François Klein

Antler size provides an honest signal of male phenotypic quality in roe deer.

Identifying factors shaping secondary sexual traits is essential in understanding how their variation may influence male fitness. Little information is available on the allocation of resources to antler growth in territorial ungulates with low sexual size dimorphism. We investigated phenotypic and environmental factors affecting both absolute and relative antler size of male roe deer in three contrasting populations in France and Sweden. In the three populations, we found marked age‐specific variation in antler size, with an increase in both absolute and relative antler size between yearling and prime‐age stages, followed by a decrease (senescence) for males older than 7 years. Antler size increased allometrically with body mass. This increase was particularly strong for senescent males, suggesting the evolution of two reproductive tactics: heavy old males invested particularly heavily in antler growth (potentially remaining competitive for territories), whereas light old males grew small antlers (potentially abandoning territory defense). Finally, environmental conditions had little effect on antler size: only population density negatively affected absolute antler size in one of the three populations. Antler size may therefore provide an honest signal of male phenotypic quality in roe deer. We discuss the implications of these results in terms of territory tenure and mating competition.

Multiple causes of sexual segregation in European red deer: enlightenments from varying breeding phenology at high and low latitude.

Sexual segregation outside the mating season occurs in most species of sexually dimorphic ungulates and has been extensively described in the literature, but the mechanisms causing segregation are still debated. The detailed pattern of sexual segregation throughout the year has rarely been presented for mammals, and no study, to our knowledge, has used latitudinal–related variation in breeding phenology to shed light on the underlying mechanisms. Recent methodological developments have made it possible to quantify separate components of segregation (social, habitat) and activity synchrony in animal groups, but these major improvements have so far been little used. We observed European red deer year round at two widely different latitudes (France and Norway) and tested three different mechanistic hypotheses of segregation related to: (i) predation risk; (ii) body–size–related forage selection; and (iii) activity budget. Habitat segregation peaked during calving in both populations and dropped rapidly after calving. Females with calves were more segregated from males than were females without calves, pointing to a key role of anti–predator behaviour even though large predators are absent in France and extremely rare in Norway. However, at both sites individuals also grouped with their own sex within habitat types (i.e. social segregation), and individuals in mixed–sex groups were less synchronized in activity type than individuals in either unisex male or unisex female groups, suggesting that differences in activity budgets are involved. Social segregation peaked during calving and was lowest during the rut (indicating aggregation) in both populations; these activities occurred one month later in the Northern populations, corresponding well with known differences in breeding phenology. We conclude that latitude–dependent breeding phenology shapes the seasonal pattern of sexual segregation and that sexual segregation in ungulates has multiple causes.

HETEROZYGOSITY-FITNESS CORRELATIONS REVEALED BY NEUTRAL AND CANDIDATE GENE MARKERS IN ROE DEER FROM A LONG-TERM STUDY

Heterozygosity-fitness correlations (HFCs) are increasingly reported but the underlying mechanisms causing HFCs are generally poorly understood. Here, we test for HFCs in roe deer (Capreolus capreolus) using 22 neutral microsatellites widely distributed in the genome and four microsatellites in genes that are potentially under selection. Juvenile survival was used as a proxy for individual fitness in a population that has been intensively studied for 30 years in northeastern France. For 222 juveniles, we computed two measures of genetic diversity: individual heterozygosity (H), and mean d 2 (relatedness of parental genomes). We found a relationship between genetic diversity and fitness both for the 22 neutral markers and two candidate genes: IGF1 (Insulin-like Growth Factor I) and NRAMP (natural resistance-associated macrophage protein). Statistical evidence and the size of genetic effects on juvenile survival were comparable to those reported for early development and cohort variation, suggesting a substantial influence of genetic components on fitness in this roe deer population. For the 22 neutral microsatellites, a correlation with fitness was revealed for mean d 2, but not for H, suggesting a possible outbreeding advantage. This heterosis effect could have been favored by introduction of genetically distant (Hungarian) roe deer to the population in recent times and, possibly, by the structuring of the population into distinct clans. The locus-specific correlations with fitness may be driven by growth rate advantages and resistance to diseases known to exist in the studied population. Our analyses of neutral and candidate gene markers both suggest that the observed HFCs are likely mainly due to linkage with dominant or overdominant loci that affect fitness (“local” effect) rather than to a genome-wide relationship with homozygosity due to inbreeding (“general” effect).

Habitat use under predation risk: hunting, roads and human dwellings influence the spatial behaviour of roe deer

Wildlife populations are subjected to increasing pressure linked to human activities, which introduce multiple stressors. Recently, in addition to direct effects, it has been shown that indirect (non-lethal) effects of predation risk are predominant in many populations. Predation risk is often structured in space and time, generating a heterogeneous “landscape of fear” within which animals can minimize risks by modifying their habitat use. Furthermore, for ungulates, resource quality seems to be positively correlated with human-related sources of risk. We studied the trade-off between access to resources of high-quality and risk-taking by contrasting habitat use of roe deer during daytime with that during nighttime for 94 roe deer in a hunted population. Our first hypothesis was that roe deer should avoid human disturbance by modifying their habitat use during daytime compared to nighttime. Our results supported this, as roe deer mainly used open fields during nighttime, but used more forested habitats during daytime, when human disturbance is higher. Moreover, we found that diel patterns in habitat use were influenced by hunting disturbance. Indeed, the roe deer decreased their use of high-crops during daytime, an important source of cover and food, during the hunting season. The proximity of roads and dwellings also affected habitat use, since roe deer used open fields during daytime to a greater extent when the distance to these sources of disturbance was higher. Hence, our results suggest that roe deer resolve the trade-off between the acquisition of high-quality resources and risk avoidance by modifying their habitat use between day and night.

Maternal and individual effects in selection of bed sites and their consequences for fawn survival at different spatial scales

We examined the relationship between survival of roe deer (Capreolus capreolus) fawns at Trois Fontaines, Champagne-Ardennes, France, and factors related to bed-site selection (predator avoidance and thermoregulation) and maternal food resources (forage availability in the maternal home range). Previous studies have demonstrated that at small scales, the young of large herbivores select bed sites independently from their mothers, although this selection takes place within the limits of their mother’s home range. Fawn survival was influenced largely by the availability of good bed sites within the maternal home range, not by the fawn’s selection of bed sites; however, selection for thermal cover when selecting bed sites positively influenced survival of young fawns. Typical features of a good home range included close proximity to habitat edges, which is related to forage accessibility for roe deer. The availability of bed sites changed as fawns aged, probably due to an increased mobility of the fawn or a different use of the home range by the mother; sites offering high concealment and thermal protection became less available in favor of areas with higher forage accessibility. Despite the minor influence of bed-site selection on survival, roe deer fawns strongly selected their bed sites according to several environmental factors linked to predator avoidance and thermoregulation. Fawns selected for sites providing concealment, light penetration, and avoided signs of wild boar (Sus scrofa) activity. Avoidance of sites with high light penetration by young fawns positively affected their survival, confirming a negative effect on thermoregulation due to reduced thermal cover. Selection for light penetration by older fawns was less clear. We discuss these results in the context of cross-generational effects in habitat selection across multiple scales, and the potential influence of the ‘ghost of predation past’.

How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer.

How populations respond to climate change depends on the interplay between life history, resource availability, and the intensity of the change. Roe deer are income breeders, with high levels of allocation to reproduction, and are hence strongly constrained by the availability of high quality resources during spring. We investigated how recent climate change has influenced demographic processes in two populations of this widespread species. Spring began increasingly earlier over the study, allowing us to identify 2 periods with contrasting onset of spring. Both populations grew more slowly when spring was early. As expected for a long-lived and iteroparous species, adult survival had the greatest potential impact on population growth. Using perturbation analyses, we measured the relative contribution of the demographic parameters to observed variation in population growth, both within and between periods and populations. Within periods, the identity of the critical parameter depended on the variance in growth rate, but variation in recruitment was the main driver of observed demographic change between periods of contrasting spring earliness. Our results indicate that roe deer in forest habitats cannot currently cope with increasingly early springs. We hypothesise that they should shift their distribution to richer, more heterogeneous landscapes to offset energetic requirements during the critical rearing stage.

High red deer density depresses body mass of roe deer fawns

Many previous studies have pointed out that, when resources are limited, the potential for competition should be high among sympatric species that display overlaps in habitat and nutritional niches. However, reliable evidence of competition between red deer (Cervus elaphus) and roe deer (Capreolus capreolus) has not been yet reported for life history traits directly measuring performance such as body mass, reproduction, or survival. From long-term monitoring of deer populations in the reserve of La Petite Pierre (France), we measured the sex-specific responses of roe deer fawn body mass to changes in red deer density after accounting for possible confounding effects of date of shooting, climatic conditions, and roe deer density. As expected under the hypothesis of competition, red deer density in a given year had a marked negative influence on body mass of roe deer fawns born the same year and the following year. Fawn mass of roe deer males and females responded in similar ways to changes in red deer density. Our study provides the first evidence of a negative response of roe deer performance to high red deer density.

Bigger teeth for longer life? Longevity and molar height in two roe deer populations

The role of tooth wear as a proximate cause of senescence in ruminants has recently been highlighted. There are two competing hypotheses to explain variation in tooth height and wear; the diet-quality hypothesis predicting increased wear in low-quality habitats, and the life-history hypothesis predicting molar height to be related to expected longevity. We compared tooth height and wear from roe deer of known age from two contrasting populations of roe deer (Capreolus capreolus) in France: Trois Fontaines (TF) with good habitat and shorter animal life expectancy and Chizé (CH) with poor habitat and longer animal life expectancy. There was no population difference in tooth wear, leading to rejection of the diet-quality hypothesis. However, despite their smaller body size, initial molar height for animals from CH was larger than for animals from TF. This provides the first evidence that variation in longevity between populations can lead to differences in molar height within a species.

Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate

The predictive adaptive response (PAR) hypothesis proposes that animals adjust their physiology and developmental trajectory during early life in anticipation of their future environments. Accordingly, when environmental conditions in early life match environmental conditions during adulthood, individual fitness should be greater. Here, we test this hypothesis in a long-lived mammal, the roe deer, using data from two contrasting populations, intensively monitored for more than 35 years. In the highly productive site, the fitness of female roe deer increased with the quality of environment during adulthood and, contrary to predictions of PAR, individuals born in good conditions always outperformed those born under poor conditions. In the resource-limited site, the fitness of female roe deer born in poor years was better than those born in good conditions in poor years when the animals were adult, but not in good years. Although consistent with predictions of PAR, we showed that this pattern is likely to be a consequence of increased viability selection during the juvenile stage for animals born in poor years. While PARs are often advanced in evolutionary medicine, our findings suggest that detailed biological processes should be investigated before drawing conclusions about the existence of this phenomenon.

Environmental Factors Associated with the Seroprevalence of Toxoplasma gondii in Wild Boars (Sus scrofa), France

Toxoplasma gondii is a protozoan parasite infecting humans and animals. Wild boars Sus scrofa are a potential source of human infection and an appropriate biological model for analyzing T. gondii dynamics in the environment. Here, we aimed to identify environmental factors explaining the seroprevalence of toxoplasmosis in French wild boar populations. Considering 938 individuals sampled from 377 ‘communes’, overall seroprevalence was 23% (95% confidence interval: [22–24]). Using a Poisson regression, we found that the number of seropositive wild boars detected per ‘commune’ was positively associated with the presence of European wildcats (Felis silvestris) and moderate winter temperatures.