Evolutionary approach for pollution study: The case of ionizing radiation.

Estimating the consequences of environmental changes, specifically in a global change context, is essential for conservation issues. In the case of pollutants, the interest in using an evolutionary approach to investigate their consequences has been emphasized since the 2000s, but these studies remain rare compared to the characterization of direct effects on individual features. We focused on the study case of anthropogenic ionizing radiation because, despite its potential strong impact on evolution, the scarcity of evolutionary approaches to study the biological consequences of this stressor is particularly true. In this study, by investigating some particular features of the biological effects of this stressor, and by reviewing existing studies on evolution under ionizing radiation, we suggest that evolutionary approach may help provide an integrative view on the biological consequences of ionizing radiation. We focused on three topics: (i) the mutagenic properties of ionizing radiation and its disruption of evolutionary processes, (ii) exposures at different time scales, leading to an interaction between past and contemporary evolution, and (iii) the special features of contaminated areas called exclusion zones and how evolution could match field and laboratory observed effects. This approach can contribute to answering several key issues in radioecology: to explain species differences in the sensitivity to ionizing radiation, to improve our estimation of the impacts of ionizing radiation on populations, and to help identify the environmental features impacting organisms (e.g., interaction with other pollution, migration of populations, anthropogenic environmental changes). Evolutionary approach would benefit from being integrated to the ecological risk assessment process.

Toward a unified framework for studying behavioural tolerance.

Behavioural responses are widely held to allow animals to cope with human-induced environmental changes. Less often appreciated is that the absence of behavioural response can also be advantageous. This is particularly true when animals become tolerant to situations that may be perceived as risky, although the actual risk is nonexistent. We provide a framework to understand the causes and consequences of behavioural tolerance. Tolerance can emerge from genetic, epigenetic, or learning mechanisms, each exerting different degrees of influence on its speed of acquisition, reversibility, specificity, and duration. The ultimate impact on fitness hinges on the interplay between these mechanisms and the nature of the stressor. Mechanistic clarity is therefore essential to better understand and manage human-wildlife interactions in the Anthropocene.

Environmental and individual determinants of burrow-site microhabitat selection, occupancy, and fidelity in eastern chipmunks living in a pulsed-resource ecosystem.

Background: Habitat selection has major consequences on individual fitness, particularly selection for breeding sites such as nests or burrows. Theory predicts that animals will first use optimal habitats or rearrange their distribution by moving to higher-quality habitats whenever possible, for instance when another resident disperses or dies, or when environmental changes occur. External constraints, such as predation risk or resource abundance, and interindividual differences in age, sex and body condition can lead to variation in animals' perception of habitat quality. Following habitat use by individuals over their lifetime is thus essential to understand the causes of variation in habitat selection within a population. Methods: We used burrow occupancy data collected over eight years to assess burrow-site selection in a population of wild eastern chipmunks (Tamias striatus) relying on pulsed resources. We first compared characteristics of burrow microhabitats with those of equivalent unused plots. We then investigated the factors influencing the frequency of burrow occupation over time, and the individual and environmental causes of annual burrow fidelity decisions. Results: Our results indicate that chipmunks select microhabitats with a greater number of woody debris and greater slopes. Microhabitats of burrows with higher occupancy rates had a lower shrub stratum, were less horizontally opened and their occupants' sex-ratio was skewed towards males. Burrow fidelity was higher in non-mast years and positively related to the occupant's age, microhabitat canopy cover and density of large red maples. Conclusion: The quality of a burrow microhabitat appears to be determined in part by characteristics that favour predation avoidance, but consideration of occupancy and fidelity patterns over several years also highlighted the importance of including individual and contextual factors in habitat selection studies.

Track and dive-based movement metrics do not predict the number of prey encountered by a marine predator.

BACKGROUND: Studying animal movement in the context of the optimal foraging theory has led to the development of simple movement metrics for inferring feeding activity. Yet, the predictive capacity of these metrics in natural environments has been given little attention, raising serious questions of the validity of these metrics. The aim of this study is to test whether simple continuous movement metrics predict feeding intensity in a marine predator, the southern elephant seal (SES; Mirounga leonine), and investigate potential factors influencing the predictive capacity of these metrics. METHODS: We equipped 21 female SES from the Kerguelen Archipelago with loggers and recorded their movements during post-breeding foraging trips at sea. From accelerometry, we estimated the number of prey encounter events (nPEE) and used it as a reference for feeding intensity. We also extracted several track- and dive-based movement metrics and evaluated how well they explain and predict the variance in nPEE. We conducted our analysis at two temporal scales (dive and day), with two dive profile resolutions (high at 1 Hz and low with five dive segments), and two types of models (linear models and regression trees). RESULTS: We found that none of the movement metrics predict nPEE with satisfactory power. The vertical transit rates (primarily the ascent rate) during dives had the best predictive performance among all metrics. Dive metrics performed better than track metrics and all metrics performed on average better at the scale of days than the scale of dives. However, the performance of the models at the scale of days showed higher variability among individuals suggesting distinct foraging tactics. Dive-based metrics performed better when computed from high-resolution dive profiles than low-resolution dive profiles. Finally, regression trees produced more accurate predictions than linear models. CONCLUSIONS: Our study reveals that simple movement metrics do not predict feeding activity in free-ranging marine predators. This could emerge from differences between individuals, temporal scales, and the data resolution used, among many other factors. We conclude that these simple metrics should be avoided or carefully tested a priori with the studied species and the ecological context to account for significant influencing factors.

Ionizing radiation affects the demography and the evolution of Caenorhabditis elegans populations.

Ionizing radiation can reduce survival, reproduction and affect development, and lead to the extinction of populations if their evolutionary response is insufficient. However, demographic and evolutionary studies on the effects of ionizing radiation are still scarce. Using an experimental evolution approach, we analyzed population growth rate and associated change in life history traits across generations in Caenorhabditis elegans populations exposed to 0, 1.4, and 50.0 mGy.h-1 of ionizing radiation (gamma external irradiation). We found a higher population growth rate in the 1.4 mGy.h-1 treatment and a lower in the 50.0 mGy.h-1 treatment compared to the control. Realized fecundity was lower in both 1.4 and 50.0 mGy.h-1 than control treatment. High irradiation levels decreased brood size from self-fertilized hermaphrodites, specifically early brood size. Finally, high irradiation levels decreased hatching success compared to the control condition. In reciprocal-transplant experiments, we found that life in low irradiation conditions led to the evolution of higher hatching success and late brood size. These changes could provide better tolerance against ionizing radiation, investing more in self-maintenance than in reproduction. These evolutionary changes were with some costs of adaptation. This study shows that ionizing radiation has both demographic and evolutionary consequences on populations.

Male frequency in Caenorhabditis elegans increases in response to chronic irradiation.

Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may, therefore, switch their reproductive mode from inbreeding to outcrossing when under environmental stress. This switch may have consequences on the demographic dynamics and evolutionary trajectory of populations. For example, it may directly influence the sex ratio of a population. However, much remains to be discovered about the mechanisms and evolutionary implications of sex ratio changes in a population in response to environmental stress. Populations of the androdioecious nematode Caenorhabditis elegans, are composed of selfing hermaphrodites and rare males. Here, we investigate the changes in the sex ratio of C. elegans populations exposed to radioactive pollution for 60 days or around 20 generations. We experimentally exposed populations to three levels of ionizing radiation (i.e., 0, 1.4, and 50 mGy.h-1). We then performed reciprocal transplant experiments to evaluate genetic divergence between populations submitted to different treatments. Finally, we used a mathematical model to examine the evolutionary mechanisms that could be responsible for the change in sex ratio. Our results showed an increase in male frequency in irradiated populations, and this effect increased with the dose rate. The model showed that an increase in male fertilization success or a decrease in hermaphrodite self-fertilization could explain this increase in the frequency of males. Moreover, males persisted in populations after transplant back into the control conditions. These results suggested selection favoring outcrossing under irradiation conditions. This study shows that ionizing radiation can sustainably alter the reproductive strategy of a population, likely impacting its long-term evolutionary history. This study highlights the need to evaluate the impact of pollutants on the reproductive strategies of populations when assessing the ecological risks.

A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours.

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco-evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non-urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta-analysis of the avian literature to compare urban versus non-urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non-urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non-urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential.

The Feast and the Famine: Spring Body Mass Variations and Life History Traits in a Pulse Resource Ecosystem.

AbstractPhenotypic plasticity is the most immediate mechanism of adaptative response to environmental change. Studying plastic changes in response to fluctuating environments provides insights into how such adjustments may impact life history traits. Here, we used a 14-year data set of repeated body mass measurements in male eastern chipmunks (Tamias striatus) to assess the extent of plastic changes for this trait in a resource pulse ecosystem. We first determined the magnitude of variation in body mass at the population level in response to the drastic change in food resource availability from American beech tree seeds (Fagus grandifolia). Males that emerged in the spring from winter torpor following a nonmast year had a lower body mass than males emerging after a mast year, but they tended to recover this loss by mid-June. We found significant among-individual variation in spring body mass plasticity (i.e., individual-by-environment interaction). We then investigated the relationships between individual spring body mass plasticity, longevity, and lifetime reproductive success. Interestingly, heavier males lived longer than lighter males, but more plastic males had a lower longevity and lower lifetime reproductive success than less plastic males. The report of such plastic response in a stochastic resource system provides valuable insights into the interplay between the costs and benefits of phenotypic plasticity as an adaptation to environmental fluctuations.

Resource Availability, Sex, and Individual Differences in Exploration Drive Individual Diet Specialization.

AbstractIndividual diet specialization (IDS) is widespread and can affect the ecological and evolutionary dynamics of populations in significant ways. Extrinsic factors (e.g., food abundance) and individual variation in energetic needs, morphology, or physiology have been suggested as drivers of IDS. Behavioral traits like exploration and boldness can also impact foraging decisions, although their effects on IDS have not yet been investigated. Specifically, variation among individuals in exploratory behavior and their position along the exploration/exploitation trade-off may affect their foraging behavior, acquisition of food items, and home range size, which may in turn influence the diversity of their diet. Here, we analyzed stable carbon and nitrogen isotopes in hair of wild eastern chipmunks, Tamias striatus, to investigate the influence of individual differences in exploration on IDS. We found that exploration profile, sex, and yearly fluctuations in food availability explained differences in the degree of dietary specialization and in plasticity in stable carbon and stable nitrogen over time. Thus, consistent individual differences in exploration can be an important driver of within-population niche specialization and could therefore affect within-species competition. Our results highlight the need for a more thorough investigation of the mechanisms underlying the link between individual behavioral differences and diet specialization in wild animal populations.

Telomere length positively correlates with pace-of-life in a sex- and cohort-specific way and elongates with age in a wild mammal.

Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus coevolved with early reproduction, proactive behaviour and reduced lifespan, that is, a fast pace-of-life syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anticancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age (n = 204 and n = 20) and do not limit lifespan in this species (n = 51). Furthermore, short telomeres correlated with a slow POLS in a sex-specific way (n = 37). Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, while we found no differences in males. Our findings support most predictions adapted from the anticancer hypothesis, but none of those from the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade-offs shape the diversity of telomere length in adult somatic cells and the relationships between telomere length and life-histories.

Differences in the temporal scale of reproductive investment across the slow-fast continuum in a passerine.

Life-history strategies differ with respect to investment in current versus 'future' reproduction, but when is this future? Under the novel 'temporality in reproductive investment hypothesis', we postulate variation should exist in the time frame over which reproductive costs are paid. Slow-paced individuals should pay reproductive costs over short (e.g. inter-annual) time scales to prevent reproductive costs accumulating, whereas fast-paced individuals should allow costs to accumulate (i.e. senescence). Using Fourier transforms, we quantify adjustments in clutch size with age, across four populations of blue tits (Cyanistes caeruleus). Fast populations had more prevalent and stronger long-term changes in reproductive investment, whereas slower populations had more prevalent short-term adjustments. Inter-annual environmental variation partly accounted for short-, but not long-term changes in reproductive investment. Our study reveals individuals differ in when they pay the cost of reproduction and that failure to partition this variation across different temporal scales and environments could underestimate reproductive trade-offs.

Quantifying heritability and estimating evolutionary potential in the wild when individuals that share genes also share environments.

Accurate heritability estimates for fitness-related traits are required to predict an organism's ability to respond to global change. Heritability estimates are theoretically expected to be inflated if, due to limited dispersal, individuals that share genes are also likely to share similar environments. However, if relatives occupy similar environments due, at least partly, to genetic variation for habitat selection, then accounting for environmental similarity in quantitative genetic models may result in diminished heritability estimates in wild populations. This potential issue has been pointed out in the literature, but has not been evaluated by empirical studies. Here, we investigate whether environmental similarity among individuals can be partly explained by genetic variation for habitat selection, and how this link potentially blurs estimates for heritability in fitness-related traits. Using intensive GPS monitoring, we quantified home-range habitat composition for 293 roe deer inhabiting a heterogeneous landscape to assess environmental similarity. To investigate if environmental similarity might harbour genetic variation, we combined genome-wide data in a quantitative genetic framework to evaluate genetic variation for home-range habitat composition, which is partly the result of habitat selection at settlement. Finally, we explored how environmental similarity affects heritability estimates for behaviours related to the risk avoidance-resource acquisition trade-off (i.e. being in open habitat and distance to roads) and proxies of individual performance (i.e. body mass and hind foot length). We found substantial heritability for home-range habitat composition, with estimates ranging from 0.40 (proportion of meadows) to 0.85 (proportion of refuge habitat). Accounting for similarity in habitat composition between relatives decreased the heritability estimates for both behavioural and morphological traits (reduction ranging from 55% to 100% and from 22% to 41% respectively). As a consequence, only half of these heritability estimates remained significantly different from zero. Our results show that similar genotypes occupy similar environments, which could lead to heritable variation being incorrectly attributed to environmental effects. To accurately distinguish the sources of phenotypic variation and predict the ability of organisms to respond to global change, it is necessary to develop quantitative genetic studies investigating the mechanisms underpinning environmental similarity among relatives.

Sex, body size, and boldness shape the seasonal foraging habitat selection in southern elephant seals.

Selecting foraging habitat is a fundamental behavior in the life of organisms as it directly links resource acquisition to fitness. Differences in habitat selection among individuals may arise from several intrinsic and extrinsic factors, and yet, their interaction has been given little attention in the study of wild populations. We combine sex, body size, and boldness to explain individual differences in the seasonal foraging habitat selection of southern elephant seals (Mirounga leonina) from the Kerguelen Archipelago. We hypothesize that habitat selection is linked to the trade-off between resource acquisition and risk, and that individuals differ in their position along this trade-off because of differences in reproductive strategies, life stages, and metabolic requirements. Before the post-molt foraging trip, we used a novel object approach test to quantify the boldness of 28 subadult and adult females and 42 subadult males and equipped them with data loggers to track their movements at sea. Subadult males selected neritic and oceanic habitats, whereas females mostly selected less productive oceanic habitats. Both sexes showed a seasonal shift from Antarctic habitats in the south in the summer to the free of ice subantarctic and subtropical habitats in the north in the winter. Males avoided oceanic habitats and selected more productive neritic and Antarctic habitats with body size mostly in the winter. Bolder males selected northern warmer waters in winter, while shyer ones selected the Kerguelen plateau and southern colder oceanic waters. Bolder females selected the Kerguelen plateau in the summer when prey profitability is assumed to be the highest. This study not only provides new insights into the spatiotemporal foraging ecology of elephant seals in relation to personality but also emphasizes the relevance of combining several intrinsic and extrinsic factors in understanding among-individual variation in space use essential in wildlife management and conservation.

Linking genetic, morphological, and behavioural divergence between inland island and mainland deer mice.

The island syndrome hypothesis (ISH) stipulates that, as a result of local selection pressures and restricted gene flow, individuals from island populations should differ from individuals within mainland populations. Specifically, island populations are predicted to contain individuals that are larger, less aggressive, more sociable, and that invest more in their offspring. To date, tests of the ISH have mainly compared oceanic islands to continental sites, and rarely smaller spatial scales such as inland watersheds. Here, using a novel set of genome-wide SNP markers in wild deer mice (Peromyscus maniculatus) we conducted a genomic assessment of predictions underlying the ISH in an inland riverine island system: analysing island-mainland population structure, and quantifying heritability of phenotypes thought to underlie the ISH. We found clear genomic differentiation between the island and mainland populations and moderate to high marker-based heritability estimates for overall variation in traits previously found to differ in line with the ISH between mainland and island locations. FST outlier analyses highlighted 12 loci associated with differentiation between mainland and island populations. Together these results suggest that the island populations examined are on independent evolutionary trajectories, the traits considered have a genetic basis (rather than phenotypic variation being solely due to phenotypic plasticity). Coupled with the previous results showing significant phenotypic differentiation between the island and mainland groups in this system, this study suggests that the ISH can hold even on a small spatial scale.

Indirect genetic and environmental effects on behaviors, morphology, and life-history traits in a wild Eastern chipmunk population.

Additive genetic variance in a trait reflects its potential to respond to selection, which is key for adaptive evolution in the wild. Social interactions contribute to this genetic variation through indirect genetic effects-the effect of an individual's genotype on the expression of a trait in a conspecific. However, our understanding of the evolutionary importance of indirect genetic effects in the wild and of their strength relative to direct genetic effects is limited. In this study, we assessed how indirect genetic effects contribute to genetic variation of behavioral, morphological, and life-history traits in a wild Eastern chipmunk population. We also compared the contribution of direct and indirect genetic effects to traits evolvabilities and related these effects to selection strength across traits. We implemented a novel approach integrating the spatial structure of social interactions in quantitative genetic analyses, and supported the reliability of our results with power analyses. We found indirect genetic effects for trappability and relative fecundity, little direct genetic effects in all traits and a large role for direct and indirect permanent environmental effects. Our study highlights the potential evolutionary role of social permanent environmental effects in shaping phenotypes of conspecifics through adaptive phenotypic plasticity.

Bacterial microbiota similarity between predators and prey in a blue tit trophic network.

Trophic networks are composed of many organisms hosting microbiota that interact with their hosts and with each other. Yet, our knowledge of the factors driving variation in microbiota and their interactions in wild communities is limited. To investigate the relation among host microbiota across a trophic network, we studied the bacterial microbiota of two species of primary producers (downy and holm oaks), a primary consumer (caterpillars), and a secondary consumer (blue tits) at nine sites in Corsica. To quantify bacterial microbiota, we amplified 16S rRNA gene sequences in blue tit feces, caterpillars, and leaf samples. Our results showed that hosts from adjacent trophic levels had a more similar bacterial microbiota than hosts separated by two trophic levels. Our results also revealed a difference between bacterial microbiota present on the two oak species, and among leaves from different sites. The main drivers of bacterial microbiota variation within each trophic level differed across spatial scales, and sharing the same tree or nest box increased similarity in bacterial microbiota for caterpillars and blue tits. This study quantifies host microbiota interactions across a three-level trophic network and illustrates how the factors shaping bacterial microbiota composition vary among different hosts.

Collision between biological process and statistical analysis revealed by mean centring.

Animal ecologists often collect hierarchically structured data and analyse these with linear mixed-effects models. Specific complications arise when the effect sizes of covariates vary on multiple levels (e.g. within vs. among subjects). Mean centring of covariates within subjects offers a useful approach in such situations, but is not without problems. A statistical model represents a hypothesis about the underlying biological process. Mean centring within clusters assumes that the lower level responses (e.g. within subjects) depend on the deviation from the subject mean (relative) rather than on the absolute scale of the covariate. This may or may not be biologically realistic. We show that mismatch between the nature of the generating (i.e. biological) process and the form of the statistical analysis produce major conceptual and operational challenges for empiricists. We explored the consequences of mismatches by simulating data with three response-generating processes differing in the source of correlation between a covariate and the response. These data were then analysed by three different analysis equations. We asked how robustly different analysis equations estimate key parameters of interest and under which circumstances biases arise. Mismatches between generating and analytical equations created several intractable problems for estimating key parameters. The most widely misestimated parameter was the among-subject variance in response. We found that no single analysis equation was robust in estimating all parameters generated by all equations. Importantly, even when response-generating and analysis equations matched mathematically, bias in some parameters arose when sampling across the range of the covariate was limited. Our results have general implications for how we collect and analyse data. They also remind us more generally that conclusions from statistical analysis of data are conditional on a hypothesis, sometimes implicit, for the process(es) that generated the attributes we measure. We discuss strategies for real data analysis in face of uncertainty about the underlying biological process.

Age-dependent phenological plasticity in a wild bird.

Life-history traits are often plastic in response to environmental factors such as temperature or precipitation, and they also vary with age in many species. Trait variation during the lifetime could thus be partly driven by age-dependent plasticity in these traits. We study whether plasticity of a phenological trait-the egg-laying date-with respect to spring temperature, varies with age, and explore whether this variation relates to changes in breeding success throughout the life cycle. We use data from a four-decade long-term monitoring of a wild population of blue tits in Corsica, to estimate age-dependent plasticity of reproductive phenology and annual reproductive success. We show that both laying date plasticity and annual reproductive success vary with age: young and old females are less plastic, and fledge fewer offspring, than middle-age females. Furthermore, in contrast to young and prime-age females, in old females fledging success does not depend on laying date. Phenological plasticity is a major mechanism for coping with rapid environmental variation. Our results suggest that understanding its role in adaptation to climate change and population persistence requires integrating the age structure of the population.

Development and characterization of 14 microsatellites for the eastern chipmunk, Tamias striatus.

The number of microsatellite markers currently available for the eastern chipmunk Tamias striatus provides limited capacity to achieve sufficient pedigree building for the study of their genetic structure and relatedness patterns. We developed microsatellite loci for the eastern chipmunk, a small rodent commonly found in eastern North America. More specifically, we report data for 14 loci and 50 individuals genotyped from a population in southern Québec, Canada. We found a number of alleles ranging from 5 to 21 and there was no linkage disequilibrium among locus. One locus deviated from Hardy-Weinberg equilibrium and had a high proportion of null alleles. Those loci will be used in addition to previously developed loci to improve the precision of parentage assignment and population genetics studies on this species.

Individual and environmental determinants of Cuterebra bot fly parasitism in the eastern chipmunk (Tamias striatus).

Understanding the interactions between parasites, hosts, and their shared environment is central to ecology. Variation in infestation prevalence may be the result of varying environmental and population characteristics; however, variations in parasitism may also depend on individual characteristics that influence both the exposure and susceptibility to parasites. Using 12 years of data from a population of wild eastern chipmunks relying on pulsed food resources, we investigated the determinants of bot fly parasitism at both the population and individual level. We assessed the relationship between infestation prevalence and weather conditions, population size and food abundance. Then, we assessed the relationship between infestation intensity and chipmunk behavior, sex, age, body mass and food abundance. Precipitation, temperature and population size were positively related to infestation prevalence, while beech masts were negatively related to infestation prevalence, highlighting the importance of local environmental conditions on hosts and parasites. We also found that the influence of activity and exploration on infestation intensity varied according to sex in adults. More active and faster exploring males had more parasites compared to females, suggesting that reproductive behaviors may influence parasite exposure. For juveniles, infestation intensity was greater when juveniles emerged in the spring as opposed to fall, possibly because spring emergence is synchronized with the peak of bot fly eggs in the environment, low food availability and longer activity period. Our results suggest that the environmental, population and host characteristics that are advantageous for reproduction and resource acquisition may come at the cost of increasing parasitism.