Landscape-scale population connectivity in two parasitoid species associated with the spruce budworm: Testing the birdfeeder effect using genetic data.

Periodic and spatially synchronous outbreaks of insect pests have dramatic consequences for boreal and sub-boreal forests. Within these multitrophic systems, parasitoids can be stabilizing agents by dispersing toward patches containing higher host density (the so-called birdfeeder effect). However, we know little about the dispersal abilities of parasitoids in continuous forested landscapes, limiting our understanding of the spatiotemporal dynamics of host-parasitoid systems, and constraining our ability to predict forest resilience in the context of global changes. In this study, we investigate the spatial genetic structure and spatial variation in genetic diversity of two important species of spruce budworm larval parasitoids during outbreaks: Apanteles fumiferanae Viereck (Braconidae) and Glypta fumiferanae (Viereck) (Ichneumonidae). Using parasitoids sampled in 2014 from 26 and 29 locations across a study area of 350,000 km2 , we identified 1,012 and 992 neutral SNP loci for A. fumiferanae (N = 279 individuals) and G. fumiferanae (N = 382), respectively. Using DAPC, PCA, AMOVA, and IBD analyses, we found evidence for panmixia and high genetic connectivity for both species, matching the previously described genetic structure of the spruce budworm within the same context, suggesting similar effective dispersal during outbreaks and high parasitoid population densities between outbreaks. We also found a significant negative relationship between genetic diversity and latitude for A. fumiferanae but not for G. fumiferanae, suggesting that northern range limits may vary by species within the spruce budworm parasitoid community. These spatial dynamics should be considered when predicting future insect outbreak severities in boreal landscapes.

The role of dispersal, selection, and timing of sampling on the false discovery rate of loci under selection during geographic range expansion.

Identifying adaptive loci is important to understand the evolutionary potential of species undergoing range expansion. However, in expanding populations, spatial demographic processes such as allele surfing can create spatial patterns of neutral genetic variation that appear similar to those generated through adaptive processes. As a result, the false discovery rate of adaptive loci may be inflated in landscape genomic analyses. Here, we take a simulation modelling approach to investigate how range expansion affects our ability to correctly distinguish between neutral and adaptive genetic variation, using the mountain pine beetle outbreak system as a motivating example. We simulated the demographic and population genetic dynamics of populations undergoing range expansion using an individual-based genetic model CDMetaPOP. We investigated how the false discovery rate of adaptive loci is affected by (i) dispersal capacity, (ii) timing of sampling, and (iii) the strength of selection on an adaptive reference locus. We found that a combination of weak dispersal, weak selection, and early sampling presents the greatest risk of misidentifying loci under selection. Expanding populations present unique challenges to the reliable identification of adaptive loci. We demonstrate that there is a need for further methodological development to account for directional demographic processes in landscape genomics.

Quantifying uncertainty in inferences of landscape genetic resistance due to choice of individual-based genetic distance metric.

Estimates of gene flow resulting from landscape resistance inferences frequently inform conservation management decision-making processes. Therefore, results must be robust across approaches and reflect real-world gene flow instead of methodological artefacts. Here, we tested the impact of 32 individual-based genetic distance metrics on the robustness and accuracy of landscape resistance modelling results. We analysed three empirical microsatellite datasets and 36 simulated datasets that varied in landscape resistance and genetic spatial autocorrelation. We used ResistanceGA to generate optimised multi-feature resistance surfaces for each of these datasets using 32 different genetic distance metrics. Results of the empirical dataset demonstrated that the choice of genetic distance metric can have strong impacts on inferred optimised resistance surfaces. Simulations showed accurate parametrisation of resistance surfaces across most genetic distance metrics only when a small number of environmental features was impacting gene flow. Landscape scenarios with many features impacting gene flow led to a generally poor recovery of true resistance surfaces. Simulation results also emphasise that choosing a genetic distance metric should not be based on marginal R2 -based model fit. Until more robust methods are available, resistance surfaces can be optimised with different genetic distance metrics and the convergence of results needs to be assessed via pairwise matrix correlations. Based on the results presented here, high correlation coefficients across different genetic distance categories likely indicate accurate inference of true landscape resistance. Most importantly, empirical results should be interpreted with great caution, especially when they appear counter-intuitive in light of the ecology of a species.

Quantifying and predicting population connectivity of an outbreaking forest insect pest.

Context: Dispersal has a key role in the population dynamics of outbreaking species such as the spruce budworm (Choristoneura fumiferana) as it can synchronize the demography of distant populations and favor the transition from endemic to epidemic states. However, we know very little about how landscape structure influences dispersal in such systems while such knowledge is essential for better forecasting of spatially synchronous population dynamics and to guide management strategies. Objectives: We aimed to characterize the spatial environmental determinants of spruce budworm dispersal to determine how these features affect outbreak spread in Quebec (Canada). We then apply our findings to predict expected future landscape connectivity and explore its potential consequences on future outbreaks. Methods: We used a machine-learning landscape genetics approach on 447 larvae covering most of the outbreak area and genotyped at 3562 SNP loci to identify the main variables affecting connectivity. Results: We found that the connectivity between outbreak populations was driven by the combination of precipitation and host cover. Our forecasting suggests that between the current and next outbreaks, connectivity may increase between Ontario and Quebec, and might decrease in the eastern part, which could have the effect of limiting outbreak spread from Ontario and Quebec to the eastern provinces. Conclusions: Although we did not identify any discrete barriers, low connectivity areas might constrain dispersal in the current and future outbreaks and should in turn, be intensively monitored. However, continued sampling as the outbreak progresses is needed to confirm the temporal stability of the observed patterns. Supplementary Information: The online version contains supplementary material available at 10.1007/s10980-021-01382-9.

Interactions of cranial helminths in the European polecat (Mustela putorius): Implications for host body condition.

Multiple helminth species commonly co-occur within mammals and their interactions may negatively affect the survival and breeding success of their hosts. However, it has been difficult to prove competition or mutualism between co-infesting helminths in field studies of wild mammals. The sinus cavities of European polecats (Mustela putorius) can be parasitised by the trematode Troglotrema acutum and the nematode Skrjabingylus nasicola and both helminths can co-occur within hosts. While both parasites can damage the host's bone structure and cause severe pathologies, their impact on host body condition is unclear. It is also unknown whether both parasites interact and how this might affect cranial damage and host body condition. We examined 515 fresh polecat skulls for the presence of both helminths and measured the hosts' amount of kidney perirenal fat as a measure of body condition. Our results demonstrated that, in addition to a host-intrinsic fixed factor (sex) and random factors accounting for spatial and temporal stochasticity, the helminths influenced each other's presence. Infestation with T. acutum increased the probability of catching S. nasicola with increasing age of the host, while males already infested with S. nasicola were more likely to become infested with T. acutum than females infested with the nematode. While we speculate that both effects resulted from parasite-induced behavioural alterations (increased foot consumption), it is not clear why, in the latter case, this effect would be stronger in males than females. We showed that the abundances of both parasites had significant positive effect on the likely presence of skull damage and a significant negative effect on the predicted presence of kidney fat. Given the evolutionary arms race that both host-parasite systems have undergone, it appears unlikely that either helminth played a significant factor in the population decline of the polecat in Europe.

Community-level modelling of boreal forest mammal distribution in an oil sands landscape.

Anthropogenic landscape disturbances are known to alter, destroy, and fragment habitat, which typically leads to biodiversity loss. The effects of landscape disturbance generally vary among species and depend on the nature of the disturbances, which may interact and result in synergistic effects. Western Canada's oil sands region experiences disturbances from forestry and energy sector activities as well as municipal and transportation infrastructure. The effects of those disturbances on single species have been studied and have been implicated in declines of the boreal woodland caribou (Rangifer tarandus caribou). Yet, the specific responses of the mammal community, and of functional groups such as prey and predators, to those interacting disturbances are still poorly known. We investigated the responses of black bear, grey wolf, coyote, fisher, lynx, red fox, American red squirrel, white-tailed deer, moose, caribou, and snowshoe hare to both natural habitat and disturbance associated with anthropogenic features within Alberta's northeast boreal forest. We used a novel community-level modelling framework on three years of camera-trap data collected in an oil sands landscape. This framework allowed us to identify the natural and anthropogenic features which explained the most variation in occurrence frequency among functional groups, as well as compare responses to linear and non-linear anthropogenic disturbance. Occurrence frequency by predators was better explained by anthropogenic features than by natural habitat. Both linear and non-linear anthropogenic features helped explain occurrence frequency by prey and predators, although the effects differed in magnitude and spatial scale. To better conserve boreal biodiversity, management actions should extend beyond a focus on caribou and wolves and aim to restore habitat across a diversity of anthropogenic disturbances and monitor the dynamics of the entire mammal community.

Inferring responses to climate warming from latitudinal pattern of clonal hybridization.

Climate warming may affect reproductive isolation between sympatric sister species by modifying reproductive phenology or mate choice. This is expected to result in a latitudinal progression of hybridization in response to the shifting of environmental conditions. The fish species northern redbelly dace (Chrosomus eos) and finescale dace (C. neogaeus) display a wide sympatric distribution in North America. The asexual reproduction of their hybrids allows determining where and when hybridization occurred. The aim of this study was twofold: first, to assess whether temperature affected reproductive isolation, and second, whether the effects of climate warming resulted in a latitudinal progression of hybridization. We performed a 500 km latitudinal survey (51 sites) in southeastern Quebec (Canada) and determined the distribution of clonal hybrid lineages. Results revealed a total of 78 hybrid lineages, including 70 which originated locally. We detected a significant difference between the southern and northern range of the survey in terms of the proportion of sites harboring local hybrids (20/23 vs. 8/28 sites, respectively) and hybrid diversity (57 vs. 13 lineages, respectively). This confirmed that there was more frequent interspecific mating in the warmest sites. In the southern range, diversity of lineages and simulations suggest that hybridization first took place (>7,000 years) in sites characterized by a longer growing season, followed by northerly adjacent sites (ca. 3,500-5,000 years). Moreover, evidence of hybridization occurring in present-day time was detected. This suggests that the current warming episode is going beyond the limits of the previous warmest period of the Holocene.