Evolutionary theories predict that early-life reproductive effort should be favoured by selection at the cost of faster reproductive ageing, but empirical support for this trade-off remains mixed. Previous studies typically examined whether the rate of reproductive ageing varied among groups of individuals differing in early-life reproductive allocation. However, this approach assumes that all individuals have the same age at the onset of reproductive ageing. By analysing annual birth probabilities among women aged 16-50 years in a pre-industrial population of Nouvelle-France (Quebec, Canada), we showed reproductive ageing displayed high variability between mothers both in onset (n = 7346) and rate (n = 2663). Age at the onset of reproductive ageing varied nonlinearly with the number of children produced during early life. Regardless of sex, the first child born no later than 28 years advanced the onset of reproductive ageing by 914 ± 25 days and each additional child by 220 ± 7 days. An increasing number of children born by age 28 also accelerated the rate of reproductive ageing. These results highlight the value of individual trajectories in reproductive ageing studies and may improve understanding of how early-life reproduction influences late-life reproduction, especially in low-income countries with high birth rates.
Pollen provides a wealth of nutrients crucial to pollinators, including proteins, lipids, minerals, essential amino acids and fatty acids, vitamins, as well as flavonoids and phenols. However, pollen can be contaminated by some pesticides, pharmaceuticals, and heavy metals. There is an increasing need to characterize pollinator nutritional landscapes to implement efficient conservation measures and halt pollinator decline. However, the nutritional content of pollen is absent from most datasets on floral resources and floral traits, limiting our ability to characterize essential nutrients available in the landscape for pollinators. We reviewed the literature and provide a primary dataset on pollen nutrients of 283 plant species from 54 families. While data on proteins, lipids, and amino acids (with the exception of tryptophan) were available in the literature, information on other nutrients was scarce (e.g., for minerals, vitamins, fatty acids). Moreover, extensively characterized pollen belonged to food-producing plants, with important gaps for other flowering plants. To fill these gaps, we conducted a multidimensional assessment of 20 pollen samples from cultivated and wild plants by HPLC and mass-spectrometry (including 32 nutrients, 100 contaminants, and pollen imaging). We provide an open and dynamic database with results from this assessment-composed of nutrient and contaminant datasets and an imaging database-which will be updated over time with new species and locations. Practical implications: this database is anticipated to be used to (1) characterize pollinator nutritional landscape and (2) identify plants with nutritional value for pollinators and make recommendations for conservation management.
Mixtures of pesticides from agricultural runoff can affect non-targeted freshwater organisms and pose ecological risks even at low concentrations. Yet, ecotoxicity is rarely assessed using pesticide mixtures found at environmental concentrations under natural fluctuating habitat conditions. This study aimed at assessing the chronic toxicity of a pesticide mixture on the model species great pond snails (Lymnaea stagnalis) over a 40-day period using semi-natural outdoor mesocosms. The pesticide mixture was prepared to reflect environmental levels of agrochemicals commonly found in freshwater streams surrounding corn/soybean farming of southern Québec, Canada. It included seven pesticides (herbicides: atrazine, S-metolachlor, glyphosate; insecticides: clothianidin, thiamethoxam, imidacloprid, and chlorantraniliprole). These pesticides were tested at environmental concentrations, and at two and ten-fold reductions from these water concentrations to observe potential benefits from reduction in pesticide use. There was no effect of the pesticide mixture on overall snail survival. However, the 0.5× and 1× pesticide mixture increased average snail body mass by disproportionately decreased the proportion of smaller snails. Also, pesticide accumulation was highest in biofilm for atrazine (0.0014-0.0256 nmol/g wet wt), then s-metolachlor (0.0018-0.0126 nmol/g), glyphosate's metabolite aminomethylphosphonic acid (AMPA; 0.0002-0.0038 nmol/g) chlorantraniliprole (0.007 nmol/g), and lastly glyphosate (0.0006 nmol/g). Bioaccumulation was highest in snails for S-metolachlor (0.0185-0.0467 nmol/g wet wt), then atrazine (0.0049-0.0246 nmol/g), AMPA (0.0002-0.0074 nmol/g), chlorantraniliprole (0.0005-0.0025 nmol/g), glyphosate (0.0010-0.0021 nmol/g), imidacloprid (0.0003-0.0005 nmol/g), and lastly clothianidin (0.0001 nmol/g). We found that concentrations of pesticides in snails were determined by an interaction between biofilm pesticide concentrations and water pesticide concentrations. Our results highlight that pesticide mixtures under semi-natural conditions can produce complex interacting effects on non-target organism's body mass and bioaccumulation of chemicals that could be considered when establishing pesticide-usage policies.
Survival and reproductive success are greatly influenced by how an individual uses its surrounding environment, which can differ across spatial scales. To better understand the habitat-fitness relationships of animals, it is essential to study space use at multiple spatial scales. Here, we used 13 years of capture-mark-recapture and burrow location data to investigate how two different aspects of space use influence the survival and female reproduction in a wild population of eastern chipmunks (Tamias striatus) in southern Québec. We quantified home range size and site fidelity in a population experiencing massive inter-annual variations in food availability due to the masting of American beech trees (Fagus grandifolia). We found that site fidelity tended to increase the probability of reproduction but that this effect was strongly dependent on the context of beech seed production: probability of reproduction was higher for females that were faithful from a mast year to the following non-mast year. Site fidelity was not related to survival and we found no significant effect of home range size on either fitness trait. Our results indicate that, in our study system, different aspects of space use affect fitness traits in different ways. We emphasize the importance of examining multiple spatial scales in related analyses.
Mate choice and multiple paternity have been widely studied in natural populations, especially in research assessing inbreeding avoidance mechanisms. Ecological factors are expected to affect the costs and benefits of mate choice and multiple paternity, for instance, through their effects on the availability of partners. However, the relative importance and variation of those costs/benefits across fluctuating environmental contexts remains to be established. Here, we used reproduction data collected over 18 years on a wild population of Eastern chipmunks (Tamias striatus) to assess the influence of relatedness among mating partners on their reproductive success and on their offspring fitness in different breeding contexts. In southern Québec, chipmunks live in a pulse resource system where they anticipate masting events of the American beech (Fagus grandifolia) and breed during the summer preceding and/or the spring following a mast. We found that, within a litter, less genetically related sires were assigned more offspring than more closely related ones. This relationship was significant during the summer breeding seasons only, which is characterized by high availability of food and mating partners in the environment. Multiple paternity was also more frequent during summer breeding than during spring breeding. We found no additional effect of parental relatedness on the juvenile survival, longevity, or reproductive success of their offspring. Our results could suggest the presence of context-specific inbreeding avoidance mechanisms by females or differential mortality of offspring at early stages linked to inbreeding depression. Altogether, our findings provide a better understanding of the influence of fluctuating environments on reproduction in small mammals.
ABSTRACT Small mammals inhabiting pulsed‐resource environments, such as forests with intermittent seed masting of trees, often adjust their allocation to reproduction with the drastic fluctuations in food availability. They could, for instance, plastically allocate capital resources to reproduction when food availability is low or adopt an income breeding strategy when food availability is high. We investigated how eastern chipmunks (Tamias striatus), a food‐hoarding rodent strongly relying on the masting of beech trees (Fagus grandifolia), anticipate and respond to food pulses to reproduce. We supplemented a study site with sunflower seeds to buffer food availability for 2 years that were characterized by a non‐mast and a beech mast. We monitored chipmunks exploitation of the feeders, body mass, and reproductive activity. We tested if food‐supplemented females would reproduce in the absence of a beech mast. We compared those results with two control sites and 10 years of data on chipmunk reproduction. The probability of summer estrus significantly increased with the exploitation of feeders compared to the controls. Exploiting the feeders had a stronger effect than body mass on the probability of estrus. Still, beech masting had a broader effect on the probability of estrus across all sites than exploiting the feeders. Although most supplemented females showed oestrus during the non‐mast year, as opposed to non‐supplemented females, they did not fully reproduce despite their favorable body condition and the extensive hoard they accumulated. Those results suggest that summer reproduction in eastern chipmunks is not only financed by current food availability, revealing the complexity of plastic resource allocation in fluctuating environments.
Individual exploration types are based on the cognitive speed-accuracy trade-off, which suggests that a higher speed of information acquisition is done by sacrificing information quality. In a mating context, fast exploration could thus increase the probability of finding mates at the cost of mating with kin or suboptimal partners. We tested this hypothesis by studying male mate choice patterns in a species with a scramble competition mating system. We used genotyping, localization by radio-collar, trapping, and repeated exploration measures from a long-term study on wild Eastern chipmunks (Tamias striatus). We predicted that, according to the speed-accuracy trade-off hypothesis, slower-thorough explorers should be choosier than faster-superficial ones, and thus avoid inbreeding. We found that slower males reproduced more often with less related females, but only on one site where variance in relatedness and female density were high. Males showed no preference for their mates' exploration type. Our results suggest that superficial exploration decreases male choosiness and increases the risk of inbreeding, but only under decreased mate search costs due to high variance in relatedness among mates (at high density). Our findings reveal exploration-related, among-individual variance in inbreeding, highlighting the complexity of mate choice, and showing that many aspects of an individual's life contribute to animal decision-making. In many species, males can be choosy about their mates. Here, we investigated if personality-measured over a slow-thorough/fast-superficial continuum-was related to mate selection in Eastern chipmunks. We show that, contrary to superficial males, males that explore a novel environment thoroughly reproduced more with less genetically related females. In our studied population, such patterns were context-dependent and found only when variance in genetic relatedness was high, at high female density.
An increasing number of wild bee species are declining or threatened with extinction worldwide. Decline has been proposed to be caused by a combination of threats, including increasing wild bee disease prevalence and pathogen spillover from managed bees that can reduce health of wild bees. Most approaches aiming at characterizing bee health, however, require sacrificing tens to hundreds of individual bees per site or species, with reports of several thousand individuals collected per study. Considering the widespread need to assess bee health, this sampling approach is not sustainable, especially for endangered populations or species. Here, we present a non-destructive protocol to collect bumble bee faeces and assess parasite loads of wild-caught individuals. The standard protocol consists of net-capturing individual bumble bees and placing them in a 10 cm (diameter) petri dish to collect faeces. This fecal screening approach is frequently used in laboratory settings, but much less in the field, which can impair conservation research. When placing bumble bees in a previously refrigerated cooler, we successfully collected faeces for 86% individuals, while the standard protocol, as used in laboratory settings, yielded 76% success in collecting faeces. We also identified cells and spores of two common gut parasites Crithidia spp. and Vairimorpha spp. in faecal samples. The faecal sampling presented here opens future avenues to assess bee pathogen loads using molecular techniques, while collected faeces could also be used to assess bee health more broadly, including bee microbiota and bee diet.
In dimorphic vertebrates where males are larger than females, the energetic costs of producing and rearing sons can exceed those of daughters. In humans, differences in maternal energy intake suggest that sons require 10% and 7% more energy than daughters during pregnancy and lactation, respectively. Due to a trade-off between reproduction and somatic maintenance, having sons is expected to have a more pronounced detrimental impact on a mother's lifespan than having daughters. A limitation of previous studies investigating this hypothesis is that the increased mortality cost of having sons was assumed to affect all mothers equally. Using a dataset from a preindustrial Quebec population monitored over two centuries, we found that the number of sons decreased postmenopausal lifespan only in mothers experiencing high infant mortality. Our study highlights the importance of interindividual variation in environmental conditions and maternal health when studying effects of offspring sex on reproductive costs.
Early life environments can have long-lasting effects on adult reproductive performance, but disentangling the influence of early and adult life environments on fitness is challenging, especially for long-lived species. Using a detailed dataset spanning over two centuries, we studied how both early and adult life environments impacted reproductive performance in preindustrial women. Due to a wide geographic range, agricultural production was lower in northern compared to southern parishes, and health conditions were worse in urban than rural parishes. We tested whether reproductive traits and offspring survival varied between early and adult life environments by comparing women who moved between different environments during their lifetime with those who moved parishes but remained in the same environment. Our findings reveal that urban-born women had an earlier age at first reproduction and less offspring surviving to adulthood than rural-born women. Moreover, switching from urban to rural led to increased offspring survival, while switching from rural to urban had the opposite effect. Finally, women who switched from rural to urban and from South to North had their first child at an older age compared to those who stayed in the same environment type. Our study underscores the complex and interactive effects of early and adult life environments on reproductive traits, highlighting the need to consider both when studying environmental effects on reproductive outcomes.
Senescence is the degradation of biological functions with increasing age. Its existence and relationship with life‐history strategies remains poorly studied in short‐lived wild vertebrate species. We investigated the relationships between age at first reproduction (AFR), reproductive senescence and longevity in an eastern chipmunk Tamias striatus population, where the first opportunity to breed is conditioned by pulses of seed production by trees (i.e. masts). We used 11 years of data from a longitudinal study, in which females breed for the first time at seven, 15 or 22 months of age and males at seven or 15 months of age. We first assessed the effect of age on three traits associated with breeding performance, namely the number of offspring produced, and the probability of producing an offspring. We then tested whether an earlier AFR accelerated reproductive senescence and reduced survival of both males and females. We found sex‐specific relationships between AFR and senescence. Females reproducing at 15 or 22 months of age showed reproductive senescence, but early‐breeding females did not show any decline in reproductive performance at an older age. Also, although we observed reproductive senescence in males, it was not affected by AFR. Our results are consistent with studies highlighting the existence of reproductive senescence in small, wild mammals. Importantly, we provide the first evidence that AFR can strongly influence the patterns of senescence in small short‐lived species, and does it in a sex‐specific way. Our results highlight the importance of studying life‐history strategies in both males and females when studying senescence in the wild.
Abstract Wild bees are declining worldwide, and many species are now threatened with extinction. Decline is caused by a combination of threats, including disease spillover from managed bees that reduces health of wild bees. An increasing number of studies thus aim to characterize bee health. The common approaches, however, require sacrificing tens to hundreds of individual bees per site or species, with reports of several thousand individuals collected per study. Considering the widespread need to assess bee health, this sampling approach is not sustainable, especially for endangered populations or species. Here, we propose a non-destructive method to assess parasite loads of wild-caught bumble bees. The standard protocol consists of net-capturing individual bumble bees and placing them in a 10 cm (diameter) petri dish to collect faeces. Although this approach is frequently used in laboratory settings, it is not in the field, because of the low success in collecting faeces. Placing bumble bees in a previously refrigerated cooler, we significantly improved faecal collection in the field from 76% with the standard protocol to 86% with the cooler protocol. We also successfully identified spores and cells of two common gut parasites Crithidia spp. and Vairimorpha spp. in faecal samples. The efficacy of the cooler protocol, combined to the low-cost and widespread availability of the equipment should promote its use in field studies. Implication for insect conservation: As there are calls to reduce destructive sampling methods in bee research, using the updated cooler protocol will contribute to achieving this goal. This opens future avenues of combining this non-destructive approach to assess bee health with molecular tools.
BackgroundHabitat 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.MethodsWe 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.ResultsOur 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.ConclusionThe 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.
Early life environments can have long-lasting effects on adult reproductive performance, but disentangling the influence of early and adult life environments on fitness is challenging, especially for long-lived species. Using a detailed dataset spanning over two centuries, we studied how early and adult life environments impact reproductive performance in preindustrial women. We assessed the effect of environmental conditions associated with the parish of birth and the parish where the women had their offspring. We considered resource availability differences between rural, urban, northern, and southern parishes by comparing women who switched environments during their lifetime with those who did not. We found that urban-born women had an earlier age at first reproduction and lower offspring survival to adulthood than rural-born women, while South Québec women had more offspring born than North Québec women. Moreover, switching from urban to rural led to higher offspring survival, while the reverse had the opposite effect. In addition, moving from South to North resulted in fewer offspring born and surviving, whereas moving from North to South had the inverse effect. Finally, women who changed from rural to urban and from South to North had their first child at an older age compared to those who stayed in the same urbanity type. Our study underscores the complex and interactive effects of early and adult life environments on reproductive traits, highlighting the need to consider both when studying environmental effects on reproductive outcomes.
Pesticides and climate change are both thought to contribute to the global amphibian decline, yet their combined effects are still poorly understood. Metolachlor is a widespread herbicide applied across North America, but little is known about its effects on amphibians. We used a replicated mesocosm experimental design with different levels of drying (i.e., no drying and medium and rapid drying) and metolachlor concentrations (0, 0.8, 8, and 80 µg/L) to assess their respective and combined effects on wood frog (Lithobates sylvaticus) larvae throughout metamorphosis. Metolachlor had no significant effect on survival and development of tadpoles. However, metolachlor significantly interacted with drying levels to reduce the growth of tadpoles, which was mainly due to a difference detected among metolachlor concentrations under the rapid drying treatment. Drying also directly reduced growth and body mass at metamorphosis. Our results suggest that environmental stressors, such as drying, should be considered in toxicological experiments to provide relevant exposure conditions to pesticides for ephemeral pond species in the context of global climate change. Environ Toxicol Chem 2023;42:1772–1781. © 2023 SETAC
In dimorphic vertebrates where males are larger than females, the energetic costs of producing and rearing sons can exceed those of daughters. In humans, differences in maternal energy intake suggest that sons require 10% and 7% more energy than daughters during pregnancy and lactation, respectively. Due to trade-off between reproductive expenditure and somatic maintenance, having sons is thus expected to have a much-pronounced detrimental impact on mother’s lifespan than having daughters. However, this question has led to mixed results and lively debates in the literature. A major limitation of previous studies is that the increased mortality costs of having sons were assumed to be fairly homogeneous across mothers. Using an exceptionally detailed dataset from a preindustrial Quebec population, we found that the relationship between the proportion of sons and maternal post-menopausal lifespan varies as a function of the family environment. Within families exposed to high infant mortality indicating a poor environment, women lived shorter and each son born or reared decreased post-menopausal lifespan by 182 or 264 days, respectively. On the contrary, there was no evidence for an effect of the sons’ proportion on lifespan for mothers that lived in favourable environments. Our results bear significant evolutionary implications since grandmothers allowed their daughters to increase their number of children born in this population. These results highlight the crucial role of inter-individual variation in environmental conditions when studying the effects of offspring sex on parental health and fitness.
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.
Phenotypic 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.