Glacial survival does not matter: RAPD phylogeography of Nordic Saxifraga oppositifolia

The arctic-alpine Saxifraga oppositifolia has recently been suggested to have survived the last glaciation in high-arctic refugia, based on a finding of more genetic (RFLP) variation in Svalbard compared with more southern areas. To elucidate the migration history of this allogamous species, we analysed 18 populations from Norway, Svalbard and Novaya Zemlya using random amplified polymorphic DNAs (RAPDs). There was no more RAPD variation in the high Arctic than further south. In an analysis of molecular variance (AMOV A), most of the RAPD variation was found within populations (64%). There was less intrapopulational variation in Svalbard (65%) than in northern Norway (78%) and southern Norway (86%), suggesting that there is more inbreeding towards the north, probably because of lower pollinator activity. Twenty-eight per cent of the RAPD variation was found among populations within these geographical regions, and only 9% was found among the regions. In PCO and UPGMA analyses, plants and populations of different geographical origins were to a large extent intermingled. There was, however, a distinct, south-north clinal geographical structuring of the RAPD variation both in the PCO analysis and in a spatial autocorrelation (Mantel) analysis. These results suggest that there has been extensive gene flow among more or less continuously distributed populations of S. oppositifolia during the Weichselian, and that the extant Nordic populations were established after massive, centripetal immigration from these genetically variable, periglacial populations. The postglacial period may not have been sufficiently long for the subsequently isolated populations of this long-lived, allogamous perennial to diverge. Given the high levels of migration inferred from this study, genetic differentiation of glacial survivor populations, if any existed, would most likely have been swamped in the postglacial period. Thus, our molecular data support recent conclusions based on palaeobotanical and biogeographical data that the glacial survival hypothesis is superfluous.     

Molecular analysis of the Pleistocene history of Saxifraga oppositifolia in the Alps

A recent circumpolar survey of chloroplast DNA (cpDNA) haplotypes identified Pleistocene glacial refugia for the Arctic-Alpine Saxifraga oppositifolia in the Arctic and, potentially, at more southern latitudes. However, evidence for glacial refugia within the ice sheet covering northern Europe during the last glacial period was not detected either with cpDNA or in another study of S. oppositifolia that surveyed random amplified polymorphic DNA (RAPD) variation. If any genotypes survived in such refugia, they must have been swamped by massive postglacial immigration of periglacial genotypes. The present study tested whether it is possible to reconstruct the Pleistocene history of S. oppositifolia in the European Alps using molecular methods. Restriction fragment length polymorphism (RFLP) analysis of cpDNA of S. oppositifolia, partly sampled from potential nunatak areas, detected two common European haplotypes throughout the Alps, while three populations harboured two additional, rare haplotypes. RAPD analysis confirmed the results of former studies on S. oppositifolia; high within, but low among population genetic variation and no particular geographical patterning. Some Alpine populations were not perfectly nested in this common gene pool and contained private RAPD markers, high molecular variance or rare cpDNA haplotypes, indicating that the species could possibly have survived on ice-free mountain tops (nunataks) in some parts of the Alps during the last glaciation. However, the overall lack of a geographical genetic pattern suggests that there was massive immigration of cpDNA and RAPD genotypes by seed and pollen flow during postglacial times. Thus, the glacial history of S. oppositifolia in the Alps appears to resemble closely that suggested previously for the species in northern Europe.     

No genetic variation detected within isolated relict populations of Saxifraga cernua in the Alps using RAPD markers

Genetic variation in seven relict populations of Saxifraga cernua from three regions of the Alps was investigated using RAPD (random amplified polymorphic DNA) markers. No variation, either within the populations or within the regions, could be demonstrated. Nevertheless, each alpine region was characterized by a unique RAPD phenotype. Absence of genetic variation in these relict populations is attributed to population bottlenecks and founder effects during or following the ice ages. Contrasting hypotheses about the history of these populations, either as survivors of the glacial period or as products of postglacial immigration, are discussed in the light of the data presented.     

Sex after all: high levels of diversity detected in the arctic clonal plant Saxifraga cernua using RAPD markers

Arctic plants in general and arctic clonal plants in particular have often been assumed to contain low levels of genetic diversity. We used RAPDs (random amplified polymorphic DNAs) to investigate genetic diversity in the arctic-alpine Saxifraga cernua , which mainly reproduces clonally via bulbils, at three spatial scales in Svalbard: (i) 'macroscale', between two sites 11 km apart; (ii) 'mesoscale', along two crossing transects at each site; and (iii) 'microscale', within a 3 × 3 m square at each site. Thirteen putative clones (RAPD phenotypes) were distinguished among 93 ramets based on 38 RAPD markers. The genetic diversity ( D ; mean 0.52, range 0.10–0.81) and evenness ( E ; mean 0.42, range 0.00–0.82) were at the same level as in clonal plants in general. However, the diversity strongly depended on site and spatial scale. Several clones were highly divergent and clustered independently of site in UPGMA and PCO analyses. In an analysis of molecular variance ( AMOVA ), most of the variation (59%) was found within sites. Mantel tests revealed no correlation between spatial and genetic distance within sites. Our results suggest that occasional sexual reproduction as well as clonal migration via bulbil dispersal play a significant role in the treeless arctic environment, where S. cernua is widespread and locally very abundant. In contrast, Bauert et al. ( Molecular Ecology 7, 1519–1527) found no genetic variation within populations or regions of the Alps, where the species has highly isolated occurrences.     

Understanding population history for conservation purposes: population genetics of Saxifraga aizoides (Saxifragaceae) in the lowlands and lower mountains north of the Alps

Several alpine species have outlying populations in the lowlands and lower mountains north of the Alps. These small, isolated populations are usually described as either (1) glacial relics, (2) descendants from populations living on forelands and moraines during the ice ages, or (3) populations founded by long-distance dispersal after glaciation. A floristic survey of the historic and present distributions and an allozyme investigation were performed on one of these relic species, Saxifraga aizoides. The species was historically more abundant and had more stations in more regions of northeastern Switzerland. The former population structures within regions, nowadays destroyed, were still reflected in distinct and high regional genetic diversity and variation. There was weak evidence of increased inbreeding in outlying populations, but populations did not deviate from Hardy-Weinberg equilibrium. No geographic pattern of genetic variation above the regional scale (>10 km) was found. Based on the spatial and genetic structures found, it was not possible to discriminate between the abovementioned hypotheses. Nevertheless, the study shows how a thorough evaluation of distribution and abundance data aids the interpretation of genetic data with respect to population history, biogeography, and conservation biology.     

Comparative phylogeography of codistributed aquatic insects in western North America: insights into dispersal and regional patterns of genetic structure

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Glacial refuges for three‐spined stickleback in the Iberian Peninsula: mitochondrial DNA phylogeography

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When the company does not matter: High‐quality ant seed‐disperser does not drive the spatial distribution of large‐seeded myrmecochorous plants

Mutualisms are one of the main forces shaping species spatial patterns at all geographic scales. In generalised mutualisms, however, the dependence among partners is highly variable in time and space, and therefore, the effect of diffuse mutualisms on species geographic distributions is unclear. Myrmecochorous seeds in Brazilian semi‐arid vegetation are dispersed by several ant species. However, large‐seeded species are especially dependent on dispersal by the giant ant Dinoponera quadriceps, which is the main disperser of such diaspores and the species that provide the longest dispersal distance among ant species in this system. Hence, we hypothesise that the presence of D. quadriceps shapes the distribution of large‐seeded, but not the distribution of small‐seeded myrmecochorous plant species. To evaluate this hypothesis, we modelled the potential distribution of two large‐seeded (which are predominantly dispersed by D. quadriceps) and two small‐seeded (which are barely dispersed by D. quadriceps) Euphorbiaceae species and the potential distribution of D. quadriceps. We analysed the relationship between the occurrence suitability of D. quadriceps and the occurrence suitability of plant species. We found that the potential distribution of both large‐seeded and small‐seeded myrmecochorous plants was unrelated to D. quadriceps occurrence suitability. It means that the disproportional benefits provided by high‐quality disperser at local scales may not emerge at broader geographical scales. In Caatinga vegetation, diaspores are submitted to strong abiotic filters that constraint seed germination and establishment after the dispersal phase. Such abiotic filters may dilute the initial benefit provided by long‐distance dispersers. Therefore, we suggest that in dry environments like the Caatinga, the benefits of long‐distance removals should be outweighed by the risk of reach new habitats with unfavourable conditions for germination and establishment.     

Phylogeography of a host-specific insect: genetic structure of Ips typographus in Europe does not reflect past fragmentation of its host

The phylogeography of the bark beetle Ips typographus was assessed using five microsatellite markers. Twenty-eight populations were sampled throughout Europe on the host tree Picea abies . I. typographus showed very low levels of genetic diversity, and the study revealed a lack of genetic structure across Europe. No significant barrier to gene flow was found, even though P. abies has a fragmented distribution. A weak but significant effect of isolation by distance was found. These results suggest a high dispersal capacity of I. typographus , which leads to low genetic differentiation between populations. Its high dispersal capacity is likely to have prevented I. typographus from developing important local adaptations to its host, which would have influenced its genetic structure. The nuclear data was compared to previously published mitochondrial data that showed strong differentiation between Central–Northern European populations and Russian–Baltic populations, and a founder effect in Scandinavia, probably reflecting the postglacial history of I. typographus . Discrepancies between nuclear and mitochondrial markers could be due to the maternal inheritance of mitochondrial DNA, and to sex-biased dispersal in I. typographus . The overall low genetic diversity observed on both markers on a large geographical scale is discussed. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 239–246.     

Glacial survival may matter after all: nunatak signatures in the rare European populations of two west-arctic species

Biogeographers claimed for more than a century that arctic plants survived glaciations in ice-free refugia within the limits of the North European ice sheets. Molecular studies have, however, provided overwhelming support for postglacial immigration into northern Europe, even from the west across the Atlantic. For the first time we can here present molecular evidence strongly favouring in situ glacial persistence of two species, the rare arctic-alpine pioneer species Sagina caespitosa and Arenaria humifusa. Both belong to the 'west-arctic element' of amphi-Atlantic disjuncts, having their few and only European occurrences well within the limits of the last glaciation. Sequencing of non-coding regions of chloroplast DNA revealed only limited variation. However, two very distinct and partly diverse genetic groups, one East and one West Atlantic, were detected in each species based on amplified fragment length polymorphisms (AFLPs), excluding postglacial dispersal from North America as explanation for their European occurrences. Patterns of genetic diversity and distinctiveness indicate that glacial populations existed in East Greenland and/or Svalbard (A. humifusa) and in southern Scandinavia (S. caespitosa). Despite their presumed lack of long-distance dispersal adaptations, intermixed populations in several regions indicate postglacial contact zones. Both species are declining in Nordic countries, probably due to climate change-induced habitat loss. Little or no current connectivity between their highly fragmented and partly distinct populations call for conservation of several populations in each geographic region.     

Endemic species may have complex histories: within‐refugium phylogeography of an endangered Iberian vole

Glacial refugia protected and promoted biodiversity during the Pleistocene, not only at a broader scale, but also for many endemics that contracted and expanded their ranges within refugial areas. Understanding the evolutionary history of refugial endemics is especially important in the case of endangered species to recognize the origins of their genetic structure and thus produce better informed conservation practices. The Iberian Peninsula is an important European glacial refugium, rich in endemics of conservation concern, including small mammals, such as the Cabrera vole (Microtus cabrerae). This near‐threatened rodent is characterized by an unusual suite of genetic, life history and ecological traits, being restricted to isolated geographic nuclei in fast‐disappearing Mediterranean subhumid herbaceous habitats. To reconstruct the evolutionary history of the Cabrera vole, we studied sequence variation at mitochondrial, autosomal and sex‐linked loci, using invasive and noninvasive samples. Despite low overall mitochondrial and nuclear nucleotide diversities, we observed two main well‐supported mitochondrial lineages, west and east. Phylogeographic modelling in the context of the Cabrera vole's detailed fossil record supports a demographic scenario of isolation of two populations during the Last Glacial Maximum from a single focus in the southern part of the Iberian Peninsula. In addition, our data suggest subsequent divergence within the east, and secondary contact and introgression of the expanding western population, during the late Holocene. This work emphasizes that refugial endemics may have a phylogeographic history as rich as that of more widespread species, and conservation of such endemics includes the preservation of that genetic legacy.     

A multi-compartmented glacial refugium in the northern Rocky Mountains: Evidence from the phylogeography of <Emphasis Type="Italic">Cardamine constancei</Emphasis> (Brassicaceae)

The age and origin of the mesic coniferous forest ecosystem of the Pacific Northwest of North America have long been the subject of debate by biogeographers. Cardamine constancei, an endemic of the Rocky Mountain segment of this ecosystem, was subjected to phylogeographic analysis to test explicit hypotheses on the age of the ecosystem. We have predicted genetic homogeneity among river drainages if C. constancei and other associated species migrated into the region after glaciation, in contrast to the genetic differentiation that may have accrued if the species and its ecosystem have long survived in the relatively warm river canyons south of glaciation. We detected 19 haplotypes with divergence up to 1.5%, and they comprise 4 well-differentiated cpDNA clades. These clades are allopatric except for two haplotypes from the lower Clearwater clade that appear to have dispersed north into partial sympatry with the clade endemic to St.␣Joe River. The divergence and distribution of these clades is consistent with the existence of a complex glacial refugium with at least four compartments. The surprisingly high cpDNA diversity within this species suggests that conservation of mesic coniferous forest ecosystems in the region warrant a conservation plan that accounts for the historically imposed spatial structure of genetic diversity. We are currently testing our phylogeographic hypotheses by the comparative analyses of a suite of plants, animals and fungi.     

Phylogeography of the pademelons (Marsupialia: Macropodidae: Thylogale) in New Guinea reflects both geological and climatic events during the Plio‐Pleistocene

Aim Alternative hypotheses concerning genetic structuring of the widespread endemic New Guinean forest pademelons (Thylogale) based on current taxonomy and zoogeography (northern, southern and montane species groupings) and preliminary genetic findings (western and eastern regional groupings) are investigated using mitochondrial sequence data. We examine the relationship between the observed phylogeographical structure and known or inferred geological and historical environmental change during the late Tertiary and Quaternary. Location New Guinea and associated islands. Methods We used primarily museum specimen collections to sample representatives from Thylogale populations across New Guinea and three associated islands. Mitochondrial cytochrome b and control region sequence data were used to construct phylogenies and estimate the timing of population divergence. Results Phylogenetic analyses indicated subdivision of pademelons into ‘eastern’ and ‘western’ regional clades. This was largely due to the genetic distinctiveness of north‐eastern and eastern peninsula populations, as the ‘western’ clade included samples from the northern, southern and central regions of New Guinea. Two tested island groups were closely related to populations north of the Central Cordillera; low genetic differentiation of pademelon populations between north‐eastern New Guinea and islands of the Bismarck Archipelago is consistent with late Pleistocene human‐mediated translocations, while the Aru Islands population showed divergence consistent with cessation of gene flow in the mid Pleistocene. There was relatively limited genetic divergence between currently geographically isolated populations in subalpine and nearby mid‐montane or lowland regions. Main conclusions Phylogeographical structuring does not conform to zoogeographical expectations of a north/south division across the cordillera, nor to current species designations, for this generalist forest species complex. Instead, the observed genetic structuring of Thylogale populations has probably been influenced by geological changes and Pleistocene climatic changes, in particular the recent uplift of the north‐eastern Huon Peninsula and the lowering of tree lines during glacial periods. Low sea levels during glacial maxima also allowed gene flow between the continental Aru Island group and New Guinea. More work is needed, particularly multi‐taxon comparative studies, to further develop and test phylogeographical hypotheses in New Guinea.     

Molecular phylogeography of Jerdon’s pitviper (Protobothrops jerdonii): importance of the uplift of the Tibetan plateau

Aim To investigate the population history and demographics of Jerdon’s pitviper, Protobothrops jerdonii, and elucidate how the unique physical conditions and heterogeneous mountain environments resulting from the uplift of the Tibetan Plateau shaped the genetic diversity and evolutionary history of the species. Location China and Vietnam. Methods We sequenced and analysed a total of 1752 base pairs from two mitochondrial genes, cytochrome b (cyt b) and NADH dehydrogenase subunit (ND4), for 81 specimens sampled from 27 localities across the species’ range, and a total of 464 base pairs from two nuclear genes for 28 representative samples from all mitochondrial DNA lineages. Based on these data, we constructed the genealogical relationships and estimated the divergence times of the mitochondrial DNA clades. Results The mitochondrial DNA results revealed the existence of five distinct, strongly supported and geographically structured DNA lineages within populations of P. jerdonii that are paraphyletic with respect to Protobothrops xiangchengensis. Estimation of divergence dates suggested that P. jerdonii possibly evolved in the western Hengduan Mountains region c. 6.6 Ma in the late Miocene. Nuclear DNA data did not provide sufficient resolution to distinguish the mitochondrial DNA lineages. Main conclusions Based on the present‐day distribution and intraspecific genealogy, the evolutionary history of P. jerdonii can be explained by a pattern of dispersal followed by vicariance. All lines of evidence suggest that historical biogeographical factors, particularly the north–south orientation of the higher mountains, as well as low‐elevation areas in western China, had the greatest influence on the population structure, lineage formation and species distribution of this snake. However, highly heterogeneous habitats and glacial cycles appear to have affected patterns of intraspecific differentiation. While our mitochondrial data provide evidence for clear phylogeographical structure, our small sampling of nuclear genes does not, suggesting that nuclear markers may not have had sufficient time to coalesce to match patterns observed in the mitochondrial data.