Spatial genetic structure of European wild boar, with inferences on late-Pleistocene and Holocene demographic history.

European wildlife has been subjected to intensifying levels of anthropogenic impact throughout the Holocene, yet the main genetic partitioning of many species is thought to still reflect the late-Pleistocene glacial refugia. We analyzed 26,342 nuclear SNPs of 464 wild boar (Sus scrofa) across the European continent to infer demographic history and reassess the genetic consequences of natural and anthropogenic forces. We found that population fragmentation, inbreeding and recent hybridization with domestic pigs have caused the spatial genetic structure to be heterogeneous at the local scale. Underlying local anthropogenic signatures, we found a deep genetic structure in the form of an arch-shaped cline extending from the Dinaric Alps, via Southeastern Europe and the Baltic states, to Western Europe and, finally, to the genetically diverged Iberian peninsula. These findings indicate that, despite considerable anthropogenic influence, the deeper, natural continental structure is still intact. Regarding the glacial refugia, our findings show a weaker signal than generally assumed, but are nevertheless suggestive of two main recolonization routes, with important roles for Southern France and the Balkans. Our results highlight the importance of applying genomic resources and framing genetic results within a species' demographic history and geographic distribution for a better understanding of the complex mixture of underlying processes.

Amplified Cyclicality in Mast Seeding Dynamics Positively Influences the Dynamics of a Seed Consumer Species.

AbstractTemporal autocorrelation in environmental conditions influences population dynamics through its effects on vital rates. However, a comprehensive understanding of how and to what extent temporal autocorrelation shapes population dynamics is still lacking because most empirical studies have unrealistically assumed that environmental conditions are temporally independent. Mast seeding is a biological event characterized by highly fluctuating and synchronized seed production at the tree population scale as well as a marked negative temporal autocorrelation. In the current context of global change, mast seeding events are expected to become more frequent, leading to strengthened negative temporal autocorrelations and thereby amplified cyclicality in mast seeding dynamics. Theory predicts that population growth rates are maximized when the environmental cyclicality of consumer resources and their generation times are closely matched. To test this prediction, we took advantage of the long-term monitoring of a wild boar population, a widespread seed consumer species characterized by a short generation time (∼2 years). As expected, simulations indicated that its stochastic population growth rate increased as mast seeding dynamics became more negatively autocorrelated. Our findings demonstrate that accounting for temporal autocorrelations in environmental conditions relative to the generation time of the focal population is required, especially under conditions of global warming, where the cyclicality in resource dynamics is likely to change.

Effects of habitat fragmentation and hunting activities on African swine fever dynamics among wild boar populations.

African Swine Fever (ASF) has been slowly but steadily increasing its endemic range throughout Europe, posing an imminent risk to the pig industry. ASF transmission among wild boar occurs mainly through wild boar population movements, hence wild boar presence and density are important risk factors for introducing, maintaining, and spreading the disease. The understanding of wild boar population dynamics and their role in ASF transmission and persistence remains limited. It is crucial to gain knowledge in this area to improve wildlife management while minimizing the risks for ASF introduction and spread. We adapted an individual-based spatio-temporal stochastic model developed by Halasa et al. (2019) and tailored it to two regions in France. The model assessed yearly hunting activity, the carcass persistence seasonality, and the specific landscape characteristics of the Franco-Belgian border region and the Pyrénées-Atlantiques department. Following the establishment of local population dynamics through preliminary runs of the model, the model was run 100 iterations over 8 years in the two study areas where ASF was randomly seeded after the 2nd year of simulation. For each scenario, the model was initiated with 500 wild boar groups randomly spread across the study areas. Hunting activities were included and excluded to assess the impact on population growth and ASF spread. Results showed an ever-growing wild boar population for all scenarios, which was balanced when hunting activities were included. When introducing ASF, the wild boar populations were dramatically impacted in both areas with a decrease of 63 % of the population at the Franco-Belgian border and 86 % in the Pyrénées-Atlantiques department. Habitat fragmentation and landscape connectivity were highlighted as important factors shaping ASF propagation. The Franco-Belgian border, which had the most fragmented habitat with unsuitable areas for wild boars, was shown to limit wild boar movements, reducing the probability, and spread of ASF across the landscape. The lack of connectivity was reflected in a less effective transmission and lower number of infected groups (406 versus 467). In contrast, the epidemic duration was lengthened in the fragmented habitat compared to the homogenous area (2.6 years vs 1.6 years). This study provided information on defining and implementing control measures in case of an ASF incursion, since delimitation of the area via fences artificially induces landscape fragmentation, which is important for controlling ASF outbreaks.

Does mast seeding shape mating time in wild boar? A comparative study.

In seasonal environments, the timing of reproduction often matches with the peak of food resources. One well-known effect of global warming is an earlier phenology of resources, leading to a possible mismatch between the timing of reproduction for consumers and food peak. However, global warming may also change the dynamics of food resources, such as the intensity and frequency of pulsed mast seeding. How quantitative changes in mast seeding influence the timing of reproduction of seed consumers remains unexplored. Here, we assess how yearly variation in mast seeding influences mating time in wild boar (Sus scrofa), a widespread seed consumer species. We took advantage of the intensive monitoring of both female reproduction (1636 females) and acorn production over 6 consecutive years across 15 populations of wild boar in the wild. We found that mating time occurs earlier when acorn production increases in most but not all populations. In two out of 15 populations, heavy females mated earlier than light ones. Our findings demonstrate that mast seeding advances the mating time in some populations, which could perhaps impact how boars respond to climate change.

Many lifetime growth trajectories for a single mammal.

Despite their importance in shaping life history tactics and population dynamics, individual growth trajectories have only been rarely explored in the wild because their analysis requires multiple measurements of individuals throughout their lifetime and some knowledge of age, a key timer of body growth. The availability of long-term longitudinal studies of two wild boar populations subjected to contrasting environments (rich vs. poor) provided an opportunity to analyze individual growth trajectories. We quantified wild boar growth trajectories at both the population and the individual levels using standard growth models (i.e., Gompertz, logistic, and monomolecular models) that encompass the expected range of growth shapes in determinate growers. Wild boar is a rather altricial species, with a polygynous mating system and is strongly sexually dimorphic in size. According to current theories of life history evolution, we thus expect wild boar to display a sex-specific Gompertz type growth trajectory and lower sexual size dimorphism in the poorer environment. While wild boar displayed the expected Gompertz type trajectory in the rich site at the population level, we found some evidence for potential differences in growth shapes between populations and individuals. Asymptotic body mass, growth rate and timing of maximum growth rate differed as well, which indicates a high flexibility of growth in wild boar. We also found a cohort effect on asymptotic body mass, which suggests that environmental conditions early in life shape body mass at adulthood in this species. Our findings demonstrate that body growth trajectories in wild boar are highly diverse in relation to differences of environmental context, sex and year of birth. Whether the intermediate ranking of wild boar along the precocial-altricial continuum of development at birth may explain the ability of this species to exhibit this high diversity of growth patterns remains to be investigated.

How does increasing mast seeding frequency affect population dynamics of seed consumers? Wild boar as a case study.

Mast seeding in temperate oak populations shapes the dynamics of seed consumers and numerous communities. Mast seeding responds positively to warm spring temperatures and is therefore expected to increase under global warming. We investigated the potential effects of changes in oak mast seeding on wild boar population dynamics, a widespread and abundant consumer species. Using long-term monitoring data, we showed that abundant acorn production enhances the proportion of breeding females. With a body-mass-structured population model and a fixed hunting rate of 0.424, we showed that high acorn production over time would lead to an average wild boar population growth rate of 1.197 whereas non-acorn production would lead to a stable population. Finally, using climate projections and a mechanistic model linking weather data to oak reproduction, we predicted that mast seeding frequency might increase over the next century, which would lead to increase in both wild boar population size and the magnitude of its temporal variation. Our study provides rare evidence that some species could greatly benefit from global warming thanks to higher food availability and therefore highlights the importance of investigating the cascading effects of changing weather conditions on the dynamics of wild animal populations to reliably assess the effects of climate change.

Grow fast at no cost: no evidence for a mortality cost for fast early-life growth in a hunted wild boar population.

From current theories on life-history evolution, fast early-life growth to reach early reproduction in heavily hunted populations should be favored despite the possible occurrence of mortality costs later on. However, fast growth may also be associated with better individual quality and thereby lower mortality, obscuring a clear trade-off between early-life growth and survival. Moreover, fast early-life growth can be associated with sex-specific mortality costs related to resource acquisition and allocation throughout an individual's lifetime. In this study, we explore how individual growth early in life affects age-specific mortality of both sexes in a heavily hunted population. Using longitudinal data from an intensively hunted population of wild boar (Sus scrofa), and capture-mark-recapture-recovery models, we first estimated age-specific overall mortality and expressed it as a function of early-life growth rate. Overall mortality models showed that faster-growing males experienced lower mortality at all ages. Female overall mortality was not strongly related to early-life growth rate. We then split overall mortality into its two components (i.e., non-hunting mortality vs. hunting mortality) to explore the relationship between growth early in life and mortality from each cause. Faster-growing males experienced lower non-hunting mortality as subadults and lower hunting mortality marginal on age. Females of all age classes did not display a strong association between their early-life growth rate and either mortality type. Our study does not provide evidence for a clear trade-off between early-life growth and mortality.

Should I stay or should I go? Determinants of immediate and delayed movement responses of female red deer (Cervus elaphus) to drive hunts.

Hunting can be used as a tool for wildlife management, through limitation of population densities and dissuading game from using sensitive areas. The success of these approaches requires in depth knowledge of prey movement. Indeed, movement decisions of game during hunting may affect the killing success of hunters as well as the subsequent location of surviving animals. We thus investigated red deer movement responses to drive hunts and their causal factors. We studied 34 hunting events in the National Estate of Chambord (France) and thereby provided a fine-scale characterization of the immediate and delayed movement responses of red deer to drive hunts. Red deer responded to drive hunts either by immediately fleeing the hunted area, or by initially remaining before ultimately fleeing after the hunters had departed. A few hours after the hunt, all individuals were located in distant areas (> 2 kilometres) from the hunted area. Immediate flight responses were less common when drive hunts occurred in areas with dense understorey. However, neither beater/dog densities nor site familiarity influenced the immediate flight decision. Following a drive hunt, red deer remained outside the hunted areas for periods twice as long compared to periods when no hunting occurred (34 hours vs. 17 hours). Such knowledge of game movement rates in response to drive hunts may help the development of informed management policy for hunted red deer populations.

Assessment of the impact of forestry and leisure activities on wild boar spatial disturbance with a potential application to ASF risk of spread.

In Europe, African swine fever virus (ASFV) is one of the most threatening infectious transboundary diseases of domestic pigs and wild boar. In September 2018, ASF was detected in wild boar in the South of Belgium. France, as a bordering country, is extremely concerned about the ASF situation in Belgium, and an active preparedness is ongoing in the country. One of the questions raised by this situation relates to disturbing activities that may affect wild boar movements and their possible impact on the spread of ASFV. Despite evidence of disturbance related to hunting practices, there is a paucity of information on the impact of forestry and human leisure activities. To assess this impact on wild boar movements, a systematic review was first conducted but very few useful data were obtained. For this reason, an expert elicitation was carried out by the French Agency for Food, Environmental and Occupational Health & Safety in order to deal with this knowledge gap. A total of 30 experts originating from France and adjacent neighbouring countries (Spain, Belgium and Switzerland) were elicited about the relative importance of six factors of spatial disturbance of wild boar (noise, smell, invasion of space, modification of the environment, duration and frequency of the activity). Then, for each factor of disturbance, they were asked about the impact of 16 different commercial forestry and human leisure activities. A global weighted score was estimated in order to capture the variability of a wide range of territorial conditions and the uncertainty of expert elicitation. This estimate permitted ranking all 16 activities and aggregating them in three groups according to their potential for disturbance of wild boar, using a regression tree analysis. The results of this expert elicitation provide a methodological approach that may be useful for French and other European decision makers and stakeholders involved in the crisis management of ASF.

Many, large and early: Hunting pressure on wild boar relates to simple metrics of hunting effort.

Wild boar populations have increased dramatically over the last decades throughout Europe and in France in particular. While hunting is considered the most efficient way to control game populations, many local conflicts persist after the hunting period due to remaining high densities of wild boar despite the large number of animals culled every year. Therefore, increasing the efficiency of hunting is a timely issue. Herein, we assessed how hunting effort can be measured, and we determined whether the hunting effort carried out by hunters explains the observed hunting pressure. We measured the characteristics and results of all hunts that occurred in the experimental forest of Châteauvillain-Arc-en-Barrois (Northeastern France), and we modelled the number of animals culled as a function of the hunting effort, measured by the number of beaters, hunters, and dogs, as well as the size of the hunting area. We also accounted for variables suspected to affect the hunting efficiency achieved with a given effort, such as time of day (AM/PM), the month during which hunting occurred. We found that more posted hunters, larger hunted areas, and hunts carried out early in the season, i.e. before February, increased the number of culled animals. Our model can be used by wildlife managers to adjust hunting effort in order to reach the hunting pressure expected to meet management objectives.

Reproductive allocation in pulsed-resource environments: a comparative study in two populations of wild boar.

Pulsed resources influence the demography and evolution of consumer populations and, by cascading effect, the dynamics of the entire community. Mast seeding provides a case study for exploring the evolution of life history traits of consumers in fluctuating environments. Wild boar (Sus scrofa) population dynamics is related to seed availability (acorns/beechnuts). From a long-term monitoring of two populations subjected to markedly different environmental contexts (i.e., both low vs. high frequency of pulsed resources and low vs. high hunting pressure in Italy and in France, respectively), we assessed how pulsed resources shape the reproductive output of females. Using path analyses, we showed that in both populations, abundant seed availability increases body mass and both the absolute and the relative (to body mass) allocation to reproduction through higher fertility. In the Italian population, females equally relied on past and current resources for reproduction and ranked at an intermediate position along the capital-income continuum of breeding tactics. In contrast, in the French population, females relied on current more than past resources and ranked closer to the income end of the continuum. In the French population, one-year old females born in acorn-mast years were heavier and had larger litter size than females born in beechnut-mast years. In addition to the quantity, the type of resources (acorns/beechnuts) has to be accounted for to assess reliably how females allocate resources to reproduction. Our findings highlight a high plasticity in breeding tactics in wild boar females and provide new insight on allocation strategies in fluctuating environments.

On the evolutionary consequences of increasing litter size with multiple paternity in wild boar (Sus scrofa scrofa).

Understanding how some species may be able to evolve quickly enough to deal with anthropogenic pressure is of prime interest in evolutionary biology, conservation, and management. Wild boar (Sus scrofa scrofa) populations keep growing all over Europe despite increasing hunting pressure. In wild boar populations subject to male-selective harvesting, the initially described polygynous mating system may switch to a promiscuous/polyandrous one. Such a change in the mating system, where potentially more males sire a litter at one reproductive event, may be associated with the retention of high genetic diversity and an increase of litter size. We tested these hypotheses by estimating the number of sires per litter based on a six-year long monitoring of a wild boar population subject to particularly high harvesting pressure. Our results show a high and stable genetic diversity and high rates of multiple paternity compared to other populations, thus depicting a promiscuous/polyandrous mating system in this population. We also show that litter size is positively linked to the number of sires, suggesting that multiple paternity increases fecundity. We finally discuss that multiple paternity may be one of the factors allowing rapid evolution of this population by maintaining both genetic and phenotypic diversity.

Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe.

Across Europe, wild boar numbers increased in the 1960s-1970s but stabilised in the 1980s; recent evidence suggests that the numbers and impact of wild boar has grown steadily since the 1980s. As hunting is the main cause of mortality for this species, we reviewed wild boar hunting bags and hunter population trends in 18 European countries from 1982 to 2012. Hunting statistics and numbers of hunters were used as indicators of animal numbers and hunting pressure. The results confirmed that wild boar increased consistently throughout Europe, while the number of hunters remained relatively stable or declined in most countries. We conclude that recreational hunting is insufficient to limit wild boar population growth and that the relative impact of hunting on wild boar mortality had decreased. Other factors, such as mild winters, reforestation, intensification of crop production, supplementary feeding and compensatory population responses of wild boar to hunting pressure might also explain population growth. As populations continue to grow, more human-wild boar conflicts are expected unless this trend is reversed. New interdisciplinary approaches are urgently required to mitigate human-wild boar conflicts, which are otherwise destined to grow further.

Influence of life-history tactics on transient dynamics: a comparative analysis across mammalian populations.

Most mammalian populations suffer from natural or human-induced disturbances; populations are no longer at the equilibrium (i.e., at stable [st]age distribution) and exhibit transient dynamics. From a literature survey, we studied patterns of transient dynamics for mammalian species spanning a large range of life-history tactics and population growth rates. For each population, we built an age-structured matrix and calculated six metrics of transient dynamics. After controlling for possible confounding effects of the phylogenetic relatedness among species using a phylogenetic principal component analysis and phylogenetic generalized least squares models, we found that short-term demographic responses of mammalian populations to disturbance are shaped by generation time and growth rate. Species with a slow pace of life (i.e., species with a late maturity, a low fecundity, and a long life span) displayed decreases in population size after a disturbance, whereas fast-living species increased in population size. The magnitude of short-term variation in population size increased with asymptotic population growth, being buffered in slow-growing species (i.e., species with a low population growth rate) but large in fast-growing species. By demonstrating direct links between transient dynamics, life history (generation time), and ecology (demographic regime), our comparative analysis of transient dynamics clearly improves our understanding of population dynamics in variable environments and has clear implications for future studies of the interplay between evolutionary and ecological dynamics. As most populations in the wild are not at equilibrium, we recommend that analyses of transient dynamics be performed when studying population dynamics in variable environments.

Do age-specific survival patterns of wild boar fit current evolutionary theories of senescence?

Actuarial senescence is widespread in age-structured populations. In growing populations, the progressive decline of Hamiltonian forces of selection with age leads to decreasing survival. As actuarial senescence is overcompensated by a high fertility, actuarial senescence should be more intense in species with high reproductive effort, a theoretical prediction that has not been yet explicitly tested across species. Wild boar (Sus scrofa) females have an unusual life-history strategy among large mammals by associating both early and high reproductive effort with potentially long lifespan. Therefore, wild boar females should show stronger actuarial senescence than similar-sized related mammals. Moreover, being polygynous and much larger than females, males should display higher senescence rates than females. Using a long-term monitoring (18 years) of a wild boar population, we tested these predictions. We provided clear evidence of actuarial senescence in both sexes. Wild boar females had earlier but not stronger actuarial senescence than similar-sized ungulates. Both sexes displayed similar senescence rates. Our study indicates that the timing of senescence, not the rate, is associated with the magnitude of fertility in ungulates. This demonstrates the importance of including the timing of senescence in addition to its rate to understand variation in senescence patterns in wild populations.

Fluctuating food resources influence developmental plasticity in wild boar.

To maximize long-term average reproductive success, individuals can diversify the phenotypes of offspring produced within a reproductive event by displaying the 'coin-flipping' tactic. Wild boar (Sus scrofa scrofa) females have been reported to adopt this tactic. However, whether the magnitude of developmental plasticity within a litter depends on stochasticity in food resources has not been yet investigated. From long-term monitoring, we found that juvenile females produced similar-sized fetuses within a litter independent of food availability. By contrast, adult females adjusted their relative allocation to littermates to the amount of food resources, by providing a similar allocation to all littermates in years of poor food resources but producing highly diversified offspring phenotypes within a litter in years of abundant food resources. By minimizing sibling rivalry, such a plastic reproductive tactic allows adult wild boar females to maximize the number of littermates for a given breeding event.

The relationship between phenotypic variation among offspring and mother body mass in wild boar: evidence of coin-flipping?

1. In highly variable environments, the optimal reproductive tactics of iteroparous organisms should minimize variance in yearly reproductive success to maximize the long-term average reproductive success. To minimize among-year variation in reproductive success, individuals can either minimize the variance in the number of offspring produced at each reproductive attempt (classical bet-hedging) or maximize the phenotypic diversity of offspring produced within or among reproductive attempts (coin-flipping). 2. From a long-term detailed study of an intensively exploited population facing a highly unpredictable environment, we identify a continuum of reproductive tactics in wild boar females depending on their body mass. 3. At one end, light females adjusted litter size to their body mass and produced highly similar-sized offspring within a litter. These females fitted the hypothesis of individual optimization commonly reported in warm-blooded species, which involves both an optimal mass and an optimal number of offspring for a given mother. At the other end of the continuum, heavy females produced litters of variable size including a mixture of heavy and light offspring within litters. 4. Prolific heavy wild boar females diversify the phenotype of their offspring, providing a first evidence for coin-flipping in a warm-blooded species.

Predator-prey spatial game as a tool to understand the effects of protected areas on harvester-wildlife interactions.

No-take reserves are sometimes implemented for sustainable population harvesting because they offer opportunities for animals to spatially avoid harvesters, whereas harvesters can benefit in return from the reserve spillover. Here, we used the framework of predator-prey spatial games to understand how protected areas shape spatial interactions between harvesters and target species and determine animal mortality. In these spatial games, the "predator" searches for "prey" and matches their habitat use, unless it meets spatial constraints offering the opportunity for prey to avoid the mortality source. However, such prey refuges could attract predators in the surroundings, which questions the potential benefits for prey. We located, in the Geneva Basin (France), hunting dogs and wild boar Sus scrofa L. during hunting seasons with global positioning systems and very-high-frequency collars. We quantified how the proximity of the reserve shaped the matching between both habitat uses using multivariate analyses and linked these patterns to animals' mortality with a Cox regression analysis. Results showed that habitat uses by both protagonists disassociated only when hunters were spatially constrained by the reserve. In response, hunters increased hunting efforts near the reserve boundary, which induced a higher risk exposure for animals settled over the reserve. The mortality of adult wild boar decreased near the reserve as the mismatch between both habitat uses increased. However the opposite pattern was determined for younger individuals that suffered from the high level of hunting close to the reserve. The predator-prey analogy was an accurate prediction of how the protected area modified spatial relationships between harvesters and target species. Prey-searching strategies adopted by hunters around reserves strongly impacted animal mortality and the efficiency of the protected area for this harvested species. Increasing reserve sizes and/or implementing buffer areas with harvesting limitations can dampen this edge effect and helps harvesters to benefit durably from source populations of reserves. Predator-prey spatial games therefore provide a powerful theoretical background for understanding wildlife-harvester spatial interactions and developing substantial application for sustainable harvesting.

High hunting pressure selects for earlier birth date: wild boar as a case study.

Exploitation by humans affects the size and structure of populations. This has evolutionary and demographic consequences that have typically being studied independent of one another. We here applied a framework recently developed applying quantitative tools from population ecology and selection gradient analysis to quantify the selection on a quantitative trait-birth date-through its association with multiple fitness components. From the long-term monitoring (22 years) of a wild boar (Sus scrofa scrofa) population subject to markedly increasing hunting pressure, we found that birth dates have advanced by up to 12 days throughout the study period. During the period of low hunting pressure, there was no detectable selection. However, during the period of high hunting pressure, the selection gradient linking breeding probability in the first year of life to birth date was negative, supporting current life-history theory predicting selection for early births to reproduce within the first year of life with increasing adult mortality.

Assessing whether mortality is additive using marked animals: a Bayesian state-space modeling approach.

Whether different sources of mortality are additive, compensatory, or depensatory is a key question in population biology. A way to test for additivity is to calculate the correlation between cause-specific mortality rates obtained from marked animals. However, existing methods to estimate this correlation raise several methodological issues. One difficulty is the existence of an intrinsic bias in the correlation parameter. Although this bias can be formally expressed, it requires knowledge about natural survival without any competing mortality source, which is difficult to assess in most cases. Another difficulty lies in estimating the true process correlation while properly accounting for sampling variation. Using a Bayesian approach, we developed a state-space model to assess the correlation between two competing sources of mortality. By distinguishing the mortality process from its observation through dead recoveries and live recaptures, we estimated the process correlation. To correct for the intrinsic bias, we incorporated experts' opinions on natural survival. We illustrated our approach using data on a hunted population of wild boars. Mortalities were not additive and natural mortality increased with hunting mortality likely as a consequence of non-controlled mortality by crippling loss. Our method opens perspectives for wildlife management and for the conservation of endangered species.