Prey‐processing by avian predators enhances virus transmission in the gypsy moth

The Lymantria dispar nucleopolyhedrovirus (LdNPV) is one of the most important regulators of gypsy moth populations, but some aspects of its transmission remain poorly understood, particularly its high rate of spatial spread and ability to persist in low‐density populations. We tested the role of predatory birds in the transmission of this virus using experimental gypsy moth populations in an aviary. Predatory birds captured virus‐infected caterpillars and facilitated viral dispersal via two processes: 1) by ingesting infected caterpillars and passing viral occlusion bodies (OBs) through their guts, and 2) by scattering OBs during predator‐specific processing behaviors, a mechanism documented here for the first time. The relative importance of both pathways differed by predator species. After eating virus‐infected gypsy moth larvae, red‐eyed vireos and black‐capped chickadees passed more gypsy moth nucleopolyhedrovirus in feces than did gray catbirds. During prey‐processing, the repetitive beating of caterpillars by red‐eyed vireos, a behavior that was rarely utilized by chickadees and catbirds, resulted in the scattering of infectious virus. Due to the combination of efficient gut passage and virus spread from prey beating, higher rates of transmission occurred in experimental gypsy moth populations exposed to red‐eyed vireos than those exposed to catbirds or chickadees. Our results show that effective virus transmission was achieved when virus was vectored by predatory birds through a combination of both behavioral and physiological traits.     

Variation in growth and developmental responses to supraoptimal temperatures near latitudinal range limits of gypsy moth Lymantria dispar (L.), an expanding invasive species

Variation in thermal performance within and between populations provides the potential for adaptive responses to increasing temperatures associated with climate change. Organisms experiencing temperatures above their optimum on a thermal performance curve exhibit rapid declines in function and these supraoptimal temperatures can be a critical physiological component of range limits. The gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae), is one of the best‐documented biological invasions and factors driving its spatial spread are of significant ecological and economic interest. The present study examines gypsy moth sourced from different latitudes across its North American range for sensitivity to high temperature in constant temperature growth chamber experiments. Supraoptimal temperatures result in higher mortality in northern populations compared with populations from the southern range extent (West Virginia and coastal plain of Virginia, U.S.A.). Sublethal effects of high temperature on traits associated with fitness, such as smaller pupal mass, are apparent in northern and West Virginia populations. Overall, the results indicate that populations near the southern limits of the range are less sensitive to high temperatures than northern populations from the established range. However, southern populations are lower performing overall, based on pupal mass and development time, relative to northern populations. This suggests that there may be a trade‐off associated with decreased heat sensitivity in gypsy moth. Understanding how species adapt to thermal limits and possible fitness trade‐offs of heat tolerance represents an important step toward predicting climatically driven changes in species ranges, which is a particularly critical consideration in conservation and invasion ecology.     

The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe

Gypsy moth, Lymantria dispar L., is one of the most important pests of deciduous trees in Europe. In regular cycles, it causes large‐scale defoliation mostly of oak, Quercus spp., forests. Government authorities in the most infested countries in Europe conduct large‐scale applications of pesticides against gypsy moth. In 1999, a new natural enemy, the entomopathogenic fungus Entomophaga maimaiga, was successfully introduced into a gypsy moth population in Bulgaria. Recent investigations suggest that now E. maimaiga is quickly spreading in Europe. Herein, past studies are reviewed regarding this fungus with special emphasis on its potential for becoming an important factor regulating gypsy moth populations in Europe, focusing on the host's population dynamics in relation to the fungus, the influence of environmental conditions on fungal activity, the influence of E. maimaiga on the native entomofauna, including other gypsy moth natural enemies, and spread of the fungus. Based on this analysis, the potential of E. maimaiga for providing control in European gypsy moth populations is estimated.     

Genetic structure,admixture and invasion success in a Holarctic defoliator,the gypsy moth (Lymantria dispar,Lepidoptera: Erebidae)

Characterizing the current population structure of potentially invasive species provides a critical context for identifying source populations and for understanding why invasions are successful. Non‐native populations inevitably lose genetic diversity during initial colonization events, but subsequent admixture among independently introduced lineages may increase both genetic variation and adaptive potential. Here we characterize the population structure of the gypsy moth (Lymantria dispar Linnaeus), one of the world's most destructive forest pests. Native to Eurasia and recently introduced to North America, the current distribution of gypsy moth includes forests throughout the temperate region of the northern hemisphere. Analyses of microsatellite loci and mitochondrial DNA sequences for 1738 individuals identified four genetic clusters within L. dispar. Three of these clusters correspond to the three named subspecies; North American populations represent a distinct fourth cluster, presumably a consequence of the population bottleneck and allele frequency change that accompanied introduction. We find no evidence that admixture has been an important catalyst of the successful invasion and range expansion in North America. However, we do find evidence of ongoing hybridization between subspecies and increased genetic variation in gypsy moth populations from Eastern Asia, populations that now pose a threat of further human‐mediated introductions. Finally, we show that current patterns of variation can be explained in terms of climate and habitat changes during the Pleistocene, a time when temperate forests expanded and contracted. Deeply diverged matrilines in Europe imply that gypsy moths have been there for a long time and are not recent arrivals from Asia.     

Adaptation of the gypsy moth to an unsuitable host plant

The pattern of adaptation with regard to life history traits and traits thought to be important in feeding habits of caterpillars in two populations of the gypsy moth (Lymantria dispar L.; Lepidoptera: Lymantriidae) originating from the locust tree (Robinia pseudoacacia; Fabaceae) and oak (Quercus petrea; Fagaceae) forests were investigated in the laboratory. The Robinia population has experienced unsuitable locust tree leaves as an exclusive food resource for more than 40 years. Since Quercus species are the principal host plants of the gypsy moth, the specific objectives of this study have been to measure the extent of differentiation between ancestral and derived populations in several life history traits (egg-to-adult viability, duration of larval and pupal stages, and pupal weight) and nutritional indices – relative growth rate (RGR), relative consumption rate (RCR), assimilation efficiency (AD), gross growth efficiency (ECI), and net growth efficiency (ECD). Significant differences between the Quercus and Robinia populations were detected in pupal duration, RGR, RCR, and AD. The presence of a significant population × host interaction in traits such as preadult viability, duration of pupal stage, RGR, and ECI suggests that adaptation of the gypsy moth to the unsuitable host might be ongoing. Using a full-sib design, we screened for genetic variation in life history traits within both populations, and examined the genetic correlations of performance across oak and locust leaves within both populations. The genetic variances for analyzed life history traits were lower under conditions that are commonly encountered in nature. Our data show that positive cross-host genetic correlations preponderate within both populations.     

The role of continental shelf width in determining freshwater phylogeographic patterns in south‐eastern Australian pygmy perches (Teleostei: Percichthyidae)

Biogeographic patterns displayed by obligate freshwater organisms are intimately related to the nature and extent of connectivity between suitable habitats. Two of the more significant barriers to freshwater connections are seawater and major drainage divides. South‐eastern Australia provides a contrast between these barriers as it has discrete areas that are likely influenced to a greater or lesser extent by each barrier type. We use continental shelf width as a proxy for the potential degree of river coalescence during low sea levels. Our specific hypothesis is that the degree of phylogeographic divergence between coastal river basins should correspond to the continental shelf width of each region. This predicts that genetic divergences between river basins should be lowest in regions with a wider continental shelf and that regions with similar continental shelf width should have similar genetic divergences. Pygmy perches (Nannoperca australis and Nannoperca ‘flindersi’) in south‐eastern Australia provide an ideal opportunity to test these biogeographic hypotheses. Phylogeographic patterns were examined based on range‐wide sampling of 82 populations for cytochrome b and 23 polymorphic allozyme loci. Our results recovered only limited support for our continental shelf width hypothesis, although patterns within Bass clade were largely congruent with reconstructed low sea‐level drainage patterns. In addition, we identified several instances of drainage divide crossings, typically associated with low elevational differences. Our results demonstrate high levels of genetic heterogeneity with important conservation implications, especially for declining populations in the Murray–Darling Basin and a highly restricted disjunct population in Ansons River, Tasmania.     

Genetic differentiation of the pine processionary moth at the southern edge of its range: contrasting patterns between mitochondrial and nuclear markers

The pine processionary moth (Thaumetopoea pityocampa) is an important pest of coniferous forests at the southern edge of its range in Maghreb. Based on mitochondrial markers, a strong genetic differentiation was previously found in this species between western (pityocampa clade) and eastern Maghreb populations (ENA clade), with the contact zone between the clades located in Algeria. We focused on the moth range in Algeria, using both mitochondrial (a 648 bp fragment of the tRNA‐cox2) and nuclear (11 microsatellite loci) markers. A further analysis using a shorter mtDNA fragment and the same microsatellite loci was carried out on a transect in the contact zone between the mitochondrial clades. Mitochondrial diversity showed a strong geographical structure and a well‐defined contact zone between the two clades. In particular, in the pityocampa clade, two inner subclades were found whereas ENA did not show any further structure. Microsatellite analysis outlined a different pattern of differentiation, with two main groups not overlapping with the mitochondrial clades. The inconsistency between mitochondrial and nuclear markers is probably explained by sex‐biased dispersal and recent afforestation efforts that have bridged isolated populations.     

Environmental gradients shape the genetic structure of two medicinal Salvia species in Jordan

• Environmental gradients, and particularly climatic variables, exert a strong influence on plant distribution and, potentially, population genetic diversity and differentiation. Differences in water availability can cause among‐population variation in ecological processes and can thus interrupt populations’ connectivity and isolate them environmentally. The present study examines the effect of environmental heterogeneity on plant populations due to environmental isolation unrelated to geographic distance.
• Using AFLP markers, we analyzed genetic diversity and differentiation among 12 Salvia spinosa populations and 13 Salvia syriaca populations from three phytogeographical regions (Mediterranean, Irano‐Turanian and Saharo‐Arabian) representing the extent of the species’ geographic range in Jordan. Differences in geographic location and climate were considered in the analyses.
• For both species, flowering phenology varied among populations and regions. Irano‐Turanian and Saharo‐Arabian populations had higher genetic diversity than Mediterranean populations, and genetic diversity increased significantly with increasing temperature. Genetic diversity in Salvia syriaca was affected by population size, while genetic diversity responded to drought in S. spinosa. For both species, high levels of genetic differentiation were found as well as two well‐supported phytogeographical groups of populations, with Mediterranean populations clustering in one group and the Irano‐Turanian and Saharo‐Arabian populations in another. Genetic distance was significantly correlated to environmental distance, but not to geographic distance.
• Our data indicate that populations from moist vs. arid environments are environmentally isolated, where environmental gradients affect their flowering phenology, limit gene flow and shape their genetic structure. We conclude that environmental heterogeneity may act as driver for the observed variation in genetic diversity.

     

Evolutionary genomics of gypsy moth populations sampled along a latitudinal gradient

The European gypsy moth (Lymantria dispar L.) was first introduced to Massachusetts in 1869 and within 150 years has spread throughout eastern North America. This large‐scale invasion across a heterogeneous landscape allows examination of the genetic signatures of adaptation potentially associated with rapid geographical spread. We tested the hypothesis that spatially divergent natural selection has driven observed changes in three developmental traits that were measured in a common garden for 165 adult moths sampled from six populations across a latitudinal gradient covering the entirety of the range. We generated genotype data for 91,468 single nucleotide polymorphisms based on double digest restriction‐site associated DNA sequencing and used these data to discover genome‐wide associations for each trait, as well as to test for signatures of selection on the discovered architectures. Genetic structure across the introduced range of gypsy moth was low in magnitude (F_ST = 0.069), with signatures of bottlenecks and spatial expansion apparent in the rare portion of the allele frequency spectrum. Results from applications of Bayesian sparse linear mixed models were consistent with the presumed polygenic architectures of each trait. Further analyses indicated spatially divergent natural selection acting on larval development time and pupal mass, with the linkage disequilibrium component of this test acting as the main driver of observed patterns. The populations most important for these signals were two range‐edge populations established less than 30 generations ago. We discuss the importance of rapid polygenic adaptation to the ability of non‐native species to invade novel environments.     

Phenological responses and a comparative phylogenetic insight of Anarsia lineatella and Grapholita molesta between distinct geographical regions within the Mediterranean basin

A unique logistic model for predicting population dynamics of Anarsia lineatella and Grapholita molesta was evaluated on populations sampled from Italy and Greece. Intraspecific mtDNA divergence was additionally estimated in an effort to examine whether regional differences in moth phenologies are associated with genetic divergence. A. lineatella populations displayed closer similarities on phenological responses between the two observation regions. As a result, population fluctuations in both regions could be accurately predicted based on the constructed model. However, that was not the case for G. molesta as its populations exhibited a more regional behaviour, and thus, the model was less accurate. It is notable that degree‐day accumulations above the lower temperature thresholds were recorded in Italy on month earlier than in Greece (1st March in Calabria in contrast to 1st April in Veria). That kind of observed deviations in moth phenologies could be potentially attributed to regional environmental conditions or even genetic differentiation. Despite the low number of individuals analysed, this first attempt to study the levels of intraspecific divergence between Italian and Greek moth populations revealed that both species exhibit evidence of regional‐based separation. Our study provides the first comprehensive phenological comparison between populations of A. lineatella and G. molesta from Italy and Greece. At the same time, the population genetic structure data reveal differentiation between these two regions for both species, something that should be further investigated as it could provide a possible explanation for the observed phenological differences. Moreover, DNA barcoding confirmed that G. molesta pheromone blends attracted at least two morphologically close‐related tortricid moth species. This fact probably explains the phenological variations observed for this species as well as the difficulties in defining the number of non‐overlapping flights.     

Underestimated mitochondrial diversity in gypsy moth Lymantria dispar from Asia

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Genetic variation and population structure in native Americans

We examined genetic diversity and population structure in the American landmass using 678 autosomal microsatellite markers genotyped in 422 individuals representing 24 Native American populations sampled from North, Central, and South America. These data were analyzed jointly with similar data available in 54 other indigenous populations worldwide, including an additional five Native American groups. The Native American populations have lower genetic diversity and greater differentiation than populations from other continental regions. We observe gradients both of decreasing genetic diversity as a function of geographic distance from the Bering Strait and of decreasing genetic similarity to Siberians--signals of the southward dispersal of human populations from the northwestern tip of the Americas. We also observe evidence of: (1) a higher level of diversity and lower level of population structure in western South America compared to eastern South America, (2) a relative lack of differentiation between Mesoamerican and Andean populations, (3) a scenario in which coastal routes were easier for migrating peoples to traverse in comparison with inland routes, and (4) a partial agreement on a local scale between genetic similarity and the linguistic classification of populations. These findings offer new insights into the process of population dispersal and differentiation during the peopling of the Americas.     

Risk assessment of the gypsy moth, <Emphasis Type="Italic">Lymantria dispar</Emphasis> (L), in New Zealand based on phenology modelling

The gypsy moth is a global pest that has not yet established in New Zealand despite individual moths having been discovered near ports. A climate-driven phenology model previously used in North America was applied to New Zealand. Weather and elevation data were used as inputs to predict where sustainable populations could potentially exist and predict the timing of hatch and oviposition in different regions. Results for New Zealand were compared with those in the Canadian Maritimes (New Brunswick, Nova Scotia, and Prince Edward Island) where the gypsy moth has long been established. Model results agree with the current distribution of the gypsy moth in the Canadian Maritimes and predict that the majority of New Zealand’s North Island and the northern coastal regions of the South Island have a suitable climate to allow stable seasonality of the gypsy moth. New Zealand’s climate appears more forgiving than that of the Canadian Maritimes, as the model predicts a wider range of oviposition dates leading to stable seasonality. Furthermore, we investigated the effect of climate change on the predicted potential distribution for New Zealand. Climate change scenarios show an increase in probability of establishment throughout New Zealand, most noticeably in the South Island.     

Long-distance dispersal of the gypsy moth (Lepidoptera: Lymantriidae) facilitated its initial invasion of Wisconsin

Gypsy moth (Lymantria dispar L.) spread is dominated by stratified dispersal, and, although spread rates are variable in space and time, the gypsy moth has invaded Wisconsin at a consistently higher rate than in other regions. Allee effects, which act on low-density populations ahead of the moving population that contribute to gypsy moth spread, have also been observed to be consistently weaker in Wisconsin. Because a major cause of an Allee effect in the gypsy moth is mate-finding failure at low densities, supplementing low-density populations with immigrants that arrive through dispersal may facilitate establishment and consequent spread. We used local indicator of spatial autocorrelation methods to examine space-time gypsy moth monitoring data from 1996 to 2006 and identify isolated, low-density colonies that arrived through dispersal. We measured the distance of these colonies from the moving population front to show that long-distance dispersal was markedly present in earlier years when Wisconsin was still mainly uninfested. Recently, however, immigrants arriving through long-distance dispersal may no longer be detected because instead of invading uninfested areas, they are now supplementing high-density colonies. In contrast, we observed no temporal pattern in the distance between low-density colonies and the population front in West Virginia and Virginia. We submit that long-distance dispersal, perhaps facilitated through meteorological mechanisms, played an important role in the spread dynamics of the initial Wisconsin gypsy moth invasion, but it currently plays a lesser role because the portion of Wisconsin most susceptible to long-distance immigrants from alternate sources is now heavily infested.     

Interpopulation quality in gypsy moths with implications for success of two pupal parasitoids: Brachymeria intermedia (Nees) and Coccygomimus turionellae (L.)*

Abstract.

• 1 Gypsy moth egg masses were collected from innocuous, release and outbreak populations and reared in the laboratory on synthetic diet under identical conditions.
• 2 Outbreak population gypsy moths hatched sooner, were smaller and less fecund than innocuous or release gypsy moths, but had a higher concentration of total carbohydrates in their haemolymph.
• 3 Pupae from each population source were submitted to parasitization by two pupal parasitoids. Emerging B.intermedia, an established parasitoid of the gypsy moth associated with outbreak populations, were largest on outbreak source gypsy moths. C. turionellae, not a usual parasitoid of the gypsy moth, were largest when emerging from innocuous or release population gypsy moths. Implications for population dynamics of the gypsy moth are discussed.

     

Elevational gradient in the cyclicity of a forest-defoliating insect

Observed changes in the cyclicity of herbivore populations along latitudinal gradients and the hypothesis that shifts in the importance of generalist versus specialist predators explain such gradients has long been a matter of intense interest. In contrast, elevational gradients in population cyclicity are largely unexplored. We quantified the cyclicity of gypsy moth populations along an elevational gradient by applying wavelet analysis to spatially referenced 31-year records (1975–2005) of defoliation. Based on geographically weighted regression and nonlinear regression, we found either a hump-shaped or plateauing relationship between elevation and the cyclicity of gypsy moth populations and a positive relationship between cyclicity and the density of the gypsy moth’s preferred host-tree species. The potential effects of elevational gradients in the density of generalist predators and preferred host-tree species on the cyclicity of gypsy moth populations were evaluated with mechanistic simulation models. The models suggested that an elevational gradient in the densities of preferred host tree species could partially explain elevational patterns of gypsy moth cyclicity. Results from a model assuming a type-III functional response of generalist predators to changes in gypsy moth density were inconsistent with the observed elevational gradient in gypsy moth cyclicity. However, a model with a more realistic type-II functional response gave results roughly consistent with the empirical findings. In contrast to classical studies on the effects of generalist predators on prey population cycles, our model with a type-II functional response predicts a unimodal relationship between generalist-predator density and the cyclicity of gypsy moth populations.     

Rapid identification of the Asian gypsy moth and its related species based on mitochondrial DNA

The gypsy moth—Lymantria dispar (Linnaeus)—is a worldwide forest defoliator and is of two types: the European gypsy moth and the Asian gypsy moth. Because of multiple invasions of the Asian gypsy moth, the North American Plant Protection Organization officially approved Regional Standards for Phytosanitary Measures No. 33. Accordingly, special quarantine measures have been implemented for 30 special focused ports in the epidemic areas of the Asian gypsy moth, including China, which has imposed great inconvenience on export trade. The Asian gypsy moth and its related species (i.e., Lymantria monocha and Lymantria xylina) intercepted at ports are usually at different life stages, making their identification difficult. Furthermore, Port quarantine requires speedy clearance. As such, it is difficult to identify the Asian gypsy moth and its related species only by their morphological characteristics in a speedy measure. Therefore, this study aimed to use molecular biology technology to rapidly identify the Asian gypsy moth and its related species based on the consistency of mitochondrial DNA in different life stages. We designed 10 pairs of specific primers from different fragments of the Asian gypsy moth and its related species, and their detection sensitivity met the need for rapid identification. In addition, we determined the optimal polymerase chain reaction amplification temperature of the 10 pairs of specific primers, including three pairs of specific primers for the Asian gypsy moth (L. dispar asiatic), four pairs of specific primers for the nun moth (L. monocha), and three pairs of specific primers for the casuarina moth (L. xylina). In conclusion, using our designed primers, direct rapid identification of the Asian gypsy moth and its related species is possible, and this advancement can help improve export trade in China.     

Going coastal: shared evolutionary history between coastal British Columbia and Southeast Alaska wolves (Canis lupus)

Background

Many coastal species occupying the temperate rainforests of the Pacific Northwest in North America comprise endemic populations genetically and ecologically distinct from interior continental conspecifics. Morphological variation previously identified among wolf populations resulted in recognition of multiple subspecies of wolves in the Pacific Northwest. Recently, separate genetic studies have identified diverged populations of wolves in coastal British Columbia and coastal Southeast Alaska, providing support for hypotheses of distinct coastal subspecies. These two regions are geographically and ecologically contiguous, however, there is no comprehensive analysis across all wolf populations in this coastal rainforest.

Methodology/Principal Findings

By combining mitochondrial DNA datasets from throughout the Pacific Northwest, we examined the genetic relationship between coastal British Columbia and Southeast Alaska wolf populations and compared them with adjacent continental populations. Phylogenetic analysis indicates complete overlap in the genetic diversity of coastal British Columbia and Southeast Alaska wolves, but these populations are distinct from interior continental wolves. Analyses of molecular variation support the separation of all coastal wolves in a group divergent from continental populations, as predicted based on hypothesized subspecies designations. Two novel haplotypes also were uncovered in a newly assayed continental population of interior Alaska wolves.

Conclusions/Significance

We found evidence that coastal wolves endemic to these temperate rainforests are diverged from neighbouring, interior continental wolves; a finding that necessitates new international strategies associated with the management of this species.     

Large‐scale adaptive divergence in Boechera fecunda,an endangered wild relative of Arabidopsis

Many biological species are threatened with extinction because of a number of factors such as climate change and habitat loss, and their preservation depends on an accurate understanding of the extent of their genetic variability within and among populations. In this study, we assessed the genetic divergence of five quantitative traits in 10 populations of an endangered cruciferous species, Boechera fecunda, found in only several populations in each of two geographic regions (WEST and EAST) in southwestern Montana. We analyzed variation in quantitative traits, neutral molecular markers, and environmental factors and provided evidence that despite the restricted geographical distribution of this species, it exhibits a high level of genetic variation and regional adaptation. Conservation efforts therefore should be directed to the preservation of populations in each of these two regions without attempting transplantation between regions. Heritabilities and genetic coefficients of variation estimated from nested ANOVAs were generally high for leaf and rosette traits, although lower (and not significantly different from 0) for water‐use efficiency. Measures of quantitative genetic differentiation, Q_ST, were calculated for each trait from each pair of populations. For three of the five traits, these values were significantly higher between regions compared with those within regions (after adjustment for neutral genetic variation, F_ST). This suggested that natural selection has played an important role in producing regional divergence in this species. Our analysis also revealed that the B. fecunda populations appear to be locally adapted due, at least in part, to differences in environmental conditions in the EAST and WEST regions.