian Archipelago, providing a potential mechanism for the center of origin. Efforts to conserve biodiversity in the Coral Triangle should work to preserve both existing biodiversity as well as the processes creating the biodiversity.     

Phylogeography of Varicorhinus barbatulus (Cyprinidae) in Taiwan based on nucleotide variation of mtDNA and allozymes

The phylogeographical patterns and population genetic structures of Varicorhinus barbatulus in Taiwan were investigated based on genetic diversity of 34 allozyme loci and nucleotide sequences of 3' end of the cytochrome b gene, tRNA genes, D-loop control region, and the 5' end of the 12S rRNA of mtDNA. Allozyme and mtDNA analyses revealing evident geographical structuring suggest limited gene flow between populations (F(ST)=0.511 and 0.791, respectively). Low genetic variability within populations (P=5.56%; He=0.018) based on allozymes and significantly negative Tajima's D statistics based on mtDNA suggest that most populations in Taiwan may have originated from a small number of founders followed by demographic expansion. The gene genealogy of mtDNA identified six lineages corresponding to major drainages that were separated by the geological barriers due to vicariant events. A minimum spanning network based on nucleotide substitutions reflects divergence from populations of the Miao-li Plateau to northern and southern regions of the island. In contrast to a previous hypothesis that suggests an early invasion to eastern part of Taiwan prior to the lifting of central mountain range some one million years ago, the mtDNA genealogy and molecular dating reveal very recent colonization of the eastern population. Nested clade analyses revealing significant associations between genetic structure and geographical division identify past fragmentation and range expansion as major phylogeographical events that shaped the geographical distribution of this species in Taiwan.     

Comparative phylogeography of Nearctic and Palearctic fishes

Combining phylogeographic data from mitochondrial DNA (mtDNA) of Nearctic and Palearctic freshwater and anadromous fishes, we used a comparative approach to assess the influence of historical events on evolutionary patterns and processes in regional fish faunas. Specifically, we (i) determined whether regional faunas differentially affected by Pleistocene glaciations show predictable differences in phylogeographic patterns; (ii) evaluated how processes of divergence and speciation have been influenced by such differential responses; and (iii) assessed the general contribution of phylogeographic studies to conservation issues. Comparisons among case studies revealed fundamental differences in phylogeographic patterns among regional faunas. Tree topologies were typically deeper for species from nonglaciated regions compared to northern species, whereas species with partially glaciated ranges were intermediate in their characteristics. Phylogeographic patterns were strikingly similar among southern species, whereas species in glaciated areas showed reduced concordance. The extent and locations of secondary contact among mtDNA lineages varied greatly among northern species, resulting in reduced intraspecific concordance of genetic markers for some northern species. Regression analysis of phylogeographic data for 42 species revealed significant latitudinal shifts in intraspecific genetic diversity. Both relative nucleotide diversity and estimates of evolutionary effective population size showed significant breakpoints matching the median latitude for the southern limit of the Pleistocene glaciations. Similarly, analysis of clade depth of phylogenetically distinct lineages vs. area occupied showed that evolutionary dispersal rates of species from glaciated and nonglaciated regions differed by two orders of magnitude. A negative relationship was also found between sequence divergence among sister species as a function of their median distributional latitude, indicating that recent bursts of speciation events have occurred in deglaciated habitats. Phylogeographic evidence for parallel evolution of sympatric northern species pairs in postglacial times suggested that differentiation of cospecific morphotypes may be driven by ecological release. Altogether, these results demonstrate that comparative phylogeography can be used to evaluate not only phylogeographic patterns but also evolutionary processes. As well as having significant implications for conservation programs, this approach enables new avenues of research for examining the regional, historical, and ecological factors involved in shaping intraspecific genetic diversity.     

Phylogeography of the narrow‐headed vole Lasiopodomys (Stenocranius) gregalis (Cricetidae,Rodentia) inferred from mitochondrial cytochrome b sequences: an echo of Pleistocene prosperity

A species‐wide phylogeographic study of the narrow‐headed vole Lasiopodomys (Stenocranius) gregalis was performed using the mitochondrial (mt) cytochrome b gene. We examined 164 specimens from 50 localities throughout the species distribution range. Phylogeographic pattern clearly demonstrates the division into four major mtDNA lineages with further subdivision. The level of genetic differentiation between them was found to be extremely high even for the species level: about 6–11%. The most striking result of our study is extremely high mutation rate of cytb in L. gregalis. Our estimates suggested its value of 3.1 × 10^?5 that is an order of magnitude higher than previous estimates for Microtus species. The mean estimated time of basal differentiation of the narrow‐headed vole is about 0.8 Mya. This time estimate is congruent with the known paleontological record. The greatest mitochondrial diversity is found in Southern Siberia where all four lineages occur; therewith, three of them are distributed exclusively in that area. The lineage that is distributed in south‐eastern Transbaikalia is the earliest derivate and exhibits the highest genetic divergence from all the others (11%). It is quite probable that with further research, this lineage will turn out to represent a cryptic species. Spatial patterns of genetic variation in populations of the narrow‐headed vole within the largest mt lineage indicate the normal or stepping stone model of dispersal to the north and south‐west from the Altay region in Middle Pleistocene. Both paleontological data and genetic diversity estimates suggest that this species was very successful during most of the Pleistocene, and we propose that climate humidification and wide advance of tree vegetation at the Pleistocene–Holocene boundary promoted range decrease and fragmentation for this typical member of tundra‐steppe faunistic complex. However, we still observe high genetic diversity within isolated fragments of the range.