Hares on ice: phylogeography and historical demographics of Lepus arcticus, L. othus, and L. timidus (Mammalia: Lagomorpha)

Phylogeographical investigations of arctic organisms provide spatial and temporal frameworks for interpreting the role of climate change on biotic diversity in high-latitude ecosystems. Phylogenetic analyses were conducted on 473 base pairs of the mitochondrial control region in 192 arctic hares (Lepus arcticus, Lepus othus, Lepus timidus) and two individual Lepus townsendii. The three arctic hare species are closely related. All L. othus individuals form one well-supported clade, L. arcticus individuals form two well-supported clades, and L. timidus individuals are scattered throughout the phylogeny. Arctic hare distribution was altered dramatically following post-Pleistocene recession of continental ice sheets. We tested for genetic signatures of population expansion for hare populations now found in deglaciated areas. Historical demographic estimates for 12 arctic hare populations from throughout their range indicate that L. arcticus and L. othus persisted in two separate North American arctic refugia (Beringia and High Canadian Arctic) during glacial advances of the Pleistocene, while the high genetic diversity in L. timidus likely reflects multiple Eurasian refugia.     

Repeatedly out of Beringia: Cassiope tetragona embraces the Arctic

Aim Eric Hultén hypothesized that most arctic plants initially radiated from Beringia in the Late Tertiary and persisted in this unglaciated area during the Pleistocene glaciations, while their distribution ranges were repeatedly fragmented and reformed elsewhere. Whereas taxonomic and fossil evidence suggest that Cassiope tetragona originated in Beringia and expanded into the circumarctic area before the onset of the glaciations, lack of chloroplast DNA (cpDNA) variation may suggest that colonization was more recent. We address these contradictory scenarios using high‐resolution nuclear markers. Location Circumpolar Arctic. Methods The main analysis was by amplified fragment‐length polymorphism (AFLP), while sequences of chloroplast DNA verified the use of Cassiope mertensiana as an outgroup for C. tetragona. Data were analysed using Bayesian clustering, principal coordinates analyses, parsimony and neighbour‐joining, and measures of diversity and differentiation were calculated. Results The circumpolar C. tetragona ssp. tetragona was well separated from the North American C. tetragona ssp. saximontana. The genetic structure in ssp. tetragona showed a strong east–west trend, with the Beringian populations in an intermediate position. The highest level of diversity was in Beringia, while the strongest differentiation in the data set was found between the populations from the Siberian Arctic west of Beringia and the remainder. Main conclusions The results are consistent with a Beringian origin of the species, but the levels and geographical patterns of differentiation and gene diversity suggest that the latest expansion from Beringia into the circumarctic was recent, possibly during the current interglacial. The results are in accordance with a recent leading‐edge mode of colonization, particularly towards the east throughout Canada/Greenland and across the North Atlantic into Scandinavia and Svalbard. As fossils demonstrate the presence of the species in North Greenland 2.5–2.0 Ma, as well as in the previous interglacial, we conclude that C. tetragona expanded eastwards from Beringia several times and that the earlier emigrants of this woody species became extinct. The last major westward expansion from Beringia seems older, and the data suggest a separate Siberian refugium during at least one glaciation.     

Population structure and the co-evolution between social parasites and their hosts

Co-evolutionary trajectories of host-parasite interactions are strongly affected by the antagonists' evolutionary potential, which in turn depends on population sizes as well as levels of recombination, mutation, and gene flow. Under similar selection pressures, the opponent with the higher evolutionary rate is expected to lead the co-evolutionary arms race and to develop local adaptations. Here, we use mitochondrial DNA sequence data and microsatellite markers to assess the amount of genetic variability and levels of gene flow in two host-parasite systems, each consisting of an ant social parasite--the European slavemaker Harpagoxenus sublaevis and the North American slavemaker Protomognathus americanus--and its two main host species. Our population genetic analyses revealed limited gene flow between individual populations of both host and parasite species, allowing for a geographic mosaic of co-evolution. In a between-system comparison, we found less genetic variability and more pronounced structure in Europe, where previous behavioural studies demonstrated strong local adaptation. Within the European host-parasite system, the larger host species Leptothorax acervorum exhibited higher levels of both genetic variability and gene flow, and previous field data showed that it is less affected by the social parasite H. sublaevis than the smaller host Leptothorax muscorum, which has genetically depleted and isolated populations. In North America, the parasite P. americanus showed higher levels of gene flow between sites, but overall less genetic diversity than its hyper-variable main host species, Temnothorax longispinosus. Interestingly, recent ecological and chemical studies demonstrated adaptation of P. americanus to local host populations, indicating the importance of migration in co-evolutionary interactions.     

Mitochondrial phylogeography of a Beringian relict: the endemic freshwater genus of blackfish Dallia (Esociformes)

Mitochondrial genetic variability among populations of the blackfish genus Dallia (Esociformes) across Beringia was examined. Levels of divergence and patterns of geographic distribution of mitochondrial DNA lineages were characterized using phylogenetic inference, median‐joining haplotype networks, Bayesian skyline plots, mismatch analysis and spatial analysis of molecular variance (SAMOVA) to infer genealogical relationships and to assess patterns of phylogeography among extant mitochondrial lineages in populations of species of Dallia. The observed variation includes extensive standing mitochondrial genetic diversity and patterns of distinct spatial segregation corresponding to historical and contemporary barriers with minimal or no mixing of mitochondrial haplotypes between geographic areas. Mitochondrial diversity is highest in the common delta formed by the Yukon and Kuskokwim Rivers where they meet the Bering Sea. Other regions sampled in this study host comparatively low levels of mitochondrial diversity. The observed levels of mitochondrial diversity and the spatial distribution of that diversity are consistent with persistence of mitochondrial lineages in multiple refugia through the last glacial maximum.     

Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America

Glacial cycles have played a dominant role in shaping the genetic structure and distribution of biota in northwestern North America. The two major ice age refugia of Beringia and the Pacific Northwest were connected by major mountain chains and bordered by the Pacific Ocean. As a result, numerous refugial options were available for the regions taxa during glacial advances. We reviewed the importance of glaciations and refugia in shaping northwestern North America’s phylogeographic history. We also tested whether ecological variables were associated with refugial history. The recurrent phylogeographic patterns that emerged were the following: (i) additional complexity, i.e. refugia within refugia, in both Beringia and the Pacific Northwest; and (ii) strong evidence for cryptic refugia in the Alexander Archipelago and Haida Gwaii, the Canadian Arctic and within the ice‐sheets. Species with contemporary ranges that covered multiple refugia, or those with high dispersal ability, were significantly more likely to have resided in multiple refugia. Most of the shared phylogeographic patterns can be attributed to multiple refugial locales during the last glacial maximum or major physiographic barriers like rivers and glaciers. However, some of the observed patterns are much older and appear connected to the orogeny of the Cascade‐Sierra chain or allopatric differentiation during historic glacial advances. The emergent patterns from this review suggest we should refine the classic Beringian‐southern refugial paradigm for northwestern North American biota and highlight the ecological and evolutionary consequences of colonization from multiple refugia.     

Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas

Traditional concepts of the Bering Land Bridge as a zone of predominantly eastward expansion from Eurasia and a staging area for subsequent colonization of lower latitudes in North America led to early inferences regarding biogeographic histories of North American faunas, many of which remain untested. Here we apply a host-parasite comparative phylogeographical (HPCP) approach to evaluate one such history, by testing competing biogeographic hypotheses for five lineages of host-specific parasites shared by the collared pika (Ochotona collaris) and American pika (Ochotona princeps) of North America. We determine whether the southern host species (O. princeps) was descended from a northern ancestor or vice versa. Three parasite phylogenies revealed patterns consistent with the hypothesis of a southern origin, which is corroborated by four additional parasite lineages restricted to O. princeps. This finding reverses the traditional narrative for the origins of North American pikas and highlights the role of dispersal from temperate North America into Beringia in structuring northern diversity considerably prior to the Holocene. By evaluating multiple parasite lineages simultaneously, the study demonstrates the power of HPCP for resolving complex biogeographic histories that are not revealed by characteristics of the host alone.     

One Beringian genus less: A re‐assesment of Pacifimyxas Kruglov & Starobogatov, 1985 (Mollusca: Gastropoda: Lymnaeidae) questions the current estimates of Beringian biodiversity

The taxonomic position of three nominal species of lymnaeid snails placed by Kruglov & Starobogatov (1993) into the subgenus Lymnaea (Pacifimyxas) Kruglov & Starobogatov, 1985, has been re‐assessed based on a molecular genetic study of topotypic specimens and an examination of the type series and other materials available. It has been shown that the two species, Lymnaea (Pacifimyxas) magadanensis Kruglov & Starobogatov, 1985 and Lymnaea (Pacifimyxas) streletzkajae Kruglov & Starobogatov, 1985, are identical with the species Kamtschaticana kamtschatica (Middendorff, 1850) and must be treated as its junior synonyms. Hence, Pacifimyxas becomes a junior synonym of Kamtschaticana Kruglov & Starobogatov, 1984. The taxonomic identity of the third species of Pacifimyxas, Lymnaea (Pacifimyxas) perpolita, remains obscure, and this species is considered here as taxon inquirendum. Two other nominal species, Lymnaea aberrans (Westerlund, 1897) and Lymnaea middendorffi (W. Dybowski, 1904), have been synonymized with K. kamtschatica based on morphological and geographical evidence. The lectotype of Limnaea peregra var. middendorffi is designated. The actual level of species richness in the Beringian freshwater malacofauna may be 20–25% lower than it was determined on the basis of the traditional system. Some implications of this outcome for the biogeography of the Beringian freshwater fauna are discussed.     

The role of disjunction and postglacial population expansion on phylogeographical history and genetic diversity of the circumboreal plant Chamaedaphne calyculata

In the last decade a number of studies has illustrated quite different phylogeographical patterns amongst plants with a northern present‐day geographical distribution, spanning the entire circumboreal region and/or circumarctic region and southern mountains. These works, employing several marker systems, have brought to light the complex evolutionary histories of this group. Here I focus on one circumboreal plant species, Chamaedaphne calyculata (leatherleaf), to unravel its phylogeographical history and patterns of genetic diversity across its geographical range. A survey of 29 populations with combined analyses of chloroplast DNA (cpDNA), internal transcribed spacer (ITS) and AFLP markers revealed structuring into two groups: Eurasian/north‐western North American, and north‐eastern North American. The present geographical distribution of C. calyculata has resulted from colonization from two putative refugial areas: east Beringia and south‐eastern North America. The variation of chloroplast DNA (cpDNA) and ITS sequences strongly indicated that the evolutionary histories of the Eurasian/north‐western North American and the north‐eastern North American populations were independent of each other because of a geographical disjunction in the distribution area and ice‐sheet history between north‐eastern and north‐western North America. Mismatch analysis using ITS confirmed that the present‐day population structure is the result of rapid expansion, probably since the last glacial maximum. The AFLP data revealed low genetic diversity of C. calyculata (P = 19.5%, H = 0.085) over the whole geographical range, and there was no evidence of loss of genetic diversity within populations in the continuous range, either at the margins or in formerly glaciated and nonglaciated regions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 761–775.     

Around or across the Carpathians: colonization model of the Danube basin inferred from genetic diversification of stone loach (Barbatula barbatula) populations

Despite increasing information about postglacial recolonization of European freshwater systems, very little is known about pre-Pleistocene history. We used data on the recent distribution and phylogenetic relationships of stone loach mitochondrial lineages to reconstruct the initial colonization pattern of the Danube river system, one of the most important refuges for European freshwater ichthyofauna. Fine-scale phylogeography of the Danubian populations revealed five highly divergent lineages of pre-Pleistocene age and suggested the multiple origin of the Danubian stone loach. The mean sequence divergence among lineages extended from 7.0% to 13.4%, which is the highest intraspecific divergence observed so far within this river system. Based on the phylogeographical patterns, we propose the following hypothesis to relate the evolution and dispersal of the studied species with the evolution of the Danube river system and the Carpathian Mountains: (i) during the warmer period in the Miocene, the areas surrounding the uplifting Alps and Carpathians served as mountainous refuges for cold-water adapted fish and promoted the diversification of its populations, and (ii) from these refuges, colonization of the emerging Danube river system may have taken place following the retreat of the Central Paratethys. Co-existence of highly divergent mtDNA lineages in a single river system shows that range shifts in response to climatic changes during the Quaternary did not cause extensive genetic homogenization in the stone loach populations. However, the wide distribution of some mtDNA lineages indicates that the Pleistocene glaciations promoted the dispersal and mixing of populations through the lowlands.     

Persistence and diversification of the Holarctic shrew,Sorex tundrensis (Family Soricidae), in response to climate change

Environmental processes govern demography, species movements, community turnover and diversification and yet in many respects these dynamics are still poorly understood at high latitudes. We investigate the combined effects of climate change and geography through time for a widespread Holarctic shrew, Sorex tundrensis. We include a comprehensive suite of closely related outgroup taxa and three independent loci to explore phylogeographic structure and historical demography. We then explore the implications of these findings for other members of boreal communities. The tundra shrew and its sister species, the Tien Shan shrew (Sorex asper), exhibit strong geographic population structure across Siberia and into Beringia illustrating local centres of endemism that correspond to Late Pleistocene refugia. Ecological niche predictions for both current and historical distributions indicate a model of persistence through time despite dramatic climate change. Species tree estimation under a coalescent process suggests that isolation between populations has been maintained across timeframes deeper than the periodicity of Pleistocene glacial cycling. That some species such as the tundra shrew have a history of persistence largely independent of changing climate, whereas other boreal species shifted their ranges in response to climate change, highlights the dynamic processes of community assembly at high latitudes.     

A phylogeographic, demographic and historical analysis of the short-tailed pit viper (Gloydius brevicaudus): evidence for early divergence and late expansion during the Pleistocene

The impact of quaternary glaciation in eastern China on local fanua and flora has been a topic of considerable interest. We used mitochondrial DNA (mtDNA) sequence data and coalescent simulations to test two general biogeographic hypothesis related to the effects of Pleistocene climatic fluctuations for a widespread ophidian species (Gloydius brevicaudus) in eastern China and Korean Peninsula. The phylogenetic analysis revealed three major lineages, the southeast Coastal, Yangtze and North Lineages. The latter two are closely related and jointly form a continental lineage. Divergence dating and coalescent simulations indicate a Late Pliocene to Early Pleistocene divergence between lineages from the southeast coast and continental interior, followed by a mid-to-late Pleistocene divergence between lineages from the north and the middle-lower Yangtze Valley across East China, suggesting that all these lineages predated the last glacial maximum. An overlapping range between the two lineages within the continental lineage and a secondary contact associated with ecological transition zones on the margins of the North China Plain were also observed. These results show that vicariance patterns dominated the history of G. brevicaudus. Though the climatic events of the Pleistocene have had a marked effect on the historical distribution and intra-specific divergence of reptiles in China, coalescent and non-coalescent demographic analyses indicate that all lineages of G. brevicaudus seem not to have been adversely affected by glacial cycles during the Late Pleistocene, presumably because of an increase in the amount of climatically mild habitat in East Asia due to a decline in elevation and the development of monsoons since the Mid-End Pleistocene.     

On glacial refugia,genetic diversity,and microevolutionary processes: deep phylogeographical structure in the endemic newt Lissotriton italicus1

We investigated the phylogeographical patterns of Lissotriton italcus, a newt endemic to the Italian peninsula, aiming to determine why hotspots of intraspecific diversity so ‘hot’. We found two main mitochindrial DNA lineages (net sequence divergence of 6.8% at two fragments of total length of 1897 bp): one restricted to part of the Calabrian peninsula (i.e the southernmost portion of the species range) and the other widespread throughout the rest of the species range. Both lineages, which had a parapatric distribution, showed evidence of further subdivisions, with an overall number of eight terminal haplogroups, most of whose times to the most recent common ancestors were estimated at the Late Pleistocene. Analysis of molecular variance suggested that partitioning populations according to the geographical distribution of these haplogroups can explain 97% of the observed genetic variation. These results suggest that L. italicus underwent repeated cycles of allopatric fragmentation throughout the Pleistocene, and that it likely survived the Late Pleistocene paleoenvironmental changes within eight separate refugia. Thus, the current hotspot of intraspecific diversity of L. italicus (within the Calabrian peninsula) has not been moulded by long‐term stability of large populations but rather by multiple events of allopatric fragmentation and divergence. When compared with the patterns recently identified in other species, these results suggest that the occurrence of phases of allopatric divergence (eventually followed by secondary admixture) could be a common, albeit probably underrated feature in the history of formation of hotspots of intraspecific diversity. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 42–55.     

Colonization of Pacific islands by parasites of low dispersal ability: phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean

Aim To investigate the phylogeographical patterns of two poorly dispersing but widely distributed monogenean species, Haliotrema aurigae and Euryhaliotrematoides grandis, gill parasites of coral reef fishes from the family Chaetodontidae. Location South Pacific Ocean (SPO). Methods Sequence data from the mitochondrial cytochrome oxidase subunit I (COI) gene were obtained from samples from five localities of the SPO (Heron Island, Lizard Island, Moorea, Palau and Wallis) for the two parasite species. Phylogenetic and genetic diversity analyses were used to reconstruct phylogeographical patterns, and dates of cladogenetic events were estimated. Results Overall, 50 individuals of 17 Haliotrema aurigae and 33 of Euryhaliotrematoides grandis were sequenced from five localities of the SPO for COI mtDNA (798 bp). Our results revealed a deep phylogeographical structure in the species Euryhaliotrematoides grandis. The molecular divergence between individuals from Moorea and individuals from the remaining localities (7.7%) may be related to Pleistocene sea‐level fluctuations. In contrast, Haliotrema aurigae shows no phylogeographical patterns with the presence of most of the mitochondrial haplotypes in every locality sampled. Main conclusions Our study shows contrasting phylogeographical patterns of the two monogenean parasite species studied, despite many shared characteristics. Both parasites are found on the same host family, share the same geographical range and ecology, and are phylogenetically close. We propose two hypotheses that may help explain the diparity: the hypotheses involve differences in the evolutionary age of the parasite species and their dispersal capabilities. Additionally, the lack of phylogeographical structure in Haliotrema aurigae contrasts with its apparently restricted dispersion, which is likely to occur during the egg stage of the life cycle, inducing a passive dispersal mechanism in butterflyfish monogeneans.     

Quality matters: resource quality for hosts and the timing of epidemics

Epidemiologists increasingly realize that species interactions (e.g. selective predation) can determine when epidemics start and end. We hypothesize here that resource quality can also strongly influence disease dynamics: epidemics can be inhibited when resource quality for hosts is too poor and too good. In three lakes, resource quality for the zooplankton host ( Daphnia dentifera ) was poor when fungal epidemics ( Metschnikowia bicuspidata ) commenced and increased as epidemics waned. Experiments using variation in algal food showed that resource quality had conflicting effects on underlying epidemiology: high-quality food induced large production of infective propagules (spores) and high birth rate but also reduced transmission. A model then illustrated how these underlying correlations can inhibit the start of epidemics (when spore production/birth rate are too low) but also catalyse their end (when transmission becomes too low). This resource quality mechanism is likely to interface with other ones controlling disease dynamics and warrants closer evaluation.     

Pleistocene glaciations and contemporary genetic diversity in a Beringian fish,the broad whitefish,Coregonus nasus (Pallas): inferences from microsatellite DNA variation

The contemporary distribution of genetic variation within and among high latitude populations cannot be fully understood without taking into consideration how species responded to the impacts of Pleistocene glaciations. Broad whitefish, Coregonus nasus, a species endemic to northwest North America and the Arctic coast of Russia, was undoubtedly impacted by such events because its geographic distribution suggests that it survived solely within the Beringian refuge from where it dispersed post‐glacially to achieve its current range. We used microsatellite DNA to investigate the role of glaciations in promoting intraspecific genetic variation in broad whitefish (N = 14 localities, 664 fish) throughout their North American range and in one Russian sample. Broad whitefish exhibited relatively high intrapopulation variation (average of 11.7 alleles per locus, average H_E = 0.61) and moderate levels of interpopulation divergence (overall F_ST = 0.10). The main regions assayed in our study (Russia, Alaska, Mackenzie River and Travaillant Lake systems) were genetically differentiated from each other and there were declines in genetic diversity with distance from putative refugia. Additionally, Mackenzie River system populations showed less developed and more variable patterns of isolation‐by‐distance than populations occupying former Alaskan portions of Beringia. Finally, our data suggest that broad whitefish dispersed from Beringia using coastal environments and opportunistically via headwater stream connections that once existed between Yukon and Mackenzie River drainages. Our results illustrate the importance of history (e.g. glaciation) and contemporary dispersal ecology in shaping the current genetic population structure of Arctic faunas.