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Combined Evidence Reveals the Origin of a Rapid Range Expansion Despite Retained Genetic Diversity and a Weak Founder Effect.

Many species are currently experiencing range shifts in response to changing environmental conditions with potentially serious genetic consequences. Repeated founder events and strong genetic drift are expected to erode genetic variation at the range front, reducing adaptive potential and slowing or even halting the expansion. However, the severity of these consequences for common and highly mobile species undergoing environment-driven range shifts (c.f. invasions) is less clear. Here, we combined historical observations and contemporary movement data of the common reed warbler (Acrocephalus scirpaceus) with genomic evidence from across its European breeding range to (1) infer the origin and (2) quantify the genetic consequences of a recent and rapid northward range expansion. Although there were no reductions in levels of nucleotide diversity or allelic richness, nor a signal of founder effect in the directionality index (ψ), our combined dataset approach was able to infer an expansion origin from the southwest. Furthermore, we found that private allelic richness retained a slight but significant linear decline along the colonisation route. These results suggest that high dispersal capabilities can allow even philopatric species to avoid the loss of genetic diversity during rapid range expansions. Nevertheless, if multiple lines of evidence enable identification of an expansion pathway, we may still detect genetic signals of expansion.

Founder Effect↗

A dispersal model for the range expansion of blacklegged tick (Acari: Ixodidae).

The blacklegged tick, Ixodes scapularis Say, a vector for the agents of Lyme borreliosis and other diseases, has expanded its range dramatically over the past 20 yr. However, the relative contributions of different vertebrate host species to this expansion have remained largely unexplored. To address this issue, we simulated the expansion of a theoretical tick population across a simple landscape by using a deterministic, spatially explicit, cellular automata model. The model incorporates the ecology of ticks and three vertebrate hosts: white-tailed deer, Odocoileus virginianus Zimmermann; white-footed mouse, Peromyscus leucopus Rafinesque; and American robin, Turdus migratorius L. Host contribution to tick dispersal is modeled as a function of tick burden, home range size, and population density. These parameters were determined using published and unpublished data. Our results suggest that 1) hosts with high tick burdens and large home ranges (e.g., deer) play a critical role in I. scapularis range expansion; 2) hosts with small home ranges (e.g., mice) can limit range expansion if they divert a sufficient number of ticks from feeding on more mobile hosts; and (3) birds that migrate annually (e.g., robins) can play a crucial role in tick range expansion.

Animals↗

Winter warming facilitates range expansion: cold tolerance of the butterfly Atalopedes campestris.

Our ability to predict ecological and evolutionary responses to climate change requires an understanding of the mechanistic links between climate and range limits. The warming trend over the past half-century has generated numerous opportunities to develop much-needed case studies of these links. Species that are only limited by climatic factors are likely to shift range quickly during periods of warming. Such species directly impact recipient communities and indicate trends that will become more widespread. Because minimum temperature (T (min)) is rising at twice the rate of maximum temperature, species with this range-limiting factor may be especially responsive to global warming. In this study, I test the hypothesis that rising T (min) has directly affected the range of a skipper butterfly. Atalopedes campestris has moved northward rapidly this century, recently colonizing eastern Washington where January T (min) has risen 3 degrees C in 50 years. The results show that: 1. A. campestris' range lies completely within the -4 degrees C January average minimum isotherm, and that recently colonized areas were below this threshold earlier this century. 2. In acute cold stress experiments, -4 to -7 degrees C proved to be a critical thermal limit: median supercooling point was -6.3 degrees C, and minimum lethal temperature (LT50 with 12-h exposure) was -5.7 degrees C. 3. In chronic cold stress experiments, survivorship declined sharply in diurnally fluctuating thermal regimes typical of the current range edge. High mortality occurred under constant 0 degrees C conditions as well as in fluctuating regimes, implying that thermal insulation from snow would not protect A. campestris. 4. There was no evidence of evolution in cold tolerance at the range margin, despite strong selection. Thus, winter warming was apparently a prerequisite for the range expansion. Characteristics of this species that seem to be associated with its rapid response are that it is an opportunistic species, it is not habitat or dispersal limited, and it is constrained by T (min).

Acclimatization↗

Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration.

Long-distance population dispersal leaves its characteristic signature in genomes, namely, reduced diversity and increased linkage between genetic markers. This signature enables historical patterns of range expansion to be traced. Herein, we use microsatellite loci from the human pathogen Coccidioides immitis to show that genetic diversity in this fungus is geographically partitioned throughout North America. In contrast, analyses of South American C. immitis show that this population is genetically depauperate and was founded from a single North American population centered in Texas. Variances of allele distributions show that South American C. immitis have undergone rapid population growth, consistent with an epidemic increase in postcolonization population size. Herein, we estimate the introduction into South America to have occurred within the last 9,000-140,000 years. This range increase parallels that of Homo sapiens. Because of known associations between Amerindians and this fungus, we suggest that the colonization of South America by C. immitis represents a relatively recent and rapid codispersal of a host and its pathogen.

Base Sequence↗

A novel expression system based on host-range expansion of baculovirus.

A host range expanded recombinant Autographa californica multiple-nucleocapsid nucleopolyhedrosis virus AcMNPV/r2 was obtained by cotransfection of the bacmid DNA from Escherichia coli DH10Bac along with a plasmid pBmH-M containing HindIII M fragment of Bombyx mori nuclear polyhedrosis virus (BmNPV) genomic DNA. A recombinant transposon vector carrying a mutant green fluorescent protein gene (GFP) and a polyhedrin gene was constructed. Transposition was carried out in both E. coli DH10Bac and E. coli DH10BmH, which contains AcMNPV/r2 and a helper plasmid. Recombinant DNAs were transfected into Sf-9 cells to generate recombinant virus AcMNPV/r3 and AcMNPV/r4 respectively. Viral stock of AcMNPV/r4 was then infected into Bombyx mori cells (BmN) and Bombyx mori larvae (silkworm). Analysis shows that GFP was highly expressed in Bombyx mori larvae. This expression system, is practicable therefore for mass production of foreign gene products.

Animals↗

Contrasting effects of long distance seed dispersal on genetic diversity during range expansion.

Currently many attempts are made to reconstruct the colonization history of plant species after the last ice age. A surprising finding is that during the colonization phase genetic diversity did not decrease as much as expected. In this paper we examine whether long distance seed dispersal events could play a role in the unexpected maintenance of genetic diversity during range expansion. This study is based on simulations carried out with a maternally inherited haploid locus using a cellular automaton. The simulations reveal a close relationship between the frequency of long distance seed dispersal events and the amount of genetic diversity preserved during colonization. In particular, when the colonized region is narrow, a complete loss of genetic diversity results from the occurrence of very rare long distance dispersal (LDD) events. We call this phenomenon the 'embolism effect'. However, slightly higher rates of LDD events reverse this effect, up to the point that diversity is better preserved than in a pure diffusion model. This phenomenon is linked to the reorganization of the genetic structure during colonization and is called the 'reshuffling effect'.

Computer Simulation↗

Climate-driven range expansion and morphological evolution in a marine gastropod.

Little is known about the phenotypic consequences of global climate change, despite the excellent Pleistocene fossil record of many taxa. We used morphological measurements from extant and Pleistocene populations of a marine gastropod (Acanthinucella spirata) in conjunction with mitochondrial DNA sequence variation from living populations to determine how populations responded phenotypically to Pleistocene climatic changes. Northern populations show little sequence variation as compared to southern populations, a pattern consistent with a recent northward range expansion. These recently recolonized northern populations also contain shell morphologies that are absent in extant southern populations and throughout the Pleistocene fossil record. Thus, contrary to traditional expectations that morphological evolution should occur largely within Pleistocene refugia, our data show that geographical range shifts in response to climatic change can lead to significant morphological evolution.

Animals↗

Phylogeography of Arcterica nana (Ericaceae) suggests another range expansion history of Japanese alpine plants.

We conducted a phylogeographic study on the alpine plant Arcterica nana based on haplotypes of chloroplast DNA. Using a sequence of approximately 1,071 bp of intergenic spacers of chloroplast DNA (trnT-L, psbB-psbF), we detected 13 haplotypes among 193 individuals sampled from 22 populations. Two dominant haplotypes were distributed over the entire range of this species in Japan, and we found several local private haplotypes. An analysis of molecular variance (AMOVA) indicated no geographic structure within the haplotype distribution. In addition, the genetic distance was not related to its corresponding geographic distance (Mantel test: r=-0.049, P=0.66), indicating a homogeneous geographic structure throughout the entire distribution range in the Japanese archipelago. The most parsimonious explanation for this geographic structure is that A. nana spread across its extant distribution range in the Japanese archipelago through a recent range expansion event. However, this pattern is inconsistent with the previous phylogeography of Japanese alpine plants, which reveals that haplotypes in central Honshu are differentiated from those in more northern regions. Arcterica nana may have experienced a different history from other alpine plants, suggesting that the history of Japanese alpine flora may include at least two different geographic radiation patterns.

DNA, Chloroplast↗

Modern humans did not admix with Neanderthals during their range expansion into Europe.

The process by which the Neanderthals were replaced by modern humans between 42,000 and 30,000 before present is still intriguing. Although no Neanderthal mitochondrial DNA (mtDNA) lineage is found to date among several thousands of Europeans and in seven early modern Europeans, interbreeding rates as high as 25% could not be excluded between the two subspecies. In this study, we introduce a realistic model of the range expansion of early modern humans into Europe, and of their competition and potential admixture with local Neanderthals. Under this scenario, which explicitly models the dynamics of Neanderthals' replacement, we estimate that maximum interbreeding rates between the two populations should have been smaller than 0.1%. We indeed show that the absence of Neanderthal mtDNA sequences in Europe is compatible with at most 120 admixture events between the two populations despite a likely cohabitation time of more than 12,000 y. This extremely low number strongly suggests an almost complete sterility between Neanderthal females and modern human males, implying that the two populations were probably distinct biological species.

Animals↗

Population genetic structure of the malaria mosquito Anopheles arabiensis across Nigeria suggests range expansion.

Ten microsatellite loci, four located within and six outside chromosome inversions, were employed to study the genetic structure of Anopheles arabiensis across the ecological zones of Nigeria (arid savannah in the north gradually turns into humid forest in the south). Regardless of location within or outside inversions, genetic variability at all loci was characterized by a reduction in both the number of alleles per locus and heterozygosity from savannah to forest. Across all loci, all but one allele in the forest also occurred in the savannah, whereas at least 78 alleles in the savannah were missing in the forest. Genetic differentiation increased with geographical distance; consequently, genetic distances between zones exceeded those within zones. The largest genetic distances were between localities at the extremes of the transect (range F(ST) = 0.196-0.258 and R(ST) = 0.183-0.468) and were as large as those between A. arabiensis and Anopheles gambiae s.s. Gene flow across the country was very low, so that Nm between the extremes of the transect was < 1. These data suggest that A. arabiensis has extended its range from the savannah into the forest during which it experienced a reduction in effective population size due to sequential founder effects. Gene flow post range expansion appears too restricted by geographical distance to homogenize the gene pool of A. arabiensis across Nigeria.

Alleles↗

Recency, range expansion, and unsorted lineages: implications for interpreting neutral genetic variation in the sharp-tailed grouse (Tympanuchus phasianellus).

Both current and historical patterns of variation are relevant to understanding and managing ecological diversity. Recently derived species present a challenge to the reconstruction of historical patterns because neutral molecular data for these taxa are more likely to exhibit effects of recent and ongoing demographic processes. We studied geographical patterns of neutral molecular variation in a species thought to be of relatively recent origin, Tympanuchus phasianellus (sharp-tailed grouse), using mitochondrial control region sequences (CR-I), amplified fragment length polymorphisms (AFLP), and microsatellites. For historical context, we also analysed CR-I in all species of Tympanuchus. Within T. phasianellus, we found evidence for restricted gene flow between eastern and western portions of the species range, generally corresponding with the range boundary of T. p. columbianus and T. p. jamesi. The mismatch distribution and molecular clock estimates from the CR-I data suggested that all Tympanuchus underwent a range expansion prior to sorting of mitotypes among the species, and that sorting may have been delayed as a result of mutation-drift disequilibrium. This study illustrates the challenge of using genetic data to detect historical divergence in groups that are of relatively recent origin, or that have a history dominated by nonequilibrium conditions. We suggest that in such cases, morphological, ecological, and behavioural data may be particularly important adjuncts to molecular data for the recognition of historically or adaptively divergent groups.

Animals↗

Recent range expansion and low levels of contemporary gene flow in Calomys musculinus: its relationship with the emergence and spread of Argentine haemorrhagic fever.

The geographic distribution of haplotype diversity in the rodent Calomys musculinus, sampled from 16 wild populations of Argentina, was analysed on two geographical scales. The species is the natural reservoir of the Junin virus, the etiological agent of the Argentine haemorrhagic fever (AHF). In all, 24 composite haplotypes were recognised in the mtDNA D-loop region. Haplotypes 1 and 2, internal in the network, were the most frequent and were present in almost all populations. The absence of large genetic gaps between widely distributed haplotypes, the existence of exclusive haplotypes in more than 50% of the sampled populations and the absence of isolation by distance at a macrogeographical scale are in support of the hypothesis of a recent range expansion of the populations of the Humid Pampa, with low to moderate current gene flow. The dispersal of this opportunistic species would have been favoured by the explosive increments in density after agriculture was introduced. When only nearby populations within the endemic area of AHF were considered, a pattern of isolation by distance was detected. At present, genetic drift appears to be the main force acting to randomly differentiate C. musculinus populations, which would also lead to random differentiation of Junin virus strains and a reduction in the virulence of the pathogen in 'historic' AHF areas. The knowledge of migration patterns of the reservoir populations facilitates reliable prediction of the potential spread of the human disease.

Animals↗

Distortion of symmetrical introgression in a hybrid zone: evidence for locus-specific selection and uni-directional range expansion.

The fate of species integrity upon natural hybridization depends on the interaction between selection and dispersal. The relative significance of these processes may be studied in the initial phase of contact before selection and gene flow reach equilibrium. Here we study a hybrid zone of two salamander species, Lyciasalamandra antalyana and Lyciasalamandra billae, at the initial phase of hybridization. We quantify the degree and mode of introgression using nuclear and mtDNA markers. The hybrid zone can be characterized as an abrupt transition zone, the central hybrid zone being only c. 400 m, but introgressed genes were traced up to 3 km. Introgression was traced in both sexes but gene flow may be slightly male-biased. Indirect evidence suggests that hybrid males are less viable than females. Introgression occurred at two levels: (1) locus-specific selection led to different allelic introgression patterns independent of species, while (2) asymmetrical species-level introgression occurred predominately from L. antalyana to L. billae due to range expansion of the former. This indicates that foreign genes can be incorporated into novel genomic environments, which in turn may contribute to the great diversity of morphological variants in Lyciasalamandra.

Amphibians↗

Genetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses.

Six variable microsatellite loci were used to examine genetic structuring in the closely related shy albatross (Thalassarche cauta) and white-capped albatross (T. steadi). First, levels of genetic differentiation between the species, and among three populations within each species, were analysed using amova, FST and RST. We found high levels of genetic structuring and detected many unshared alleles between the species, which provide strong evidence against any contemporary gene flow between them. Within each species, shy albatross populations were found to be genetically distinct whereas white-capped albatross populations were undifferentiated, which implies that dispersal events are much rarer in the former than in the latter. These results formed the basis for the recommendation that the three white-capped albatross populations (as a whole) and each shy albatross population be treated as separate units for conservation. Second, levels of genetic diversity and allelic patterns in shy and white-capped albatrosses were assessed for whether they support earlier mtDNA results suggesting that shy albatrosses arose through range expansion of white-capped albatrosses. All measures indicated lower genetic diversity within shy albatrosses than within white-capped albatrosses and upheld the hypothesis that shy albatrosses were founded by white-capped albatrosses.

Analysis of Variance↗

Range expansion leading to departures from neutrality in the nonsymbiotic hemoglobin gene and the cpDNA trnL-trnF intergenic spacer in Trema dielsiana (Ulmaceae).

The population genetics and phylogeography of Trema dielsiana in Taiwan were inferred from genetic diversity at the nonsymbiotic hemoglobin gene and the trnL-trnF intergenic spacer of cpDNA. Reduced genetic variation was detected in these two unlinked genes. The gene genealogy of the hemoglobin locus recovered two lineages corresponding to the western and eastern regions of Taiwan. This pattern is compatible with a past fragmentation event revealed by phylogeographical analyses. To distinguish between selective departures from neutrality (i.e., heterogeneous processes) and demographic (homogeneous) processes, Hahn et al.'s heterogeneity test was conducted on the hemoglobin gene. Lack of significant differences in Tajima's D statistics between synonymous and nonsynonymous mutations indicates that homogeneous processes may have played a key role in governing the evolution of the functional locus. Significantly negative Tajima's D estimates for both overall exons and introns of the hemoglobin gene as well as for the cpDNA intergenic spacer support a phylogeographical hypothesis of range expansion after genetic bottlenecks. High level of genetic variation and a negative Tajima's D statistic suggests a possible northern refugium that may have harbored populations during the glacial maximum.

Cell Nucleus↗

Genetic differentiation of the marbled white butterfly, Melanargia galathea, accounts for glacial distribution patterns and postglacial range expansion in southeastern Europe.

Isolation of Mediterranean species in the southern European peninsulas during the cold glacial phases often resulted in differentiation of several genetic lineages confined to the respective peninsulas. However, whilst there is good genetic evidence for multiple refugia in Iberia, there are only limited data available for the Balkans. Therefore, we wish to examine the hypothesis of a strong genetic structuring within southeastern Europe for the existence of multiple Balkan differentiation centres and/or several leading edges. As a model we use the marbled white butterfly, Melanargia galathea. We studied 18 allozyme loci of 564 individuals from 16 populations distributed over a large part of southeastern Europe. The single populations showed moderately high genetic diversity and no northward decline of genetic diversity was detected. The overall genetic differentiation between populations was considerable (F(ST) 7.0%). Cluster analysis discriminated three genetic groups: (i) a western flank in the former Yugoslavia, parts of eastern Austria and Hungary; (ii) an eastern flank with populations from Bulgaria and Romania (south of the southern Carpathians and eastern Carpathians); and (iii) the eastern Carpathian Basin. Hierarchical variance analysis distributed 53% of the variance among populations between these three groups. One sample from the Greek-Bulgarian border clustered within the eastern flank, but showed some tendency towards the eastern Carpathian Basin populations. Two populations from Carinthia clustered together with the eastern Carpathian Basin ones and a population from Styria showed an intermediate genetic composition between the three groups. Most probably, the eastern and the western flank groups are due to postglacial range expansion from the northeastern and the northwestern edges of the glacial differentiation centre (so-called leading edges). The eastern Carpathian Basin group may have resulted from postglacial expansion from northern Greece through valley systems of the central Balkan peninsula, maybe even expanding westwards north of the Balkan mountains reaching some parts of eastern Austria (e.g. Carinthia). Therefore, the Balkanic refugium of M. galathea may or may not have been continuous along the coastal areas of the Mediterranean, but must have been strongly genetically structured.

Animal Migration↗

Elastographic dynamic range expansion using variable applied strains.

In elastography, we want to image the entire range of stiffnesses of the elastic components found in inhomogeneous tissues. In order to achieve this, the elastographic dynamic range should equal the entire stiffness dynamic range in the target. Various sources of noise limit the dynamic range of elastography. The recently-defined strain filter concept offers an analytical and graphical way of observing these limitations. In this paper, we describe a method that achieves the expansion of the elastographic dynamic range. It involves the application of variable strains in combination with selective storage of strain data that have optimal elastographic signal-to-noise ratios. This expands the current dynamic range of elastography by orders of magnitude when compared to single compression elastography. The process is explained theoretically using the strain filter framework, and 1 D as well as 2D tissue simulations are used to corroborate the theory.

Algorithms↗