Changing patterns of genetic differentiation in the slender wild oat, Avena barbata.

The slender wild oat (Avena barbata) was widely studied in California using allozymes in the 1970s and interpreted as a case of ecotypic adaptation to contrasting moisture environments. However, common garden studies suggested that the moist-associated ("mesic") ecotype had high fitness in both moist and dry habitats, thus predicting an adaptive spread into areas occupied by the dry associated ("xeric") ecotype. To test this prediction, we revisited 100 populations of A. barbata that were screened genetically 40 y ago. As expected, mesic allozyme and morphological markers are much more common than in the 1970s. The less-fit xeric ecotype, while still widespread, has declined markedly in range and frequency. Genotyping by sequencing of modern populations reveals striking genetic uniformity within each of the two ecotypes. In recombinants between the two ecotypes, the mesic allele at a major fitness quantitative trait locus (QTL) shows a high frequency but so do many other genomic regions not identified as fitness QTL. Additional introduced genotypes are diverse and more widespread than in the past, and our results show that these have spread into the former range of the xeric ecotype to an even greater extent than the mesic ecotype has. While these results confirm the prediction of contemporary evolution from common gardens, they also suggest that much of the change has been driven by additional waves of introduced genotypes.

Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish.

Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

Genetic structure and range expansion of Zeugodacus Cucurbitae (Diptera: Tephritidae) in Africa.

Hypotheses about the worldwide colonization routes of the melon fly, Zeugodacus cucurbitae (Diptera: Tephritidae), are mainly based on sparse historical records. Here we aim at reconstructing the colonization history of the African continent based on an improved description of the population structure of Z. cucurbitae and approximate Bayesian analyses. Individuals of Z. cucurbitae were sampled in 17 localities from East, West and Central Africa and genotyped at 19 microsatellite markers. Bayesian analyses showed intracontinental population structuring with populations from Uganda diverging from those of Tanzania and populations from Burundi and Kenya showing traces of admixture with West African samples. Approximate Bayesian Computation provided support to the hypothesis of a single introduction Z. cucurbitae into East Africa and subsequent expansion to West Africa, each colonization event was followed by a bottleneck that promoted population divergence within Africa. Parameter estimates suggested that these events are roughly compatible with the historical records of Z. cucurbitae presence in sub-Saharan Africa (viz. 1936 in East Africa and 1999 in West Africa) and allow excluding alternative hypotheses on older or multiple introductions of Z. cucurbitae.

Mice as stowaways? Colonization history of Danish striped field mice.

Species from the steppe region of Eastern Europe likely colonized northwestern Europe in connection with agriculture after 6500 BP. The striped field mouse (Apodemus agrarius Pallas, 1783), is a steppe-derived species often found in human crops. It is common on the southern Danish islands of Lolland and Falster, which have been isolated from mainland Europe since approximately 10 300-8000 BP. Thus, this species could have been brought in with humans in connection with agriculture, or it could be an earlier natural invader. We sequenced 86 full mitochondrial genomes from the northwestern range of the striped field mouse, analysed phylogenetic relationships and estimated divergence time. The results supported human-induced colonization of Denmark in the Subatlantic or Subboreal period. A newly discovered population from Central Jutland in Denmark diverged from Falster approximately 100-670 years ago, again favouring human introduction. One individual from Sweden turned out to be a recent introduction from Central Jutland.

A portrait of a sucker using landscape genetics: how colonization and life history undermine the idealized dendritic metapopulation.

Dendritic metapopulations have been attributed unique properties by in silico studies, including an elevated genetic diversity relative to a panmictic population of equal total size. These predictions have not been rigorously tested in nature, nor has there been full consideration of the interacting effects among contemporary landscape features, colonization history and life history traits of the target species. We tested for the effects of dendritic structure as well as the relative importance of life history, environmental barriers and historical colonization on the neutral genetic structure of a longnose sucker (Catostomus catostomus) metapopulation in the Kogaluk watershed of northern Labrador, Canada. Samples were collected from eight lakes, genotyped with 17 microsatellites, and aged using opercula. Lakes varied in differentiation, historical and contemporary connectivity, and life history traits. Isolation by distance was detected only by removing two highly genetically differentiated lakes, suggesting a lack of migration-drift equilibrium and the lingering influence of historical factors on genetic structure. Bayesian analyses supported colonization via the Kogaluk's headwaters. The historical concentration of genetic diversity in headwaters inferred by this result was supported by high historical and contemporary effective sizes of the headwater lake, T-Bone. Alternatively, reduced allelic richness in headwaters confirmed the dendritic structure's influence on gene flow, but this did not translate to an elevated metapopulation effective size. A lack of equilibrium and upstream migration may have dampened the effects of dendritic structure. We suggest that interacting historical and contemporary factors prevent the achievement of the idealized traits of a dendritic metapopulation in nature.

The role of neutral and adaptive evolutionary processes on patterns of genetic diversity across small cave-dwelling populations of Icelandic Arctic charr (Salvelinus alpinus).

Understanding the adaptability of small populations in the face of environmental change is a central problem in evolutionary biology. Solving this problem is challenging because neutral evolutionary processes that operate on historical and contemporary timescales can override the effects of selection in small populations. We assessed the effects of isolation by colonization (IBC), isolation by dispersal limitation (IBDL) as reflected by a pattern of isolation by distance (IBD), and isolation by adaptation (IBA) and the roles of genetic drift and gene flow on patterns of genetic differentiation among 19 cave-dwelling populations of Icelandic Arctic charr (Salvelinus alpinus). We detected evidence of IBC based on the genetic affinity of nearby cave populations and the genetic relationships between the cave populations and the presumed ancestral population in the lake. A pattern of IBD was evident regardless of whether high-level genetic structuring (IBC) was taken into account. Genetic signatures of bottlenecks and lower genetic diversity in smaller populations indicate the effect of drift. Estimates of gene flow and fish movement suggest that gene flow is limited to nearby populations. In contrast, we found little evidence of IBA as patterns of local ecological and phenotypic variation showed little association with genetic differentiation among populations. Thus, patterns of genetic variation in these small populations likely reflect localized gene flow and genetic drift superimposed onto a larger-scale structure that is largely a result of colonization history. Our simultaneous assessment of the effects of neutral and adaptive processes in a tractable and replicated system has yielded novel insights into the evolution of small populations on both historical and contemporary timescales and over a smaller spatial scale than is typically studied.

No evidence for local adaptation in an invasive alien plant: field and greenhouse experiments tracing a colonization sequence.

BACKGROUND AND AIMS: Local adaptation enables plant species to persist under different environmental conditions. Evolutionary change can occur rapidly in invasive annual species and has been shown to lead to local adaptation. However, the patterns and mechanisms of local adaptation in invasive species along colonization sequences are not yet understood. Thus, in this study the alien annual Impatiens glandulifera was used to investigate local adaptation to distinct habitats that have been consecutively invaded in central Europe. METHODS: A reciprocal transplant experiment was performed using 15 populations from alluvial deciduous forests, fallow meadows and coniferous upland forests, and a greenhouse experiment was performed in which plants from these habitats were grown under treatments reflecting the main habitat differentiators (shade, soil acidity, competition). KEY RESULTS: Biomass production, specific leaf area, plant height and relative growth rate differed between habitats in the field experiment and between treatments in the greenhouse, but not between seed origins. Overall, there was no indication of local adaptation in either experiment. CONCLUSIONS: Since I. glandulifera is a successful invader in many habitats without showing local adaptation, it is suggested that the species is coping with environmental variation by means of high phenotypic plasticity. The species seems to follow a 'jack-and-master' strategy, i.e. it is able to maintain high fitness under a wide range of environmental conditions, but performs particularly well in favourable habitats. Therefore, the proposed colonization sequence is likely to be based primarily on changes in propagule pressure. It is concluded that invasive alien plants can become dominant in distinct habitats without local adaptation.

Was Jeju Island a glacial refugium for East Asian warm-temperate plants? Insights from the homosporous fern Selliguea hastata (Polypodiaceae).

PREMISE OF THE STUDY: We posed two hypotheses for broad scenarios of postglacial recolonization of Korea by the warm-temperate vegetation: (1) that extant Korean populations are derived from a single refugium, or (2) that they are derived from multiple refugia. We chose a homosporous fern typical of East Asian warm-temperate vegetation, Selliguea hastata, to test which of the two scenarios is more likely and to check whether Japan contained putative glacial refugia. METHODS: Using 16 allozyme loci, we obtained genotypes of 756 individuals from 20 populations, representative of the whole distribution area in Korea (including Jeju Island), Japan, and Taiwan. We assessed genetic variability within and among populations, Wright's F-statistics, and conducted analysis of molecular variance, model-based Bayesian clustering, and bottleneck tests. KEY RESULTS: We found no allozyme variation within populations of S. hastata in mainland Korea, whereas genetic polymorphism was detected for populations from Jeju Island, Japan (in particular a population from southeastern Shikoku), and Taiwan. The levels of inbreeding within populations were high, consistent with the potential of S. hastata for intragametophytic selfing. CONCLUSIONS: Data on allelic richness together with Bayesian clustering methods suggest a pattern of postglacial recolonization of mainland Korea from a single refugium, probably located either on Jeju Island or in Japan. Jeju Island should merit the highest priority for conservation biogeography, as it played a role as a Quaternary refugium for arctic-alpine, boreal, temperate as well as warm-temperate plants, as suggested here.

Comparative phylogeography of two commensal rat species (Rattus tanezumi and Rattus norvegicus) in China: Insights from mitochondrial DNA, microsatellite, and 2b-RAD data.

Rattus norvegicus and Rattus tanezumi are dominant species of Chinese house rats, but the colonization and demographic history of two species in China have not been thoroughly explored. Phylogenetic analyses with mitochondrial DNA including 486 individuals from 31 localities revealed that R. norvegicus is widely distributed in China, R. tanezumi is mainly distributed in southern China with currently invading northward; northeast China was the natal region of R. norvegicus, while the spread of R. tanezumi in China most likely started from the southeast coast. A total of 123 individuals from 18 localities were subjected to 2b-RAD analyses. In neighbor-joining tree, individuals of R. tanezumi grouped into geographic-specific branches, and populations from southeast coast were ancestral groups, which confirmed the colonization route from southeast coast to central and western China. However, individuals of R. norvegicus were generally grouped into two clusters instead of geographic-specific branches. One cluster comprised inland populations, and another cluster included both southeast coast and inland populations, which indicated that spread history of R. norvegicus in China was complex; in addition to on-land colonization, shipping transportation also have played great roles. ADMIXTURE and principal component analyses provided further supports for the colonization history. Demographic analyses revealed that climate changes at ~40,000 to 18,000 years ago and ~4000 years ago had led to population declines of both species; the R. norvegicus declined rapidly while the population of R. tanezumi continuously expanded since ~1500 years ago, indicating the importance of interspecies' competition in their population size changes. Our study provided a valuable framework for further investigation on phylogeography of two species in China.

Genomic variation, population history and within-archipelago adaptation between island bird populations.

Oceanic island archipelagos provide excellent models to understand evolutionary processes. Colonization events and gene flow can interact with selection to shape genetic variation at different spatial scales. Landscape-scale variation in biotic and abiotic factors may drive fine-scale selection within islands, while long-term evolutionary processes may drive divergence between distantly related populations. Here, we examine patterns of population history and selection between recently diverged populations of the Berthelot's pipit (Anthus berthelotii), a passerine endemic to three North Atlantic archipelagos. First, we use demographic trees and f3 statistics to show that genome-wide divergence across the species range is largely shaped by colonization and bottlenecks, with evidence of very weak gene flow between populations. Then, using a genome scan approach, we identify signatures of divergent selection within archipelagos at single nucleotide polymorphisms (SNPs) in genes potentially associated with craniofacial development and DNA repair. We did not detect within-archipelago selection at the same SNPs as were detected previously at broader spatial scales between archipelagos, but did identify signatures of selection at loci associated with similar biological functions. These findings suggest that similar ecological factors may repeatedly drive selection between recently separated populations, as well as at broad spatial scales across varied landscapes.

Priority effects: How the order of arrival of an invasive grass, Bromus tectorum, alters productivity and plant community structure when grown with native grass species.

Theories and models attempt to explain how and why particular plant species grow together at particular sites or why invasive exotic species dominate plant communities. As local climates change and human-use degrades and disturbs ecosystems, a better understanding of how plant communities assemble is pertinent, particularly when restoring grassland ecosystems that are frequently disturbed. One such community assembly theory is priority effects, which suggests that arrival order of species into a community alters plant-plant interactions and community assembly. Theoretically, priority effects can have lasting effects on ecosystems and will likely be altered as the risk of invasion by exotic species increases. It is difficult to predict how and when priority effects occur, as experimental reconstruction of arrival order is often difficult in adequate detail. As a result, limited experimental studies have explored priority effects on plant community assembly and plant invasions. To determine if and how priority effects affect the success of invasive species, we conducted a greenhouse study exploring how the arrival order of an invasive grass, Bromus tectorum, affects productivity and community composition when grown with native grasses. We found evidence for priority effects, as productivity was positively related to dominance of B. tectorum and was greater the earlier B. tectorum arrived. This suggests that priority effects could be important for plant communities as the early arrival of an invasive species drastically impacted the productivity and biodiversity of our system at the early establishment stages of plant community development.

Postglacial colonization history reflects in the genetic structure of natural populations of Festuca rubra in Europe.

We conducted a large-scale population genetic survey of genetic diversity of the host grass Festuca rubra s.l., which fitness can be highly dependent on its symbiotic fungus Epichloë festucae, to evaluate genetic variation and population structure across the European range. The 27 studied populations have previously been found to differ in frequencies of occurrence of the symbiotic fungus E. festucae and ploidy levels. As predicted, we found decreased genetic diversity in previously glaciated areas in comparison with nonglaciated regions and discovered three major maternal genetic groups: southern, northeastern, and northwestern Europe. Interestingly, host populations from Greenland were genetically similar to those from the Faroe Islands and Iceland, suggesting gene flow also between those areas. The level of variation among populations within regions is evidently highly dependent on the postglacial colonization history, in particular on the number of independent long-distance seed colonization events. Yet, also anthropogenic effects may have affected the population structure in F. rubra. We did not observe higher fungal infection rates in grass populations with lower levels of genetic variability. In fact, the fungal infection rates of E. festucae in relation to genetic variability of the host populations varied widely among geographical areas, which indicate differences in population histories due to colonization events and possible costs of systemic fungi in harsh environmental conditions. We found that the plants of different ploidy levels are genetically closely related within geographic areas indicating independent formation of polyploids in different maternal lineages.

Landscape genetic structure of Scirpus mariqueter reveals a putatively adaptive differentiation under strong gene flow in estuaries.

Estuarine organisms grow in highly heterogeneous habitats, and their genetic differentiation is driven by selective and neutral processes as well as population colonization history. However, the relative importance of the processes that underlie genetic structure is still puzzling. Scirpus mariqueter is a perennial grass almost limited in the Changjiang River estuary and its adjacent Qiantang River estuary. Here, using amplified fragment length polymorphism (AFLP), a moderate-high level of genetic differentiation among populations (range F ST: 0.0310-0.3325) was showed despite large ongoing dispersal. FLOCK assigned all individuals to 13 clusters and revealed a complex genetic structure. Some genetic clusters were limited in peripheries compared with very mixing constitution in center populations, suggesting local adaptation was more likely to occur in peripheral populations. 21 candidate outliers under positive selection were detected, and further, the differentiation patterns correlated with geographic distance, salinity difference, and colonization history were analyzed with or without the outliers. Combined results of AMOVA and IBD based on different dataset, it was found that the effects of geographic distance and population colonization history on isolation seemed to be promoted by divergent selection. However, none-liner IBE pattern indicates the effects of salinity were overwhelmed by spatial distance or other ecological processes in certain areas and also suggests that salinity was not the only selective factor driving population differentiation. These results together indicate that geographic distance, salinity difference, and colonization history co-contributed in shaping the genetic structure of S. mariqueter and that their relative importance was correlated with spatial scale and environment gradient.

Lessons from a natural experiment: Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way.

Explaining why some lineages diversify while others do not and how are key objectives in evolutionary biology. Young radiations of closely related species derived from the same source population provide an excellent opportunity to disentangle the relative contributions of possible drivers of diversification. In these settings, lineage-specific effects are shared and can be ruled out. Moreover, the relevant demographic and ecological parameters can be estimated accurately. Midas cichlid fish in Nicaragua have repeatedly colonized several crater lakes, diverged from the same source populations, and, interestingly, diversified in some of them but not others. Here, using the most comprehensive molecular and geometric morphometric data set on Midas cichlids to date (∼20,000 SNPs, 12 landmarks, ∼700 individuals), we aim to understand why and how crater lake populations diverge and why some of them are more prone to diversify in sympatry than others. Taking ancestor-descendant relationships into account, we find that Midas cichlids diverged in parallel from their source population mostly-but not exclusively-by evolving more slender body shapes in all six investigated crater lakes. Admixture among crater lakes has possibly facilitated this process in one case, but overall, admixture and secondary waves of colonization cannot predict morphological divergence and intralacustrine diversification. Instead, morphological divergence is larger the more dissimilar a crater lake is compared to the source lake and happens rapidly after colonization followed by a slow-down with time. Our data also provide some evidence that founder effects may positively contribute to divergence. The depth of a crater lake is positively associated with variation in body shapes (and number of species), presumably by providing more ecological opportunities. In conclusion, we find that parallel morphological divergence in allopatry and the propensity for diversification in sympatry across the entire Midas cichlid fish radiation is partly predictable and mostly driven by ecology.

Species ecological similarity modulates the importance of colonization history for adaptive radiation.

Adaptive radiation is an important evolutionary process, through which a single ancestral lineage rapidly gives rise to multiple newly formed lineages that specialize in different niches. In the first-arrival hypothesis, David Lack emphasized the importance of species colonization history for adaptive radiation, suggesting that the earlier arrival of a diversifying species would allow it to radiate to a greater extent. Here, we report on the first rigorous experimental test of this hypothesis, using the rapidly evolving bacterium Pseudomonas fluorescens SBW25 and six different bacterial competitors. We show that the earlier arrival of P. fluorescens facilitated its diversification. Nevertheless, significant effects of colonization history, which led to alternative diversification trajectories, were observed only when the competitors shared similar niche and competitive fitness with P. fluorescens. These results highlight the important role of species colonization history, modified by their ecological differences, for adaptive radiation.

Multiple, independent colonizations of the Hawaiian Archipelago by the family Dolichopodidae (Diptera).

The family Dolichopodidae forms two of the four largest evolutionary radiations in the Hawaiian Islands across all flies: Campsicnemus (183 spp) and the Eurynogaster complex (66 spp). They also include a small radiation of Conchopus (6 spp). A handful of other dolichopodid species are native to the islands in singleton lineages or small radiations. This study provides a phylogenetic perspective on the colonization history of the dolichopodid fauna in the islands. We generated a multi-gene data set including representatives from 11 of the 14 endemic Hawaiian dolichopodid genera to examine the history of colonization to the islands, and analyzed it using Bayesian and maximum likelihood phylogenetic methods. We used a subset of the data that included Conchopus and the eight genera comprising the Eurynogaster complex to estimate the first phylogenetic hypothesis for these endemic groups, then used Beast to estimate their age of arrival to the archipelago. The Eurynogaster complex, Campsicnemus and Conchopus are clearly the result of independent colonizations. The results strongly support the Eurynogaster complex as a monophyletic group, and also supports the monophyly of 4 of the 8 described genera within the complex (Adachia, Arciellia, Uropachys and Eurynogaster). Members of the family Dolichopodidae have been dispersing over vast distances to colonize the Hawaiian Archipelago for millions of years, leading to multiple independent evolutionary diversification events. The Eurynogaster complex arrived in the Hawaiian Archipelago 11.8 Ma, well before the arrival of Campsicnemus (4.5 Ma), and the even more recent Conchopus (1.8 Ma). Data presented here demonstrate that the Hawaiian Dolichopodidae both disperse and diversify easily, a rare combination that lays the groundwork for field studies on the reproductive isolating mechanisms and ecological partitioning of this group.

MITOCHONDRIAL DNA VARIATION IN THE FIELD VOLE (MICROTUS AGRESTIS): REGIONAL POPULATION STRUCTURE AND COLONIZATION HISTORY.

Restriction fragment length polymorphism analysis of mitochondrial DNA (mtDNA) was used to examine the genetic structure among field voles (Microtus agrestis) from southern and central Sweden. A total of 57 haplotypes was identified in 158 voles from 60 localities. Overall mtDNA diversity was high, but both haplotype and nucleotide diversity exhibited pronounced geographic heterogeneity. Phylogenetic analyses revealed a shallow tree with seven primary mtDNA lineages separated by sequence divergences ranging from 0.6% to 1.0%. The geographic structure of mtDNA diversity and lineage distribution was complex but strongly structured and deviated significantly from an equilibrium situation. The extensive mtDNA diversity observed and the recent biogeographic history of the region suggests that the shallow mtDNA structure in the field vole cannot be explained solely by stochastic lineage sorting in situ or isolation by distance. Instead, the data suggest that the genetic imprints of historical demographic conditions and vicariant geographic events have been preserved and to a large extent determine the contemporary geographic distribution of mtDNA variation. A plausible historical scenario involves differentiation of mtDNA lineages in local populations in glacial refugia, a moving postglacial population structure, and bottlenecks and expansions of mtDNA lineages during the postglacial recolonization of Sweden. By combining the mtDNA data with an analysis of Y-chromosome variation, a specific population unit was identified in southwestern Sweden. This population, defined by a unique mtDNA lineage and fixation of a Y-chromosome variant, probably originated in a population bottleneck in southern Sweden about 12,000 to 13,000 calendar years ago.