Phenotypic divergence in reproductive traits of a moth population experiencing a phenological shift

Allochrony that is reproductive isolation by time may further lead to divergence of reproductive adaptive traits in response to different environmental pressures over time. A unique “summer” population of the pine processionary moth Thaumetopoea pityocampa, reproductively isolated from the typical winter populations by allochronic differentiation, is here analyzed. This allochronically shifted population reproduces in the spring and develops in the summer, whereas “winter” populations reproduce in the late summer and have winter larval development. Both summer and winter populations coexist in the same pine stands, yet they face different climatic pressures as their active stages are present in different seasons. The occurrence of significant differences between the reproductive traits of the summer population and the typical winter populations (either sympatric or allopatric) is thus hypothesized. Female fecundity, egg size, egg covering, and egg parasitism were analyzed showing that the egg load was lower and that egg size was higher in the summer population than in all the studied winter populations. The scales that cover the egg batches of T. pityocampa differed significantly between populations in shape and color, resulting in a looser and darker covering in the summer population. The single specialist egg parasitoid species of this moth was almost missing in the summer population, and the overall parasitism rates were lower than in the winter population. Results suggest the occurrence of phenotypic differentiation between the summer population and the typical T. pityocampa winter populations for the life‐history traits studied. This work provides an insight into how ecological divergence may follow the process of allochronic reproductive isolation.     

The relationship between pheromone trap catch and local population density of the oak processionary moth Thaumetopoea processionea (Lepidoptera: Thaumetopoeidae)

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Genetic differentiation in the winter pine processionary moth (Thaumetopoea pityocampa--wilkinsoni complex), inferred by AFLP and mitochondrial DNA markers

The winter pine processionary moth has become an important pine pest in the last century, as a consequence of the spread of pine cultivation in the Mediterranean region. The pattern of genetic differentiation of this group, that includes two sibling species (Thaumetopoea pityocampa and Th. wilkinsoni), has been studied in nine populations using amplified fragment length polymorphism (AFLP) and single strand conformation polymorphism-sequence analysis (SSCP) of the mitochondrial cytochrome oxidase 1 (COI) and cytochrome oxydase 2 (COII). Results indicate the existence of strong genetic differentiation between the two species that became separated before the Quaternary ice ages. Moreover data indicate that Th. pityocampa has a strong geographical structure, particularly evident at the nuclear level, where all pairwise phiST resulted to be highly significant and individuals from the same population resulted to be strongly clustered when an individual tree was reconstructed. The estimates of the absolute number of migrants between populations (Nm), obtained from mitochondrial and nuclear DNA markers, suggest that gene flow is low and that a gender-related dispersal could occur in this species. The males appear to disperse more than females, contributing to the genetic diversity of populations on a relatively wide range, reducing the risks of inbreeding and the genetic loss associated with bottlenecks occurring in isolated populations.     

The role of topography in structuring the demographic history of the pine processionary moth,Thaumetopoea pityocampa (Lepidoptera: Notodontidae)

Aim We investigated the Quaternary history of the pine processionary moth, Thaumetopoea pityocampa, an oligophagous insect currently expanding its range. We tested the potential role played by mountain ranges during the post‐glacial recolonization of western Europe. Location Western Europe, with a focus on the Pyrenees, Massif Central and western Alps. Methods Maternal genetic structure was investigated using a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene. We analysed 412 individuals from 61 locations and performed maximum likelihood and maximum parsimony phylogenetic analyses and hierarchical analysis of molecular variance, and we investigated signs of past expansion. Results A strong phylogeographic pattern was found, with two deeply divergent clades. Surprisingly, these clades were not separated by the Pyrenees but rather were distributed from western to central Iberia and from eastern Iberia to the Italian Peninsula, respectively. This latter group consisted of three shallowly divergent lineages that exhibited strong geographic structure and independent population expansions. The three identified lineages occurred: (1) on both sides of the Pyrenean range, with more genetically diverse populations in the east, (2) from eastern Iberia to western France, with a higher genetic diversity in the south, and (3) from the western Massif Central to Italy. Admixture areas were found at the foot of the Pyrenees and Massif Central. Main conclusions The identified genetic lineages were geographically structured, but surprisingly the unsuitable high‐elevation areas of the main mountainous ranges were not responsible for the spatial separation of genetic groups. Rather than acting as barriers to dispersal, mountains appear to have served as refugia during the Pleistocene glaciations, and current distributions largely reflect expansion from these bottlenecked refugial populations. The western and central Iberian clade did not contribute to the northward post‐glacial recolonization of Europe, yet its northern limit does not correspond to the Pyrenees. The different contributions of the identified refugia to post‐glacial expansion might be explained by differences in host plant species richness. For example, the Pyrenean lineage could have been trapped elevationally by tracking montane pines, while the eastern Iberian lineage could have expanded latitudinally by tracking thermophilic lowland pine species.     

Temperature as a predictor of survival of the pine processionary moth in the Italian Alps

1 The pine processionary moth Thaumetopoea pityocampa is expanding its geographical range in Europe, as a consequence of enhanced winter survival under a warmer climate. A combination of daytime nest temperatures and night air temperatures determines the number of hours larvae are able to feed (hours above realized feeding threshold, RFT). 2 We tested the RFT‐based model for survival across multiple areas of the insect’s range in the Italian Alps over a 2‐year period. In a series of translocation experiments using natural temperature gradients as spatial analogues for global warming, we transferred colonies of T. pityocampa larvae to sites within zones of historical distribution, recent distribution, and outside the present range. The sites included traditional (Pinus nigra, Pinus sylvestris) as well as novel (Pinus mugo, Pinus uncinata, Pinus cembra) hosts. 3 Survival during precold (August to November), cold (December to February) and postcold (March to May) periods were analysed against climatic variables (temperature and rainfall) and predictors developed by the model. 4 Host species did not significantly affect final survival, with the exception of slower larval development, and resulting lower cold tolerance, on P. cembra than on P. mugo at the same site. 5 Across all the sites and hosts, final survival of colonies depended on the number of feeding hours during the cold period (RFT), which explained 82% of the variance in a regression model. We recommend using RFT, or its surrogate daily mean minimum temperature when nest temperature is not available, in predictive models of range expansion of T. pityocampa under climate change scenarios.     

Does landscape composition alter the spatiotemporal distribution of the pine processionary moth in a pine plantation forest?

Landscape composition and physiognomy affect community structure and species distribution across space and time. The pine processionary moth (PPM) (Thaumetopoea pityocampa Den. & Schiff., Lepidoptera, Notodontidae) is a common pine defoliator throughout southern Europe and Mediterranean countries. We surveyed the spatiotemporal distribution of the PPM in a pine plantation forest in southwestern France and used the density of the winter nests as a proxy for population density. The study spanned 4 years (2005–2008) and showed a high temporal variability in nest density. We found a strong edge effect with nest densities at stand edges more than twice as large as within-stand densities. At the landscape scale, the spatial distribution of the moth exhibited a significant spatial autocorrelation in 3 out of 4 years of our study. The spatial scales of the autocorrelation ranged from ca. 2 km to more than 22 km. We found a positive correlation between spatial distributions corresponding to certain sampling years, but the relationship was not systematic. Landscape configuration appeared to be an important driver of the PPM spatial pattern. Bivariate Moran’s I correlograms showed that patch richness density as well as the percentage of local landscape covered by various land uses were correlated with population density. The study showed that accounting for landscape characteristics may be important in order to understand forest insect pest distribution, even in cases where the host species is abundant and homogeneously distributed throughout the study area, e.g., pure plantation forests.     

Low temperature tolerance and starvation ability of the oak processionary moth: implications in a context of increasing epidemics

• 1 We investigated how modifications in winter and spring temperature conditions may affect the survival of a spring‐hatching Lepidoptera, the oak processionary moth Thaumetopoea processionea.
• 2 Supercooling and chilling injury experiments indicate that eggs are especially cold hardy at the start of the winter period, although this ability is reduced later in the season. In the spring, young larvae are sufficiently cold hardy to ensure no direct mortality as a result of late frosts.
• 3 A comparison of phenological models shows that neonate larvae may await the unfolding of new oak leaves for relatively long periods (e.g. 1–30 days). Under both low (4°C after 5 days at 16°C) and high temperature experimental scenarios (constant 16°C), the majority of neonate larvae can survive starvation for more than 2 weeks.
• 4 Larvae may also suffer from food depletion once their development has been initiated (e.g. during cold springs) if the threshold temperature for feeding is not reached for several consecutive days, or in the case of late frosts affecting foliage availability. When temperature is reduced to 4°C, developing larvae become inactive and do not feed anymore; their starvation survival capability is reduced to approximately 2 weeks (cold spring hypothesis). At 16°C, developing larvae that are deprived of food can only survive for 10 days (late frost hypothesis).
• 5 We conclude that, in the oak processionary moth, neonate larvae are relatively well adapted to early hatching relative to budburst, ensuring them the highest foliage quality for development. In some years, however, phenological asynchrony or cold spring conditions may affect the persistence of populations at the limits of the species' range.

     

Characterization of five microsatellite loci in the Pine Processionary Moth Thaumetopoea pityocampa (Lepidoptera Notodontidae Thaumetopoeinae)

Five microsatellite markers were developed for the lepidopteran species Thaumetopoea pityocampa using an enrichment protocol. All loci could be amplified with no evidence of null alleles and will be useful for population genetic studies. The number of alleles ranged from three to 12 for a population of 30 individuals. Observed heterozygosities ranged from 0.53 to 0.80. No significant heterozygote deficiency was detected. Four markers might be of interest for Th. wilkinsoni.     

Egg mortality in the cedar processionary moth,Thaumetopoea bonjeani (Lepidoptera: Notodontidae), in an outbreak area of Algeria

The cedar processionary moth, Thaumetopoea bonjeani (Lepidoptera: Notodontidae), is one of the most serious pests of Cedrus atlantica in north-western Africa (Algeria and Morocco). We report on T. bonjeani egg mortality and the diversity and abundance of parasitoids associated with its eggs in the area of Djurdjura Mountain (Tala-Guilef, Algeria). For this goal, 223 egg batches were collected from C. atlantica over two cohorts (2012 and 2013). The average number of eggs per egg batch increased from 143 in 2012 to 171 in 2013, while the egg mortality decreased from 47.4% and 23.9%, respectively, possibly because of a dilution effect. The most important factors of egg mortality were parasitoids and predators, with hymenopteran egg parasitoids killing from 12.1% to 34.9%, and predators from 5.2% to 7.4% of the eggs. The pattern of egg parasitism was driven largely by Ooencyrtus pityocampae, accounting for about 94% of the total parasitoids, followed by Baryscapus servadeii and Trichogramma embryophagum. An hyperparasitoid Chartocerus sp. was collected for the first time from eggs of Thaumetopoea species. As the two major egg parasitoids are shared with the pine processionary moth Thaumetopoea pityocampa in the same area, it is likely that parasitoid abundance may depend on the occurrence of both hosts.     

Modelling the effects of climate change on the potential feeding activity of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Notodontidae) in France

Aim We investigated whether climate change has affected the potential feeding activity of a winter active larva, the pine processionary moth (PPM), Thaumetopoea pityocampa L., and whether it may explain its range expansion. Location The study area is France and, at a smaller scale, the Paris Basin. Methods We used a statistical model derived from Huchon and Démolin [1970 Revue Forestière Française (special issue: La lutte biologique en forêt), 220–234] to test whether their model, updated with climate change, could explain the observed range expansion. Since Battisti and colleagues have recently shown that climate could affect survival of the PPM through its effect on feeding activity, we also developed a mechanistic model based on larval feeding requirements (night air temperature above 0 °C and temperature inside the nest above 9 °C on the preceding day). We reconstructed the geographical distribution of feeding activity and we compared the resulting change with the PPM range expansion. Results The statistical model did not successfully predict the observed expansion but the mechanistic model showed considerable change in the feeding activity of the PPM. In the Paris Basin, the PPM border coincided with a zone unfavourable for feeding activity in the period 1992–96. Feeding conditions became more favourable in the period 2001–04, and the PPM succeeded in crossing this zone. Over larger temporal and spatial scales improved feeding conditions in the north‐western part of France were forecast by the mechanistic model. Main conclusions (1) The range distribution of the PPM in the Paris Basin is no longer limited by unfavourable feeding conditions. (2) The pattern of range expansion of the PPM is now governed mainly by its dispersal capabilities and host tree distribution. (3) At the country scale, this approach gives an approximate prediction of the potential distribution of the PPM, though the model may not be reliable in mountainous regions.