Oak masting drivers vary between populations depending on their climatic environments.

Large interannual variation in seed production, called masting, is very common in wind-pollinated tree populations and has profound implications for the dynamics of forest ecosystems and the epidemiology of certain human diseases.1,2,3,4,5 Comparing the reproductive characteristics of populations established in climatically contrasting environments would provide powerful insight into masting mechanisms, but the required data are extremely scarce. We built a database from an unprecedented fine-scale 8-year survey of 150 sessile oak trees (Quercus petraea) from 15 populations distributed over a broad climatic gradient, including individual recordings of annual flowering effort, fruiting rate, and fruit production. Although oak masting was previously considered to depend mainly on fruiting rate variations,6,7 we show that the female flowering effort is highly variable from year to year and explains most of the fruiting dynamics in two-thirds of the populations. What drives masting was found to differ among populations living under various climates. In soft-climate populations, the fruiting rate increases initially strongly with the flowering effort, and the intensity of masting results mainly from the flowering synchrony level between individuals. By contrast, the fruiting rate of harsh-climate populations depends mainly on spring weather, which ensures intense masting regardless of the flowering synchronization level. Our work highlights the need for jointly measuring flowering effort and fruit production to decipher the diversity of masting mechanisms among populations. Accounting for such diversity will be decisive in proposing accurate, and possibly contrasted, scenarios about future reproductive patterns of perennial plants with ongoing climate change and their numerous cascading effects.

Age and spatio-temporal variations in food resources modulate stress-immunity relationships in three populations of wild roe deer.

Living in variable and unpredictable environments, organisms face recurrent stressful situations. The endocrine stress response, which includes the secretion of glucocorticoids, helps organisms to cope with these perturbations. Although short-term elevations of glucocorticoid levels are often associated with immediate beneficial consequences for individuals, long-term glucocorticoid elevation can compromise key physiological functions such as immunity. While laboratory works highlighted the immunosuppressive effect of long-term elevated glucocorticoids, it remains largely unknown, especially in wild animals, whether this relationship is modulated by individual and environmental characteristics. In this study, we explored the co-variation between integrated cortisol levels, assessed non-invasively using faecal cortisol metabolites (FCMs), and 12 constitutive indices of innate, inflammatory, and adaptive immune functions, in wild roe deer living in three populations with previously known contrasting environmental conditions. Using longitudinal data on 564 individuals, we further investigated whether age and spatio-temporal variations in the quantity and quality of food resources modulate the relationship between FCMs and immunity. Negative covariation with glucocorticoids was evident only for innate and inflammatory markers of immunity, while adaptive immunity appeared to be positively or not linked to glucocorticoids. In addition, the negative covariations were generally stronger in individuals facing harsh environmental constraints and in old individuals. Therefore, our results highlight the importance of measuring multiple immune markers of immunity in individuals from contrasted environments to unravel the complex relationships between glucocorticoids and immunity in wild animals. Our results also help explain conflicting results found in the literature and could improve our understanding of the link between elevated glucocorticoid levels and disease spread, and its consequences on population dynamics.

DNA methylation as a tool to explore ageing in wild roe deer populations.

DNA methylation-based biomarkers of ageing (epigenetic clocks) promise to lead to new insights into evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic ageing effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual roe deer (Capreolus capreolus) living in two wild populations (Chizé and Trois-Fontaines, France) facing different ecological contexts, to investigate the relationship between chronological age and levels of DNA methylation (DNAm). We generated novel DNA methylation data from n = 94 blood samples, from which we extracted leucocyte DNA, using a custom methylation array (HorvathMammalMethylChip40). We present three DNA methylation-based estimators of age (DNAm or epigenetic age), which were trained in males, females, and both sexes combined. We investigated how sex differences influenced the relationship between DNAm age and chronological age using sex-specific epigenetic clocks. Our results highlight that old females may display a lower degree of biological ageing than males. Further, we identify the main sites of epigenetic alteration that have distinct ageing patterns between the two sexes. These findings open the door to promising avenues of research at the crossroads of evolutionary biology and biogerontology.

Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes.

BACKGROUND: Gastrointestinal nematodes are ubiquitous for both domestic and wild ungulates and have varying consequences for health and fitness. They exist as complex communities of multiple co-infecting species, and we have a limited understanding of how these communities vary in different hosts, regions and circumstances or of how this affects their impacts. METHODS: We have undertaken ITS2 rDNA nemabiome metabarcoding with next-generation sequencing on populations of nematode larvae isolated from 149 fecal samples of roe deer of different sex and age classes in the two isolated populations of Chizé and Trois Fontaines in France not co-grazing with any domestic ungulate species. RESULTS: We identified 100 amplified sequence variants (ASVs) that were assigned to 14 gastrointestinal nematode taxa overall at either genus (29%) or species (71%) level. These taxa were dominated by parasites classically found in cervids-e.g. Ostertagia leptospicularis, Spiculopteragia spp. Higher parasite species diversity was present in the Trois Fontaines population than in the Chizé population including the presence of species more typically seen in domestic livestock (Haemonchus contortus, Bunostomum sp., Cooperia punctata, Teladorsagia circumcincta). No differences in parasite species diversity or community composition were seen in the samples collected from three zones of differing habitat quality within the Chizé study area. Young roe deer hosted the highest diversity of gastrointestinal nematodes, with more pronounced effects of age apparent in Trois Fontaines. The effect of host age differed between gastrointestinal nematode species, e.g. there was little effect on O. leptospicularis but a large effect on Trichostrongylus spp. No effect of host sex was detected in either site. CONCLUSIONS: The presence of some livestock parasite species in the Trois Fontaines roe deer population was unexpected given the isolation of this population away from grazing domestic livestock since decades. Overall, our results illustrate the influence of host traits and the local environment on roe deer nemabiome and demonstrate the power of the nemabiome metabarcoding approach to elucidate the composition of gastrointestinal nematode communities in wildlife.

Detection and monitoring of Drosophila suzukii in raspberry and cherry orchards with volatile organic compounds in the USA and Europe.

Spotted wing drosophila (SWD) causes significant economic loss in fruit crops to growers worldwide. There is immediate need for efficacious and selective monitoring tools that can detect infestations early. Previously, volatile organic compounds derived from apple were studied and a quinary chemical component blend (QB) was identified as the key SWD attractant in a blueberry orchard in the United States. This study's aim was to determine whether previously observed QB efficacy, selectivity, and early detection levels could be attained within raspberry and cherry fields in the USA and Europe. Results demonstrated that sticky trap baited QB dispenser provided earlier SWD detection potential than the usually adopted apple cider vinegar (ACV) trap. The number of SWD captured/trap by QB baited trapping systems was significantly lower than that of the ACV trap. However, percent SWD/trap of QB baited traps was same within cherry. Lower non-target capture will save farmer/grower's labor and time allocated to traps installation and drosophila species identification. Within the USA, SWD selectivity of QB baited liquid traps was consistently greater than sticky trap in raspberry field, suggesting that the QB dispenser can be an alternative to the standard ACV lure and that trap design could improve selectivity further.

Maternal effects shape offspring physiological condition but do not senesce in a wild mammal.

In vertebrates, offspring survival often decreases with increasing maternal age. While many studies have reported a decline in fitness-related traits of offspring with increasing maternal age, the study of senescence in maternal effect through age-specific changes in offspring physiological condition is still at its infancy. We assessed the influence of maternal age and body mass on offspring physiological condition in two populations of roe deer (Capreolus capreolus) subjected to markedly different environmental conditions. We measured seven markers to index body condition and characterize the immune profile in 86 fawns which became recently independent of their known-aged mothers. We did not find striking effects of maternal age on offspring physiological condition measured at 8 months of age. This absence of evidence for senescence in maternal effects is likely due to the strong viability selection observed in the very first months of life in this species. Offspring physiological condition was, on the other hand, positively influenced by maternal body mass. Between-population differences in environmental conditions experienced by fawns also influenced their average body condition and immune phenotype. Fawns facing food limitation displayed lower values in some markers of body condition (body mass and haemoglobin levels) than those living in good quality habitat. They also allocated preferentially to humoral immunity, contrary to those living in good conditions, which allocated more to cellular response. These results shed a new light on the eco-physiological pathways mediating the relationship between mother's mass and offspring condition.

Short-term telomere dynamics is associated with glucocorticoid levels in wild populations of roe deer.

While evidence that telomere length is associated with health and mortality in humans and birds is accumulating, a large body of research is currently seeking to identify factors that modulate telomere dynamics. We tested the hypothesis that high levels of glucocorticoids in individuals under environmental stress should accelerate telomere shortening in two wild populations of roe deer (Capreolus capreolus) living in different ecological contexts. From two consecutive annual sampling sessions, we found that individuals with faster rates of telomere shortening had higher concentrations of fecal glucocorticoid metabolites, suggesting a functional link between glucocorticoid levels and telomere attrition rate. This relationship was consistent for both sexes and populations. This finding paves the way for further studies of the fitness consequences of exposure to environmental stressors in wild vertebrates.

The influence of early-life allocation to antlers on male performance during adulthood: Evidence from contrasted populations of a large herbivore.

To secure mating opportunities, males often develop and maintain conspicuous traits that are involved in intrasexual and/or intersexual competition. While current models of sexual selection rely on the assumption that producing such traits is costly, quantifying the cost of allocating to secondary sexual traits remains challenging. According to the principle of allocation, high energy allocation to growth or sexual traits in males should lead to reduced energy allocation to the maintenance of cellular and physiological functions, potentially causing them to age faster, with impaired survival. We evaluated the short-term and delayed consequences of energy allocation to antlers early in life in two contrasted populations of roe deer, Capreolus capreolus. Although most males mate successfully for the first time in their fourth year, antlers are grown annually from the first year of life onwards. We tested the prediction that a high level of allocation to antler growth during the first two years of life should lead to lower body mass, antler size and survival during the early and late prime stages, as well as to reduced longevity overall. Growing and carrying long antlers during the first years of life was not associated with any detectable cost in the late prime stage. The positive association between antler growth in early life and adult body mass instead supports that fawn antler acts as an honest signal of phenotypic quality in roe deer. For a given body mass, yearling males growing longer antlers displayed impaired performance during their late prime. We also found a trend for a short-term survival cost of allocation to relative antler length during the second year of life. Yearling males that grow long antlers relative to their mass might display a fast life-history tactic. We argue that differential allocation to secondary sexual traits generates a diversity of individual trajectories that should impact population dynamics.

Fruiting Strategies of Perennial Plants: A Resource Budget Model to Couple Mast Seeding to Pollination Efficiency and Resource Allocation Strategies.

Masting, a breeding strategy common in perennial plants, is defined by seed production that is highly variable over years and synchronized at the population level. Resource budget models (RBMs) proposed that masting relies on two processes: (i) the depletion of plant reserves following high fruiting levels, which leads to marked temporal fluctuations in fruiting; and (ii) outcross pollination that synchronizes seed crops among neighboring trees. We revisited the RBM approach to examine the extent to which masting could be impacted by the degree of pollination efficiency, by taking into account various logistic relationships between pollination success and pollen availability. To link masting to other reproductive traits, we split the reserve depletion coefficient into three biological parameters related to resource allocation strategies for flowering and fruiting. While outcross pollination is considered to be the key mechanism that synchronizes fruiting in RBMs, our model counterintuitively showed that intense masting should arise under low-efficiency pollination. When pollination is very efficient, medium-level masting may occur, provided that the costs of female flowering (relative to pollen production) and of fruiting (maximum fruit set and fruit size) are both very high. Our work highlights the powerful framework of RBMs, which include explicit biological parameters, to link fruiting dynamics to various reproductive traits and to provide new insights into the reproductive strategies of perennial plants.

The evolution of bet hedging in response to local ecological conditions.

Genotypes that hedge their bets can be favored by selection in an unpredictably varying environment. Bet hedging can be achieved by systematically expressing several phenotypes, such as one that readily attempts to reproduce and one that procrastinates in a dormant stage. But how much of each phenotype should a genotype express? Theory predicts that evolving bet-hedging strategies depend on local environmental variation, on how the population is regulated, and on exchanges with neighboring populations. Empirically, however, it remains unknown whether bet hedging can evolve to cope with the ecological conditions experienced by populations. Here we study the evolution of bet-hedging dormancy frequencies in two neighboring populations of the chestnut weevil, Curculio elephas. We estimate the temporal distribution of demographic parameters together with the form of the relationship between fecundity and population density and use both to parameterize models that predict the bet-hedging dormancy frequency expected to evolve in each population. Strikingly, the observed dormancy frequencies closely match predictions in their respective localities. We also found that dormancy frequencies vary randomly across generations, likely due to environmental perturbations of the underlying physiological mechanism. Using a model that includes these constraints, we predict the whole distribution of dormancy frequencies whose mean and shape agree with our observed data. Overall, our results suggest that dormancy frequencies have evolved according to local ecological conditions and physiological constraints.

Coexistence of insect species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments.

BACKGROUND: One major challenge in understanding how biodiversity is organized is finding out whether communities of competing species are shaped exclusively by species-level differences in ecological traits (niche theory), exclusively by random processes (neutral theory of biodiversity), or by both processes simultaneously. Communities of species competing for a pulsed resource are a suitable system for testing these theories: due to marked fluctuations in resource availability, the theories yield very different predictions about the timing of resource use and the synchronization of the population dynamics between the competing species. Accordingly, we explored mechanisms that might promote the local coexistence of phytophagous insects (four sister species of the genus Curculio) competing for oak acorns, a pulsed resource. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed the time partitioning of the exploitation of oak acorns by the four weevil species in two independent communities, and we assessed the level of synchronization in their population dynamics. In accordance with the niche theory, overall these species exhibited marked time partitioning of resource use, both within a given year and between different years owing to different dormancy strategies between species, as well as distinct demographic patterns. Two of the four weevil species, however, consistently exploited the resource during the same period of the year, exhibited a similar dormancy pattern, and did not show any significant difference in their population dynamics. CONCLUSIONS/SIGNIFICANCE: The marked time partitioning of the resource use appears as a keystone of the coexistence of these competing insect species, except for two of them which are demographically nearly equivalent. Communities of consumers of pulsed resources thus seem to offer a promising avenue for developing a unifying theory of biodiversity in fluctuating environments which might predict the co-occurrence, within the same community, of species that are ecologically either very similar, or very different.