On the origin of the Norwegian lemming

The Pleistocene glacial cycles resulted in significant changes in species distributions, and it has been discussed whether this caused increased rates of population divergence and speciation. One species that is likely to have evolved during the Pleistocene is the Norwegian lemming (Lemmus lemmus). However, the origin of this species, both in terms of when and from what ancestral taxon it evolved, has been difficult to ascertain. Here, we use ancient DNA recovered from lemming remains from a series of Late Pleistocene and Holocene sites to explore the species' evolutionary history. The results revealed considerable genetic differentiation between glacial and contemporary samples. Moreover, the analyses provided strong support for a divergence time prior to the Last Glacial Maximum (LGM), therefore likely ruling out a postglacial colonization of Scandinavia. Consequently, it appears that the Norwegian lemming evolved from a small population that survived the LGM in an ice‐free Scandinavian refugium.     

Morphotypic variability of masticatory surface pattern of molars in the recent and Pleistocene Lemmus and Myopus (Rodentia,Cricetidae) of Europe and Western Siberia

In this article, we present the results of morphological study, applying multivariate statistical analysis, of seven samples of recent Lemmini species (Lemmus lemmus, L. sibiricus, Myopus schisricolor) and eight samples of the ancient Siberian lemmings from the Middle and Late Pleistocene localities, mainly in northeastern Europe. On the basis of studying variability of masticatory surface pattern of molars, 24 morphotypes have been described. The differences in morphotypes frequencies were found between the recent Myopus and Lemmus and between the two Norwegian lemming samples. There are some indications of an evolutionary trend in molar morphology of the Siberian lemmings of the Middle, Late Pleistocene, and the recent of Eastern Europe. The distinctions, at least, between the Middle Pleistocene and modern lemmings exceed a species level.     

Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus)

We describe the gastrointestinal helminth fauna of true lemmings (Lemmus spp., Arvicolinae) based on published and original material throughout the Holarctic range of these hosts. According to the existing data, the helminth fauna of true lemmings consists of three widespread and/or locally common taxa: Hymenolepis horrida (sensu lato) (Hymenolepididae), Anoplocephaloides lemmi (Anoplocephalidae) and Heligmosomoides spp. (Heligmosomidae). Despite the taxonomic boundaries and ancient phylogenetic splits in the hosts, there are no major faunistic differences for parasites within western (Siberian) L. sibiricus and L. bungei, and eastern (North American) L. trimucronatus throughout their distribution range. In contrast, the Norwegian lemming L. lemmus, which is a Fennoscandian endemic and closely related to the western populations of L. sibiricus, has only a single host-specific helminth, the cestode Paranoplocephala fellmani n. sp. (Anoplocephalidae). We describe the new species and show that it differs consistently from related species by its long and slender cirrus-sac. However, there are also a number of other significant differences, e.g., P. fellmani n. sp. and Andrya primordialis in Tamiasciurus hudsonicus (Sciuridae) evidently have a unique (sub)type of uterine development among Andrya/Paranoplocephala spp. Because P. fellmani n. sp. was also found to occur in Alaska (host L. trimucronatus), this species seems to follow the same biogeographical pattern as the other specialist helminths of Lemmus. We suggest alternative explanations for the absence of three major helminth taxa in the Norwegian lemming in Fennoscandia.     

Phylogeography of lemmings (Lemmus): no evidence for postglacial colonization of Arctic from the Beringian refugium

Beringia is considered as an important glacial refugium that served as the main source for colonization of formerly glaciated Arctic regions. To obtain high resolution views of Arctic refugial history, we examined mitochondrial cytochrome b phylogeography in the northern genus of rodents, Lemmus (true lemmings), sampled across its circumpolar distribution. Strong phylogeographical structure suggests vicariant separation over several glacial-interglacial periods and does not provide evidence supporting the importance of Beringia for extensive colonization of formerly glaciated regions. Rather than a source of postglacial colonization, Beringia represents an area of intraspecific endemism previously undetected by biogeographical analysis. Existing phylogeographical structure suggests that vicariant separation by glacial barriers was an important factor generating genetic divergence and, thus, increasing genetic diversity in lemmings on continental and circumpolar scales. However, there is little evidence for the direct effect of the last glaciation on the level of genetic variation and allele genealogy in lemmings on a regional geographical scale. This finding implies that the population genetic models of postglacial colonization suggested for temperate taxa might have limited applicability for Arctic species.     

Amphibian phylogeography in the Antipodes: Refugia and postglacial colonization explain mitochondrial haplotype distribution in the Patagonian frog Eupsophus calcaratus (Cycloramphidae)

Climatic oscillations, heterogeneity in elevation, topographical position, and isolation time in southwestern Patagonia have been important in promoting diversification of the biota. Geological studies have shown that this region had wide ice-free areas during periods of the last glacial maximum and provided forested refugia for the biota during Pleistocene glaciations. In this study, we sampled the endemic frog Eupsophus calcaratus from 20 localities, covering most of its distribution and including glaciated and non-glaciated regions. We collected DNA sequences for three mitochondrial regions (D-loop, cyt b, 16S), and describe patterns of variation consistent with a history of both the displacement to glacial refugia and recent recolonization to extensively glaciated regions. The inferred demographic history and divergence times of the lineages of E. calcaratus suggest that the Pleistocene had profound effects on the genetic patterns within this taxon in which some populations were able to survive in refugia within colder regions followed by demographic increases but without evidence of significant range expansion. The mtDNA gene tree recovers six major haploclades of E. calcaratus, which we consider diagnostic of species lineages. These results contribute to our understanding of how geological events, predominately glacial oscillations, have influenced current population structure of a broad-ranging, ectothermic vertebrate in the Valdivian Forest region of southern South America.     

Extra-Mediterranean refugia: The rule and not the exception?

ABSTRACT: Some decades ago, biogeographers distinguished three major faunal types of high importance for Europe: (i) Mediterranean elements with exclusive glacial survival in the Mediterranean refugia, (ii) Siberian elements with glacial refugia in the eastern Palearctic and only postglacial expansion to Europe and (iii) arctic and/or alpine elements with large zonal distributions in the periglacial areas and postglacial retreat to the North and/or into the high mountain systems. Genetic analyses have unravelled numerous additional refugia both of continental and Mediterranean species, thus strongly modifying the biogeographical view of Europe. This modified notion is particularly true for the so-called Siberian species, which in many cases have not immigrated into Europe during the postglacial period, but most likely have survived the last, or even several glacial phases, in extra-Mediterranean refugia in some climatically favourable but geographically limited areas of southern Central and Eastern Europe. Recently, genetic analyses revealed that typical Mediterranean species have also survived the Last Glacial Maximum in cryptic northern refugia (e.g. in the Carpathians or even north of the Alps) in addition to their Mediterranean refuge areas.     

Multiple glacial refugia in the North American Arctic: inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus)

Cryptic northern refugia beyond the ice limit of the Pleistocene glaciations may have had significant influence on the current pattern of biodiversity in Arctic regions. In order to evaluate whether northern glacial refugia existed in the Canadian Arctic, we examined mitochondrial DNA phylogeography in the northernmost species of rodents, the collared lemming (Dicrostonyx groenlandicus) sampled across its range of distribution in the North American Arctic and Greenland. The division of the collared lemming into the Canadian Arctic and eastern Beringia phylogroups does not support postglacial colonization of the North American Arctic from a single eastern Beringia refugium. Rather, the phylogeographical structure and sparse fossil records indicate that, during the last glaciation, some biologically significant refugia and important sources of postglacial colonization were located to the northwest of the main ice sheet in the Canadian Arctic.     

New findings concerning the spread of natural foci of infection in the transpolar region of eastern Siberia]

New materials are presented on the presence of the foci of anthropozoonozes in the Extreme North. For the first time there was established the existence in the subarctic tundra of the Taimyr peninsula of the arbovirus foci of the tick-borne encephalitis complex. A virus of the tick-borne encephalitis complex was isolated in 1973 from the gamasida ticks Haemogamasus ambulans Thorel. and Hirstionyssus isabellinus Oudms. and the nests of the Siberian lemming Lemmus lemmus L. This pointed to the existence in the Transpolar region of the foci or arboviruses in the nest-hole biocenoses of the lemmings outside the bird colonies. Cultures of tularemia bacilli (which proved the etiology of the epizootic among the lemmings observed in 1973 and also the presence of the lemming natural foci of tularemia and their combination with the arbovirus foci) were isolated from the lemmings at the same territory. The results of serological examination of the local population and of the animals pointed to the circulation in the Transpolar region of the causative agents of leptospirosis, toxoplasmosis, Q-fever and of the Asian tick-borne rickettsiosis.     

Predator–prey relationships: arctic foxes and lemmings

1. The number of breeding dens and litter sizes of arctic foxes Alopex lagopus were recorded and the diet of the foxes was analysed during a ship-based expedition to 17 sites along the Siberian north coast. At the same time the cyclic dynamics of co-existing lemming species were examined.
2. The diet of arctic foxes was dominated by the Siberian lemming Lemmus sibiricus (on one site the Norwegian lemming L. lemmus ), followed by the collared lemming Dicrostonyx torquatus .
3. The examined Lemmus sibiricus populations were in different phases of the lemming cycle as determined by age profiles and population densities.
4. The numerical response of arctic foxes to varying densities of Lemmus had a time lag of 1 year, producing a pattern of limit cycles in lemming–arctic fox interactions. Arctic fox litter sizes showed no time lag, but a linear relation to Lemmus densities. We found no evidence for a numerical response to population density changes in Dicrostonyx .
5. The functional or dietary response of arctic foxes followed a type II curve for Lemmus , but a type III response curve for Dicrostonyx .
6. Arctic foxes act as resident specialist for Lemmus and may increase the amplitude and period of their population cycles. For Dicrostonyx , on the other hand, arctic foxes act as generalists which suggests a capacity to dampen oscillations.     

Phylogeographic analysis reveals northerly refugia for the riverine amphibian Triturus dobrogicus (Caudata: Salamandridae)

We investigated the recent evolutionary history of the Danube crested newt, Triturus dobrogicus through reconstructions of: (1) the number and position of refugia at the last glacial maximum, (2) the role of major central European rivers in pattern of post‐glacial dispersal, and (3) the present‐day distribution pattern. We analysed sequences of mitochondrial DNA (ND2, 1065 bp) and six microsatellite loci in 363 T. dobrogicus individuals from 58 populations covering the range of the species. Our analyses suggested that T. dobrogicus survived the last glacial maximum in two separate refugia positioned in northwestern Pannonia and in Southern Pannonia from where its range expanded along the Danube and Tisza Rivers. Our findings also confirmed that rivers played an important role in shaping the evolutionary history of amphibian species in Central Europe. We compared the T. dobrogicus range with another lowland amphibian, the fire‐bellied toad Bombina bombina, using species distribution modelling. In line with these models, the isolated mountains inside Pannonia are occupied not by B. bombina, but by its mountain‐dwelling sister‐species B. variegata. However, in contrast to the model, crested newts (including T. dobrogicus) are absent from these mountains. We attribute this biogeographical discrepancy to the positioning of the species’ refugia at the last glacial maximum.     

Comparing the genetic population structure of two species of arctic lemmings: more local differentiation in Lemmus trimucronatus than in Dicrostonyx groenlandicus

Collared and brown lemmings ( Dicrostonyx groenlandicus and Lemmus trimucronatus ) are two largely sympatric and ecologically comparable species of arctic microtine rodents, differing however in some respects which allow us to hypothesise differences in the genetic structure of their populations. Collared lemmings are particularly well adapted to life at high latitude, they occasionally emerge to the surface of the snow and may disperse over larger distances than brown lemmings – possibly even over snow and ice. This should result in more local differentiation among populations of brown lemmings than among populations of collared lemmings. We compared the genetic population structure between the two lemming species in a fragmented landscape with small islands in the central Canadian Arctic using four microsatellite loci and partial mitochondrial control region sequences. Both types of genetic markers showed higher differentiation ( F _ST values) among local populations for brown lemmings than for collared lemmings. We discuss to what extent the observed genetic differences may be explained by differences in dispersal rates in addition to differences in average effective population size.     

Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data

In order to contribute to the debate about southern glacial refugia used by temperate species and more northern refugia used by boreal or cold-temperate species, we examined the phylogeography of a widespread snake species (Vipera berus) inhabiting Europe up to the Arctic Circle. The analysis of the mitochondrial DNA (mtDNA) sequence variation in 1043 bp of the cytochrome b gene and in 918 bp of the noncoding control region was performed with phylogenetic approaches. Our results suggest that both the duplicated control region and cytochrome b evolve at a similar rate in this species. Phylogenetic analysis showed that V. berus is divided into three major mitochondrial lineages, probably resulting from an Italian, a Balkan and a Northern (from France to Russia) refugial area in Eastern Europe, near the Carpathian Mountains. In addition, the Northern clade presents an important substructure, suggesting two sequential colonization events in Europe. First, the continent was colonized from the three main refugial areas mentioned above during the Lower-Mid Pleistocene. Second, recolonization of most of Europe most likely originated from several refugia located outside of the Mediterranean peninsulas (Carpathian region, east of the Carpathians, France and possibly Hungary) during the Mid-Late Pleistocene, while populations within the Italian and Balkan Peninsulas fluctuated only slightly in distribution range, with larger lowland populations during glacial times and with refugial mountain populations during interglacials, as in the present time. The phylogeographical structure revealed in our study suggests complex recolonization dynamics of the European continent by V. berus, characterized by latitudinal as well as altitudinal range shifts, driven by both climatic changes and competition with related species.     

Time to the most recent common ancestor and divergence times of populations of common chaffinches (Fringilla coelebs) in Europe and North Africa: insights into Pleistocene refugia and current levels of migration

We analyzed sequences from a 275-bp hypervariable region in the 5' end of the mitochondrial DNA control region in 190 common chaffinches (Fringilla coelebs) from 19 populations in Europe and North Africa, including new samples from Greece and Morocco. Coalescent techniques were applied to estimate the time to the most recent common ancestor (TMRCA) and divergence times of these populations. The first objective of this study was to infer the locations of refugia where chaffinches survived the last glacial episode, and this was achieved by estimating the TMRCA of populations in regions surrounding the Mediterranean that were unglaciated in the late Pleistocene. Although extant populations in Iberia, Corsica, Greece, and North Africa harbor haplotypes that are basal in a phylogenetic tree, this information alone cannot be used to infer that these localities served as refugia, because it is impossible to infer the ages of populations and their divergence times without also considering the population genetic processes of mutation, migration, and drift. Provided we assume the TMRCAs of populations are a reasonable estimate of a population's age, coalescent-based methods place resident populations in Iberia, Corsica, Greece, and North Africa during the time of the last glacial maximum, suggesting these regions served as refugia for the common chaffinch. The second objective was to determine when populations began diverging from each other and to use this as a baseline to estimate current levels of gene flow. Divergence time estimates suggest that European populations began diverging about 60,000 years before present. The relatively recent divergence of populations in North Africa, Italy, and Iberia may explain why classic migration estimates based on equilibrium assumptions are high for these populations. We compare these estimates with nonequilibrium-based estimates and show that the nonequilibrium estimates are consistently lower than the equilibrium estimates.     

Phylogeography and historical demography of the Lusitanian snail <Emphasis Type="Italic">Elona quimperiana</Emphasis> reveal survival in unexpected separate glacial refugia

Background  

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.     

Asynchronous population dynamics of Siberian lemmings across the Palaearctic tundra

The synchrony of Siberian lemming (Lemmus sibiricus L.) population dynamics was investigated during a ship-borne expedition along the Palaearctic tundra coast in the summer of 1994. On 12 sites along the coast from the Kola Peninsula to Wrangel Island, relative densities of lemmings were recorded using a standardised snap-trapping programme. The phase position of the lemming cycle in each of the studied populations was determined based on current density estimates, signs of previous density and the age profile of each population (ageing based on eye lens mass). In addition, dendrochronological methods were used to determine when the last peak in the density of microtine populations occurred at each site. The examined lemming populations were in different phases of the lemming cycle. Some populations were in the peak phase, as indicated by high current densities, an age profile in which older individuals were well represented, and signs of high previous density (abundant old lemming faeces). Other populations were in the decline phase, as reflected in a moderate current density, a predominance of older individuals and signs of high previous density. Populations in the low phase had an extremely low current density and showed signs of high previous density, while populations in the increase phase had a moderate current density, a predominance of younger individuals and showed signs of low previous density. The results of phase determinations based on dendrochronological methods support the findings based on lemming demography. Recent Russian studies carried out on some of the sites also agreed with our phase determination results. Thus, on a regional scale (across the whole Palaearctic tundra), the population dynamics of Siberian lemmings can be considered asynchronous. However, sites situated adjacent to each other were often phase synchronous, suggesting a more fine-grained pattern of dynamics with synchrony over distances as long as 1000 km or so, e.g. the Yamal and Taymyr Peninsulas. Received: 19 August 1998 / Accepted: 1 March 1999     

Glacial refugia and the phylogeography of Steller's sea lion (Eumatopias jubatus) in the North Pacific

Mitochondrial DNA sequence data were used to examine the phylogeographic history of Steller's sea lions (Eumetopias jubatus) in relation to the presence of Plio-Pleistocene insular refugia. Cytochrome b and control region sequences from 336 Steller's sea lions reveal phylogenetic lineages associated with continental refugia south of the ice sheets in North America and Eurasia. Phylogenetic analysis suggests the genetic structure of E. jubatus is the result of Pleistocene glacial geology, which caused the elimination and subsequent reappearance of suitable rookery habitat during glacial and interglacial periods. The cyclic nature of geological change produced a series of independent population expansions, contractions and isolations that had analogous results on Steller's sea lions and other marine and terrestrial species. Our data show evidence of four glacial refugia in which populations of Steller's sea lions diverged. These events occurred from approximately 60,000 to 180,000 years BP and thus preceded the last glacial maximum.     

Phylogeographic structure and mitochondrial DNA variation in true lemmings (Lemmus) from the Eurasian Arctic

The geographic pattern of mtDNA variation in lemmings from 13 localities throughout the Eurasian Arctic was studied by using eight restriction enzymes and sequencing of the cytochrome b region. These data are used to reveal the vicariant history of Lemmus , and to examine the effect of the last glaciation on mtDNA variation by comparing diversity in formerly glaciated areas to the diversity in non-glaciated areas. Phylogenetic congruence across different Arctic taxa and association between observed discontinuities, and probable Pleistocene barriers, suggest that glacial-interglacial periods were crucial in the vicariant history of Lemmus. Differences in amount of divergence (2.1–9.1%) across different historical barriers indicate chronologically separate vicariant events during the Quaternary. Populations from a formerly glaciated area are no less variable than those in the non-glaciated area. Regardless of glaciation history, no population structure and high haplotype diversity were found within geographic regions. The lack of population structure indicates that populations with high ancestral haplotype diversity shifted their distribution during the Holocene, and that lemmings tracked a changing environment during the Quaternary without reduction of effective population size.     

The topography of Gomori positive neurosecretory elements of the hypothalamus of the lemmings Dicrostonyx torquatus and Lemmus sibiricus]

Under study was the structure of the hypothalamo-hypophyseal neurosecretory system in two species of lemmings of the Wrangel island: the collared lemming, (Dicrostonyx torquatus) and the Ob lemming (Lemmus sibiricus). Inspite of the similarity in the general organization of this system in all rodents, certain species features were found in the topography of neurosecretory elements in the animals studied. In the Ob lemming there is a great similarity in the structures of the neurosecretory system with the albino rat than in the collared lemming. In both species of lemmings, and in the collared lemming in particular, the supraoptic nucleus is located more dorso-caudally and the paraventricular one-more dorsally. A greater amount of neurosecretory cells is found which from additional groups. The hypothalamo-hypophyseal and extrahypothalamic pathways are well pronounced. The postoptical nucleus is considerably developed. In the collared lemming it is almost equal to the supraoptic one in the amount of cells composing it. The ratio of the cells in the supraoptic and postoptic nuclei is suggested to be related to the level of the water-salt metabolism and the specific ecology of lemmings.     

Across the southern Andes on fin: glacial refugia,drainage reversals and a secondary contact zone revealed by the phylogeographical signal of Galaxias platei in Patagonia

We employed DNA sequence variation at two mitochondrial (control region, COI) regions from 212 individuals of Galaxias platei (Pisces, Galaxiidae) collected throughout Patagonia (25 lakes/rivers) to examine how Andean orogeny and the climatic cycles throughout the Quaternary affected the genetic diversity and phylogeography of this species. Phylogenetic analyses revealed four deep genealogical lineages which likely represent the initial division of G. platei into eastern and western lineages by Andean uplift, followed by further subdivision of each lineage into separate glacial refugia by repeated Pleistocene glacial cycles. West of the Andes, refugia were likely restricted to the northern region of Patagonia with small relicts in the south, whereas eastern refugia appear to have been much larger and widespread, consisting of separate northern and southern regions that collectively spanned most of Argentinean Patagonia. The retreat of glacial ice following the last glacial maximum allowed re‐colonization of central Chile from nonlocal refugia from the north and east, representing a region of secondary contact between all four glacial lineages. Northwestern glacial relicts likely followed pro‐glacial lakes into central Chilean Patagonia, whereas catastrophic changes in drainage direction (Atlantic → Pacific) for several eastern palaeolakes were the likely avenues for invasions from the east. These mechanisms, combined with evidence for recent, rapid and widespread population growth could explain the extensive contemporary distribution of G. platei throughout Patagonia.     

Genetic structure of sable (Martes zibellina L.) in Eurasia—analysis of the mitochondrial lineages distribution

The phylogeography of the sable, which is a commercially valuable species, is extremely complicated and poorly investigated. Specifically, the effects of factors such as the range dynamics of the sable during the Pleistocene Epoch, the localization of glacial refugia, species distribution pattern in Holocene, and recent dramatic population decline, along with massive reacclimatization measures, on the species phylogeography remain unclear. Based on the sequence analysis of the control region of mitochondrial DNA from sables that inhabit different parts of the species range, a suggestion was made of the considerably high Pleistocene genetic diversity in sable, which was subsequently lost. The initial diversity of mitochondrial lineages is mostly preserved in the Urals, while in the eastern part of the range, it seems to have been depleted as early as before the last glacial maximum. On the other hand, the even greater depletion of the mitochondrial lineages observed in some populations of central Siberia can be associated with the dramatic population decline at the turn of the 20th century.