Recent range expansion and agricultural landscape heterogeneity have only minimal effect on the spatial genetic structure of the plant pathogenic fungus Mycosphaerella fijiensis

Understanding how geographical and environmental features affect genetic variation at both the population and individual levels is crucial in biology, especially in the case of pathogens. However, distinguishing between these factors and the effects of historical range expansion on spatial genetic structure remains challenging. In the present study, we investigated the case of Mycosphaerella fijiensis—a plant pathogenic fungus that has recently colonized an agricultural landscape characterized by the presence of potential barriers to gene flow, including several commercial plantations in which disease control practises such as the use of fungicides are applied frequently, and low host density areas. We first genotyped 300 isolates sampled at a global scale on untreated plants in two dimensions over a 50 × 80-km area. Using two different clustering algorithms, no genetic structure was detected in the studied area, suggesting expansion of large populations and/or no influence of potential barriers. Second, we investigated the potential effect of disease control practises on M. fijiensis diversity by comparing populations sampled in commercial vs food-crop plantations. At this local scale, we detected significantly higher allelic richness inside commercial plantations compared with the surrounding food-crop plantation populations. Analysis of molecular variance indicated that 99% of the total genetic variance occurred within populations. We discuss the suggestion that high population size and/or high migration rate between populations might be responsible for the absence of any effect of disease control practises on genetic diversity and differentiation.     

The importance of long-distance dispersal in biodiversity conservation

Dispersal is universally considered important for biodiversity conservation. However, the significance of long‐ as opposed to short‐distance dispersal is insufficiently recognized in the conservation context. Long‐distance dispersal (LDD) events, although typically rare, are crucial to population spread and to maintenance of genetic connectivity. The main threats to global biodiversity involve excessive LDD of elements alien to ecosystems and insufficient dispersal of native species, for example, because of habitat fragmentation. In this paper, we attempt to bridge the gap in the treatment of LDD by reviewing the conservation issues for which LDD is most important. We then demonstrate how taking LDD into consideration can improve conservation management decisions.     

Retention of gene diversity during the spread of a non‐native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.     

Movement ofMycosphaerella fijiensis spores and sigatoka disease development on plantain close to an inoculum source

Investigations into the short-distance dispersal of ascospores and conidia ofMycosphaerella fijiensis and subsequent disease development, from point sources of inoculum, were carried out in a small plot of 100 initially uninfected plantain plants in Costa Rica during 1995. Plants were examined every 4 days from the time of planting in early May for the first appearance of disease symptoms. After 3 months, all plants were infected. Levels of inoculum within the plot were monitored with spore traps and weather data were collected. Results suggested that Black Sigatoka disease was spread on the wind, with conidia ofM. fijiensis probably responsible for short-distance dispersal and ascospores for spread of the disease over longer distances. No evidence was found to support splash dispersal of these spores.     

Breach of the northern Rocky Mountain geoclimatic barrier: initiation of range expansion by the mountain pine beetle

Aim Our aim is to examine the historical breach of the geoclimatic barrier of the Rocky Mountains by the mountain pine beetle (Dendroctonus ponderosae Hopkins). This recent range expansion from west of the North American continental divide into the eastern boreal forest threatens to provide a conduit to naïve pine hosts in eastern North America. We examine the initial expansion events and determine potential mechanism(s) of spread by comparing spread patterns in consecutive years to various dispersal hypotheses such as: (1) meso‐scale atmospheric dispersal of insects from source populations south‐west of the Rocky Mountains in British Columbia (i.e. their historical range), (2) anthropogenic transport of infested plant material, and (3) spread of insect populations across adjacent stands via corridors of suitable habitat. Location British Columbia, Canada. Methods We explore potential mechanism(s) of invasion of the mountain pine beetle using spatial point process models for the initial 3 years of landscape‐level data collection, 2004–2006. Specifically, we examine observed patterns of infestation relative to covariates reflecting various dispersal hypotheses. We select the most parsimonious models for each of the initial 3 years of invasion using information criteria statistics. Results The initial range expansion and invasion of the beetle was characterized by aerial deposition along a strong north‐west to south‐east gradient, with additional aerial deposition and localized dispersal from persisting populations in following years. Main conclusions Following deposition of a wave front of mountain pine beetles parallel to the Rocky Mountains via meso‐scale atmospheric dispersal, the areas of highest intensity of infestations advanced up to 25 km north‐east towards jack pine (Pinus banksiana) habitat in a single year. There appeared to be no association between putative anthropogenic movement of infested materials and initial range expansion of the mountain pine beetle across the continental divide.     

Polymerase chain reaction–restriction fragment length polymorphism markers for the fungal banana pathogen Mycosphaerella fijiensis

Polymerase chain reaction–restriction fragment length polymorphism markers were developed to study populations of the fungal banana pathogen Mycosphaerella fijiensis. Twelve markers were defined, 11 in anonymous and single‐copy nuclear DNA sequences and one in the internal transcribed spacer and 5.8S rDNA sequence. The polymerase chain reaction products obtained with locus‐specific primer pairs were digested with restriction enzymes to reveal polymorphism. Between five and 12 markers were polymorph in M. fijiensis populations from different geographical origins (Papua New Guinea, the Philippines, Cameroon and Latin America). The mean of allele number and gene diversity (expected heterozygosity) per locus in the different geographical populations ranged between 1.4 and 2.7 and 0.17 and 0.45, respectively.     

Drifting fronds and drifting alleles: range dynamics,local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides

Aim The seaweed Fucus ceranoides is restricted to spatially discrete estuarine habitats and lacks planktonic dispersal phases; it is therefore expected to exhibit strong population differentiation. Its cold‐temperate affinities and mtDNA variation imply that the northern part of the species’ range, where F. ceranoides is now ubiquitous, was recently colonized after the onset of the last deglaciation, potentially resulting in areas with greater genetic homogeneity. Here we examine the population structure of F. ceranoides to test these predictions, emphasizing the contrasting genetic signatures of limited dispersal in refugial versus recently colonized regions. Location North‐eastern Atlantic estuaries from Portugal to Norway. Methods A total of 504 individuals from 21 estuarine sites spanning the entire range of F. ceranoides were sampled and genotyped for nine microsatellite loci. Population structure was inferred from several genotypic and allele‐frequency analyses. Geographical patterns of genetic diversity were used to reconstruct the historical biogeography of the species. Results Genetic diversity and regional population differentiation showed a consistent decline with increasing latitude. Southernmost populations harboured most of the endemic variation, whereas the northern populations (> 55° N) were almost fixed for the same alleles across loci. In southern and central regions of its distribution, F. ceranoides showed striking population subdivision, with many of the sampled estuaries corresponding to coherent genetic units that were easily discriminated from one another with standard clustering methods. Main conclusions The geographical pattern of genetic diversity supports the long‐term refugial status of Iberia and a post‐glacial range expansion of F. ceranoides into previously glaciated latitudes. Despite the species’ capacity to colonize newly available habitats, the genetic structure of F. ceranoides outside the recently (re)colonized range reveals that gene flow between populations is extremely low. This study provides a remarkable example of how infrequent and spatially limited dispersal can have contrasting effects at the scales of meta‐population (connectivity) versus range dynamics (habitat tracking), and of how dispersal restrictions can result in either genetic divergence or homogeneity depending on the maturity and demographic conditions of the populations.     

Shifting dispersal modes at an expanding species’ range margin

While it is generally recognized that noncontiguous (long‐distance) dispersal of small numbers of individuals is important for range expansion over large geographic areas, it is often assumed that colonization on more local scales proceeds by population expansion and diffusion dispersal (larger numbers of individuals colonizing adjacent sites). There are few empirical studies of dispersal modes at the front of expanding ranges, and very little information is available on dispersal dynamics at smaller geographic scales where we expect contiguous (diffusion) dispersal to be prevalent. We used highly polymorphic genetic markers to characterize dispersal modes at a local geographic scale for populations at the edge of the range of a newly invasive grass species (Brachypodium sylvaticum) that is undergoing rapid range expansion in the Pacific Northwest of North America. Comparisons of Bayesian clustering of populations, patterns of genetic diversity, and gametic disequilibrium indicate that new populations are colonized ahead of the invasion front by noncontiguous dispersal from source populations, with admixture occurring as populations age. This pattern of noncontiguous colonization was maintained even at a local scale. Absence of evidence for dispersal among adjacent pioneer sites at the edge of the expanding range of this species suggests that pioneer populations undergo an establishment phase during which they do not contribute emigrants for colonization of neighbouring sites. Our data indicate that dispersal modes change as the invasion matures: initial colonization processes appear to be dominated by noncontiguous dispersal from only a few sources, while contiguous dispersal may play a greater role once populations become established.     

Using neutral cline decay to estimate contemporary dispersal: a generic tool and its application to a major crop pathogen

Dispersal is a key parameter of adaptation, invasion and persistence. Yet standard population genetics inference methods hardly distinguish it from drift and many species cannot be studied by direct mark‐recapture methods. Here, we introduce a method using rates of change in cline shapes for neutral markers to estimate contemporary dispersal. We apply it to the devastating banana pest Mycosphaerella fijiensis, a wind‐dispersed fungus for which a secondary contact zone had previously been detected using landscape genetics tools. By tracking the spatio‐temporal frequency change of 15 microsatellite markers, we find that σ, the standard deviation of parent–offspring dispersal distances, is 1.2 km/generation^1/2. The analysis is further shown robust to a large range of dispersal kernels. We conclude that combining landscape genetics approaches to detect breaks in allelic frequencies with analyses of changes in neutral genetic clines offers a powerful way to obtain ecologically relevant estimates of dispersal in many species.     

Genetic analysis across different spatial scales reveals multiple dispersal mechanisms for the invasive hydrozoan Cordylophora in the Great Lakes

Discerning patterns of post‐establishment spread by invasive species is critically important for the design of effective management strategies and the development of appropriate theoretical models predicting spatial expansion of introduced populations. The globally invasive colonial hydrozoan Cordylophora produces propagules both sexually and vegetatively and is associated with multiple potential dispersal mechanisms, making it a promising system to investigate complex patterns of population structure generated throughout the course of rapid range expansion. Here, we explore genetic patterns associated with the spread of this taxon within the North American Great Lakes basin. We collected intensively from eight harbours in the Chicago area in order to conduct detailed investigation of local population expansion. In addition, we collected from Lakes Michigan, Erie, and Ontario, as well as Lake Cayuga in the Finger Lakes of upstate New York in order to assess genetic structure on a regional scale. Based on data from eight highly polymorphic microsatellite loci we examined the spatial extent of clonal genotypes, assessed levels of neutral genetic diversity, and explored patterns of migration and dispersal at multiple spatial scales through assessment of population level genetic differentiation (pairwise F_ST and factorial correspondence analysis), Bayesian inference of population structure, and assignment tests on individual genotypes. Results of these analyses indicate that Cordylophora populations in this region spread predominantly through sexually produced propagules, and that while limited natural larval dispersal can drive expansion locally, regional expansion likely relies on anthropogenic dispersal vectors.     

Northwestward range expansion of the bumblebee Bombus haematurus into Central Europe is associated with warmer winters and niche conservatism

Species range expansions are crucial for understanding niche formation and the interaction with the environment. Here, we studied the bumblebee Bombus haematurus Kriechbaumer, 1870, a species historically distributed from northern Serbia through northern Iran which has very recently started expanding northwestward into Central Europe without human-mediated dispersal (i.e., it is a natural spread). After updating the global distribution of this species, we investigated if niche shifts took place during this range expansion between newly colonized and historical areas. In addition, we have explored which climatic factors may have favored the natural range expansion of the species. Our results indicated that Bombus haematurus has colonized large territories in 7 European countries outside the historical area in the period from the 1980s to 2018, a natural expansion over an area that equals 20% of the historical distribution. In addition, this bumblebee performs generalism in flower visitation and it occurs in different habitats, although a preference for forested areas clearly emerges. The land-use associated with the species in the colonized areas is similar to the historical distribution, indicating that no major niche shifts occurred during the spread. Furthermore, in recently colonized localities, the range expansion was associated with warming temperatures during the winter and also during both queen overwintering and emergence phases. These findings document a case of natural range expansion due to environmental change rather than due to niche shifts, and specifically they suggest that warmer winters could be linked to the process of natural colonization of new areas.     

Population genetic structure of a common host predicts the spread of white‐nose syndrome,an emerging infectious disease in bats

Landscape complexity influences patterns of animal dispersal, which in turn may affect both gene flow and the spread of pathogens. White‐nose syndrome (WNS) is an introduced fungal disease that has spread rapidly throughout eastern North America, causing massive mortality in bat populations. We tested for a relationship between the population genetic structure of the most common host, the little brown myotis (Myotis lucifugus), and the geographic spread of WNS to date by evaluating logistic regression models of WNS risk among hibernating colonies in eastern North America. We hypothesized that risk of WNS to susceptible host colonies should increase with both geographic proximity and genetic similarity, reflecting historical connectivity, to infected colonies. Consistent with this hypothesis, inclusion of genetic distance between infected and susceptible colonies significantly improved models of disease spread, capturing heterogeneity in the spatial expansion of WNS despite low levels of genetic differentiation among eastern populations. Expanding our genetic analysis to the continental range of little brown myotis reveals strongly contrasting patterns of population structure between eastern and western North America. Genetic structure increases markedly moving westward into the northern Great Plains, beyond the current distribution of WNS. In western North America, genetic differentiation of geographically proximate populations often exceeds levels observed across the entire eastern region, suggesting infrequent and/or locally restricted dispersal, and thus relatively limited opportunities for pathogen introduction in western North America. Taken together, our analyses suggest a possibly slower future rate of spread of the WNS pathogen, at least as mediated by little brown myotis.     

Lichen colonization patterns show minor effects of dispersal distance at landscape scale

The role of dispersal in controlling the distribution of species at landscape scale (10²–10⁴ m) is still a matter of dispute. Here, we use the early colonization pattern of 23 epiphytic lichen species in a former tree‐less heathland landscape (170 km²) to test three hypotheses on how a landscape is colonized: A) mainly by long‐distance dispersal (LDD), B) by rare LDD events followed by limited local dispersal, and C) mainly by limited dispersal, resulting in a colonization front. The study system consisted of a chronosequence of 94 habitat patches constituting 0.4% of the landscape area, with a minimum inter‐site distance of 0.2 km. We used generalized linear mixed models with Bayesian inference to test predictions from the hypotheses. When age of sites and habitat area were accounted for, additional effects of geographical position of sites (distance from old sites, distance‐dependent relative propagule pressure, and distance from border of study area) on the probability of colonization by lichen species were small. Furthermore, species richness of sites did not depend on geographical position, either. Our results support a colonization process mainly governed by LDD at landscape scale, and that local stepwise colonization was not important. We argue that passively dispersed species with numerous small propagules tend to exhibit patchy populations with extensive dispersal at the landscape scale, rather than behaving like classical metapopulations.     

Biogeographically dynamic genetic structure bridging two continents in the monotypic Central American rodent Ototylomys phyllotis

Central America is an ideal region in which to study patterns of historical divergence and population genetic differentiation, because of its extraordinarily dynamic biogeographical, tectonic, and climatic history. The rodent Ototylomys phyllotis is the only extant species of the genus Ototylomys and is distributed within this region from the Isthmus of Tehuantepec, Mexico, to central Costa Rica, offering an excellent opportunity to study spatial and temporal patterns of population structure of the species and to explain the ecological and evolutionary processes responsible for those patterns. We estimated the genetic diversity and structure within and between populations of O. phyllotis, times of divergence, and migration patterns using mitochondrial DNA and a comprehensive combination of phylogenetic and phylogeographical computational analyses. Our results support monophyly of the genus Ototylomys. We identified three major phylogeographical lineages within O. phyllotis that are linked to its diversification and coincide with the main geological features that shaped Middle America. The origin of the genus was before 3.35 Mya, prior to the Great American Biotic Interchange (GABI), and its initial occurrence was near the centre of its current distribution (Honduras/El Salvador), from which it later spread (3.20–2.84 Mya) following a series of GABI pulses. The species showed an initial northward dispersal to the Chiapas and Guatemala highlands (2.27 Mya) followed by diversification. A later dispersal (1.82 Mya) occurred toward both the south (Nicaragua, Costa Rica) and the north (Belize). The Yucatan peninsula was colonized (0.8 Mya) by individuals from Belize. Extremely high radiation and range expansion occurred throughout the entire range, the highest of which was in the Yucatan peninsula (0.125 Mya). © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 593–610.     

Reconstruction of a windborne insect invasion using a particle dispersal model,historical wind data,and Bayesian analysis of genetic data

Understanding how invasive species establish and spread is vital for developing effective management strategies for invaded areas and identifying new areas where the risk of invasion is highest. We investigated the explanatory power of dispersal histories reconstructed based on local‐scale wind data and a regional‐scale wind‐dispersed particle trajectory model for the invasive seed chalcid wasp Megastigmus schimitscheki (Hymenoptera: Torymidae) in France. The explanatory power was tested by: (1) survival analysis of empirical data on M. schimitscheki presence, absence and year of arrival at 52 stands of the wasp's obligate hosts, Cedrus (true cedar trees); and (2) Approximate Bayesian analysis of M. schimitscheki genetic data using a coalescence model. The Bayesian demographic modeling and traditional population genetic analysis suggested that initial invasion across the range was the result of long‐distance dispersal from the longest established sites. The survival analyses of the windborne expansion patterns derived from a particle dispersal model indicated that there was an informative correlation between the M. schimitscheki presence/absence data from the annual surveys and the scenarios based on regional‐scale wind data. These three very different analyses produced highly congruent results supporting our proposal that wind is the most probable vector for passive long‐distance dispersal of this invasive seed wasp. This result confirms that long‐distance dispersal from introduction areas is a likely driver of secondary expansion of alien invasive species. Based on our results, management programs for this and other windborne invasive species may consider (1) focusing effort at the longest established sites and (2) monitoring outlying populations remains critically important due to their influence on rates of spread. We also suggest that there is a distinct need for new analysis methods that have the capacity to combine empirical spatiotemporal field data, genetic data, and environmental data to investigate dispersal and invasion.     

The interplay of dispersal limitation,rivers, and historical events shapes the genetic structure of an Amazonian frog

Disentangling the impact of landscape features such as rivers and historical events on dispersal is a challenging but necessary task to gain a comprehensive picture of the evolution of diverse biota such as that found in Amazonia. Adenomera andreae, a small, territorial, terrestrial frog species of the Amazonian forest represents a good model for such studies. We combined cytochrome b sequences with 12 microsatellites to investigate the genetic structure at two contrasted spatial scales in French Guiana: along a ～6‐km transect, to evaluate dispersal ability, and between paired bank populations along a ～65‐km stretch of the Approuague river, to test the effect of rivers as barriers to dispersal. We observed significant spatial genetic structure between individuals at a remarkably small geographical scale, and conclude that the species has a restricted dispersal ability that is probably tied to its life‐history traits. Mitochondrial and microsatellite data also indicate a high level of differentiation among populations on opposite banks of the river, and, in some cases, among populations on the same riverbank. These results suggest that the observed population structure in A. andreae is the result of restricted dispersal abilities combined with the action of rivers and Quaternary population isolation. Given that Amazonia hosts a great portion of anurans, as well as other small vertebrates, that display life‐history traits comparable with A. andreae, we argue that our analyses provide new insights into the complex interactions among evolutionary processes shaping Amazonian biodiversity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 356–373.     

Range expansion and retraction along a moving contact zone has no effect on the genetic diversity of two passerine birds

Disentangling the factors shaping species distributions remains a central goal in biogeography, ecology and evolutionary biology. The extrinsic pressures that may facilitate range shifts, such as climatic factors or biotic interactions are well known. However, in contrast, the possible intrinsic factors are manifold and hard to generalize across taxa. Recently, several theoretical studies have investigated the consequences of moving range borders on genetic diversity. However, empirical studies that support or refute these theoretical predictions are scarce. Moving contact zones between parapatric sister species are suitable models to test these hypotheses. Changes in genetic diversity can be tested simultaneously along the expanding and receding edges of two species of the contact zone while accounting for intra‐specific effects (e.g. introgression). The two Old World warblers Hippolais polyglotta and H. icterina form a narrow moving contact zone, where interspecific interactions are suspected to be the main factor shaping this zone. We investigated the population genetic structure of both species along a transect ranging from the core range of the expanding H. polyglotta across the contact zone and far into the range of the receding H. icterina. The theoretical predictions of changes in genetic diversity at the range edges were tested. No gradual change in genetic diversity was detected for both the expanding and the receding range margin. Furthermore, no genetic structure was found in either species supporting the hypothesis that long distance dispersal (LDD) occurs frequently due to the high mobility of these long‐distance migrants. The results suggest that when dispersal propensity is high and accompanied by frequent LDD events, then neither an enrichment nor a depletion of alleles along moving range edges would be detected. This these species as the probability to retain genetic diversity during exogenous induced range shifts is high in such mobile species.     

The genetic signature of rapid range expansions: How dispersal,growth and invasion speed impact heterozygosity and allele surfing

As researchers collect spatiotemporal population and genetic data in tandem, models that connect demography and dispersal to genetics are increasingly relevant. The dominant spatiotemporal model of invasion genetics is the stepping-stone model which represents a gradual range expansion in which individuals jump to uncolonized locations one step at a time. However, many range expansions occur quickly as individuals disperse far from currently colonized regions. For these types of expansion, stepping-stone models are inappropriate. To more accurately reflect wider dispersal in many organisms, we created kernel-based models of invasion genetics based on integrodifference equations. Classic theory relating to integrodifference equations suggests that the speed of range expansions is a function of population growth and dispersal. In our simulations, populations that expanded at the same speed but with spread rates driven by dispersal retained more heterozygosity along axes of expansion than range expansions with rates of spread that were driven primarily by population growth. To investigate surfing we introduced mutant alleles in wave fronts of simulated range expansions. In our models based on random mating, surfing alleles remained at relatively low frequencies and surfed less often compared to previous results based on stepping-stone simulations with asexual reproduction.     

Intercontinental long‐distance seed dispersal across the Mediterranean Basin explains population genetic structure of a bird‐dispersed shrub

Long‐distance dispersal (LDD) is a pivotal process for plants determining their range of distribution and promoting gene flow among distant populations. Most fleshy‐fruited species rely on frugivorous vertebrates to disperse their seeds across the landscape. While LDD events are difficult to record, a few ecological studies have shown that birds move a sizeable number of ingested seeds across geographic barriers, such as sea straits. The foraging movements of migrant frugivores across distant populations, including those separated by geographic barriers, creates a constant flow of propagules that in turn shapes the spatial distributions of the genetic variation in populations. Here, we have analysed the genetic diversity and structure of 74 populations of Pistacia lentiscus, a fleshy‐fruited shrub widely distributed in the Mediterranean Basin, to elucidate whether the Mediterranean Sea acts as a geographic barrier or alternatively whether migratory frugivorous birds promote gene flow among populations located on both sides of the sea. Our results show reduced genetic distances among populations, including intercontinental populations, and they show a significant genetic structure across an eastern‐western axis. These findings are consistent with known bird migratory routes that connect the European and African continents following a north‐southwards direction during the fruiting season of many fleshy‐fruited plants. Further, approximate Bayesian analysis failed to explain the observed patterns as a result of historical population migrations at the end of Last Glacial Maximum. Therefore, anthropic and/or climatic changes that would disrupt the migratory routes of frugivorous birds might have genetic consequences for the plant species they feed upon.