Long-term Fitness Consequences Research Articles

Long-term effects of litter characteristics on reproduction in female cavies (Cavia aperea)

In mammals, birth mass is an important predictor of early growth and survival. Within litters, heavier siblings are usually able to outcompete smaller siblings and gain more resources, thereby often permanently shaping phenotypic development. Early body size and growth are particularly important for later fitness. Only few studies investigated if and how differences within the early family environment contribute to long-term variation in fitness among individuals. We quantified if initial differences in size translate to size differences in adulthood and whether birth mass, relative size within the litter, litter size or the litter sex-ratio affect maturation and reproductive output of female wild cavies (Cavia aperea). Initial differences in mass were maintained until animals reached maximum adult mass at two years of age. Heavier sisters matured earlier and invested more into their first litter than smaller sisters, presumably because smaller sisters invested more into their own growth during the first pregnancy. Growing up in mixed-sexed litters in comparison to female-only litters slowed down maturation in smaller but not the heaviest female within a litter and had no effect on female reproductive effort. Variation in reproduction of multiparous females was to a lesser extent explained by the initial relative size of siblings. Offspring survival to independence was high but slightly lower when mothers had been born as smaller sisters. Our results demonstrate that factors of the early family environment not only affect immediate offspring development but lead to long-term fitness consequences.

A colonial-nesting seabird shows limited heart rate responses to natural variation in threats of polar bears.

Several predator-prey systems are in flux as an indirect result of climate change. In the Arctic, earlier sea-ice loss is driving polar bears (Ursus maritimus) onto land when many colonial nesting seabirds are breeding. The result is a higher threat of nest predation for birds with potential limited ability to respond. We quantified heart rate change in a large common eider (Somateria mollissima) breeding colony in the Canadian Arctic to explore their adaptive capacity to keep pace with the increasing risk of egg predation by polar bears. Eiders displayed on average higher heart rates from baseline when polar bears were within their field of view. Moreover, eiders were insensitive to variation in the distance bears were to their nests, but exhibited mild bradycardia (lowered heart rate) the longer the eider was exposed to the bear given the hen's visibility. Results indicate that a limited ability to assess the risks posed by polar bears may result in long-term fitness consequences for eiders from the increasing frequency in interactions with this predator.

Early-life diet specificity is associated with long-lasting differences in apparent survival in a generalist predator.

Early-life conditions can have long-term fitness consequences. However, it is still unclear what optimal rearing conditions are, especially for long-lived carnivores. A more diverse diet ('balanced diet') might optimize nutrient availability and allow young to make experiences with a larger diversity of prey, whereas a narrow diet breadth ('specialized diet') might result in overall higher energy net gain. A diet that is dominated by a specific prey type (i.e. fish, 'prey type hypothesis') might be beneficial or detrimental, depending for example, on its toxicity or contaminant load. Generalist predators such as the white-tailed eagle Haliaeetus albicilla provide an interesting possibility to examine the relationship between early life diet and long-term offspring survival. In the Åland Islands, an archipelago in the Baltic Sea, white-tailed eagles live in various coastal habitats and feed on highly variable proportions of birds and fish. We use data from 21,116 prey individuals that were collected from 120 territories during the annual surveys, to examine how early-life diet is associated with apparent annual survival of 574 ringed and molecular-sexed eaglets. We supplement this analysis by assessing the relationships between diet, reproductive performance and nestling physical condition, to consider whether they are confounding with possible long-term associations. We find that early-life diet is associated with long-term fitness: Nestlings that are fed a diverse diet are in lower physical condition but have higher survival rates. Eagles that are fed more fish as nestlings have lower survival as breeding-age adults, but territories associated with fish-rich diets have higher breeding success. Our results show that young carnivores benefit from a high diversity of prey in their natal territory, either through a nutritional or learning benefit, explaining the higher survival rates. The strong relationship between early-life diet and adult survival suggests that early life shapes adult foraging decisions and that eating fish is associated with high costs. This could be due to high levels of contaminants or high competition for fish-rich territories. Long-lasting consequences of early-life diet are likely not only limited to individual-level consequences but have the potential to drive eco-evolutionary dynamics in this population.

Chill out: Environmentally relevant cooling challenge does not increase telomere loss during early life

In vertebrates, exposure to diverse stressors during early life activates a stress response that can initiate compensatory mechanisms or promote cellular damage with long-term fitness consequences. A growing number of studies associate exposure to stressors during early life with increased damage to telomeres (i.e., promoting the shortening of these highly conserved, repeating sequences of non-coding DNA at chromosome ends). However, some studies show no such relationship, suggesting that the nature, timing, and context of these challenges may determine the degree to which physiological mediators of the stress response act in a damage-mitigating or damage promoting way in relation to telomere dynamics. In free-living eastern bluebirds (Sialia sialis), we have previously demonstrated that bouts of offspring cooling that occur when brooding females leave the nest increase at least one such physiological mediator of the stress response (circulating glucocorticoids), suggesting that variation in patterns of maternal brooding may result in different impacts on telomere dynamics at a young age. Here we experimentally tested whether repeated bouts of ecologically relevant offspring cooling affected telomere dynamics during post-natal development. Rates of telomere shortening during the nestling stage were not affected by experimental cooling, but they were affected by brood size and the rate of growth during the nestling stage. Our data suggest that the effects of developmental stress exposure on offspring telomeres are often context-dependent and that not all challenges that increase physiological mediators of stress result in damage to telomeres. Under some conditions, physiological mediators of stress may instead act as protective regulators, allowing for optimization of fitness outcomes in the face of environmental challenges.

An invasive prey provides long-lasting silver spoon effects for an endangered predator.

The natal environment can have long-term fitness consequences for individuals, particularly via ‘silver spoon’ or ‘environmental matching’ effects. Invasive species could alter natal effects on native species by changing species interactions, but this potential remains unknown. Using 17 years of data on 2588 individuals across the entire US breeding range of the endangered snail kite (Rostrhamus sociabilis), a wetland raptor that feeds entirely on Pomacea snails, we tested for silver spoon and environmental matching effects on survival and movement and whether the invasion of a non-native snail may alter outcomes. We found support for silver spoon effects, not environmental matching, on survival that operated through body condition at fledging, explained by hydrology in the natal wetland. When non-native snails were present at the natal site, kites were in better condition, individual condition was less sensitive to hydrology, and kites fledged across a wider range of hydrologic conditions, leading to higher survival that persisted for at least 10 years. Movement between wetlands was driven by the current (adult) environment, and birds born in both invaded and uninvaded wetlands preferred to occupy invaded wetlands post-fledging. These results illustrate that species invasions may profoundly impact the role of natal environments on native species.

Tree Species Diversity and Forest Edge Density Jointly Shape the Gut Microbiota Composition in Juvenile Great Tits (Parus major).

Despite the microbiome’s key role in health and fitness, little is known about the environmental factors shaping the gut microbiome of wild birds. With habitat fragmentation being recognised as a major threat to biological diversity, we here determined how forest structure influences the bacterial species richness and diversity of wild great tit nestlings (Parus major). Using an Illumina metabarcoding approach which amplifies the 16S bacterial ribosomal RNA gene, we measured gut microbiota diversity and composition from 49 great tit nestlings, originating from 23 different nests that were located in 22 different study plots across a gradient of forest fragmentation and tree species diversity. Per nest, an average microbiome was determined on which the influence of tree species (composition and richness) and forest fragmentation (fragment area and edge density) was examined and whether this was linked to host characteristics (body condition and fledging success). We found an interaction effect of edge density with tree species richness or composition on both the microbial richness (alpha diversity: Chao1 and Shannon) and community structure (beta diversity: weighted and unweighted UniFrac). No significant short-term impact was observed of the overall faecal microbiome on host characteristics, but rather an adverse effect of specific bacterial genera on fledging success. These results highlight the influence of environmental factors on the microbial richness as well as the phylogenetic diversity during a life stage where the birds’ microbiota is shaped, which could lead to long-term consequences for host fitness.

Variation in growth patterns of Marsh Harrier Circus aeruginosus nestlings: effects of hatching order, nestling subperiod, brood size and weather conditions

Post-natal growth has long-term consequences for survival and fitness in birds and is subject to strong directional selection. Highly variable patterns of nestling development are influenced by an array of extrinsic and intrinsic factors. This study analysed the impacts of hatching order, nestling subperiod, brood size and weather conditions, all of which could influence the growth rate of Marsh Harrier Circus aeruginosus nestlings. It was conducted over a period of 6 years, during which measurements of 173 nestlings from 66 nests were made at fishpond complexes in eastern Poland. Relative growth rates (RGR) were calculated on the basis of tarsus and wing lengths during two subperiods of nestling development. Linear mixed models showed that the hatching order and nestling subperiod influenced nestling growth, whereas brood size did not affect wing or tarsus relative growth rates. The effect of hatching order differed between the two traits and between subperiods. Marginal nestlings in broods of five exhibited poor wing growth and perished before fledging. In contrast to wing growth, tarsus growth rates were similar in all the siblings in the first subperiod. During the second developmental subperiod, the growth rates of both locomotor traits exhibited the same pattern, i.e., higher values in the later-hatched chicks than in the earlier ones. Precipitation, but not temperature, had a negative impact on growth in the second subperiod. Our results show a variation in growth patterns between nestmates, which was the most evident in the rate of wing growth. The study enhances our understanding of brood reduction and cainism in birds of prey.

Thyroid disruption and oxidative stress in American kestrels following embryonic exposure to the alternative flame retardants, EHTBB and TBPH

Brominated flame retardant chemicals, such as 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (EHTBB) (CAS #: 183658-27-7) and bis(2-ethylhexyl)-2,3,4,5-tetrabromophthalate (TBPH) (CAS #: 26040-51-7), have been detected in avian tissues and eggs from remote regions. Exposure to EHTBB and TBPH has been shown to cause oxidative stress and altered thyroid function in rodents and fish, yet no controlled studies have examined potential adverse effects of exposure in birds. Because flame retardants have been detected in wild raptors, we used American kestrels (Falco sparverius) as a model raptor to determine whether in ovo exposure to EHTBB or TBPH affected growth, hatching success, oxidative stress, or thyroid function. We exposed kestrel embryos to nominal concentrations (10, 50, or 100ngg-1 egg weight) of EHTBB and TBPH via egg-injection on embryonic day 5. Embryonic exposure (~23 d) to EHTBB increased thyroid gland mass, reduced glandular colloid and total thyroxine (T4) in hatchling males and females, whereas deiodinase enzyme activity increased in males but decreased in females. Hatchlings exposed to TBPH in ovo exhibited reduced colloid and increased oxidative stress. Although exposure to EHTBB and TBPH caused several physiological effects (e.g., heart and brain mass), only exposure to 50ngg-1 EHTBB appeared to reduce hatching success. Our results suggest these flame retardants may be hazardous for predatory birds. Future research should evaluate long-term survival and fitness consequences in birds exposed to these chemicals.

Effects of maternal exposure to a bacterial antigen and altered post-hatching rearing conditions on avian offspring behaviour

The early-life environment plays a crucial role in shaping morphological, physiological, and behavioural traits, with potential long-term consequences for fitness. Indeed, a set of factors experienced by offspring during prenatal and early post-natal development has been recognised to affect behavioural trait expression in later life. Several studies have shown that in birds, nutritional and social rearing conditions and maternal and/or neonatal immunisations may profoundly determine the development and establishment of behaviour in offspring. To our knowledge, no research has examined whether and how the interaction between immune-mediated maternal effects and post-hatching rearing conditions affects offspring behaviour. Here, we studied the effects of maternal exposure to a bacterial antigen and altered brood size on docility, breathing rate, and aggression in the offspring of great tit, Parus major. We used a 2 × 2 design to investigate the interactive effects of maternal immunisation and brood size manipulation on offspring behavioural development. We found no such interactive effect on offspring behaviour, although we observed it regarding to offspring body mass and tarsus length. Maternal immunisation itself did not affect offspring behaviour. However, we demonstrated that the offspring breathing rate and level of aggression were affected by brood size manipulation. Both breathing rate and aggression in offspring reared in enlarged broods were lower than those in offspring reared in non-manipulated broods. Our study did not confirm earlier reports that immune-mediated maternal effects modulate offspring behavioural development, but we showed that brood size during rearing might indeed be a factor that affects offspring behaviour.Significance statementThe early environment experienced by offspring constitutes a significant source of developmental plasticity, which may profoundly affect the establishment of their behavioural traits. Food availability, social conditions, and maternal or offspring infection are crucial factors shaping various behavioural traits in birds. However, there remains a lack of studies emphasising the potential interactive effects of early-life conditions on behavioural trait development in natural bird populations. Here, to our knowledge for the first time, we experimentally examined how maternal immunisation and altered post-hatching rearing conditions interact to determine the behaviour of fledged offspring. We found that maternal treatment and brood size manipulation interactively affected offspring body mass and tarsus length, but this interaction had no effect on offspring behaviour. Our findings suggest that different mechanisms may underlie the development of morphological and behavioural traits.

Short-term behavioural impact contrasts with long-term fitness consequences of biologging in a long-lived seabird

Biologging has emerged as one of the most powerful and widely used technologies in ethology and ecology, providing unprecedented insight into animal behaviour. However, attaching loggers to animals may alter their behaviour, leading to the collection of data that fails to represent natural activity accurately. This is of particular concern in free-ranging animals, where tagged individuals can rarely be monitored directly. One of the most commonly reported measures of impact is breeding success, but this ignores potential short-term alterations to individual behaviour. When collecting ecological or behavioural data, such changes can have important consequences for the inference of results. Here, we take a multifaceted approach to investigate whether tagging leads to short-term behavioural changes, and whether these are later reflected in breeding performance, in a pelagic seabird. We analyse a long-term dataset of tracking data from Manx shearwaters (Puffinus puffinus), comparing the effects of carrying no device, small geolocator (GLS) devices (0.6% body mass), large Global Positioning System (GPS) devices (4.2% body mass) and a combination of the two (4.8% body mass). Despite exhibiting normal breeding success in both the year of tagging and the following year, incubating birds carrying GPS devices altered their foraging behaviour compared to untagged birds. During their foraging trips, GPS-tagged birds doubled their time away from the nest, experienced reduced foraging gains (64% reduction in mass gained per day) and reduced flight time by 14%. These findings demonstrate that the perceived impacts of device deployment depends on the scale over which they are sought: long-term measures, such as breeding success, can obscure finer-scale behavioural change, potentially limiting the validity of using GPS to infer at-sea behaviour when answering behavioural or ecological questions.

Juvenile rank acquisition is associated with fitness independent of adult rank.

Social rank is a significant determinant of fitness in a variety of species. The importance of social rank suggests that the process by which juveniles come to establish their position in the social hierarchy is a critical component of development. Here, we use the highly predictable process of rank acquisition in spotted hyenas to study the consequences of variation in rank acquisition in early life. In spotted hyenas, rank is 'inherited' through a learning process called 'maternal rank inheritance.' This pattern is very consistent: approximately 80% of juveniles acquire the exact rank expected under the rules of maternal rank inheritance. The predictable nature of rank acquisition in these societies allows the process of rank acquisition to be studied independently from the ultimate rank that each juvenile attains. In this study, we use Elo-deviance scores, a novel application of the Elo-rating method, to calculate each juvenile's deviation from the expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition among juveniles, most of these juveniles come to attain the exact rank expected of them according to the rules of maternal rank inheritance. Nevertheless, we find that transient variation in rank acquisition in early life is associated with long-term fitness consequences for these individuals: juveniles 'underperforming' their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers, and this relationship is independent of both maternal rank and rank achieved in adulthood. We also find that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness. Future work is needed to determine if variation in rank acquisition directly affects fitness, or if some other variable, such as maternal investment or juvenile condition, causes variation in both of these outcomes.

Subtle short-term physiological costs of an experimental augmentation of fleas in wild Columbian ground squirrels.

Parasites affect many aspects of host physiology and behavior, and thus are generally thought to negatively impact host fitness. However, changes in form of short-term parasite effects on host physiological markers have generally been overlooked in favor of fitness measures. Here, we studied flea (Oropsylla idahoensis and Oropsylla opisocroistis tuberculata) parasitism on a natural population of Columbian ground squirrels (Urocitellus columbianus) in Sheep River Provincial Park, AB, Canada. Fleas were experimentally added to adult female U. columbianus at physiologically demanding times, including birth, lactation and weaning of their young. The body mass of adult females, as well as their oxidative stress and immunity were recorded multiple times over the active season under flea-augmented and control conditions. We also measured the prevalence of an internal parasite (Trypanosoma otospermophili). Doubly labeled water (DLW) was intra-peritoneally injected at peak lactation to examine energy expenditure. Effects of parasites on oxidative stress were only observed after offspring were weaned. There was no direct effect of experimentally heightened flea prevalence on energy use. A short-term 24 h mass loss (-17 g) was detected briefly after parasite addition, likely due to U. columbianus preferentially allocating time for grooming. Our parasite augmentation did not strongly affect hosts and suggested that short-term physiological effects were unlikely to culminate in long-term fitness consequences. Columbian ground squirrels appear to rapidly manage parasite costs, probably through grooming.

Long-term fitness consequences of breeding density in starling colonies: an observational approach

Understanding the evolution of gregarious breeding in birds necessitates assessing how fitness components vary in relation to conspecific density. So far, the ultimate causes of breeding density remain contentious, owing to the logistic challenges in both obtaining and interpreting long-term effects of density on fledgling survival, recruitment rates or natal dispersal in wild populations. Here, we used observational data from a 13-year study on the reproduction of a facultatively gregarious bird, the Spotless Starling, Sturnus unicolor, to investigate the consequences of breeding density for fitness and offspring natal dispersal. We compared breeding performance, recruitment success and dispersal distances of offspring arising from nest-boxes placed in either a high (HD) or a low density (LD). We found that although neither clutch size nor fledgling survival varied in relation to density, HD nests produced significantly fewer recruits. Moreover, recruits from HD nests settled closer to their natal territories than those from LD nests. These findings suggest that the proximity to neighbours incurs delayed fitness costs in the Spotless Starling. Furthermore, the negative density-dependent dispersal may result from the increased mortality of individuals in worse condition and with lower ability to compete for breeding vacancies in the vicinity of their natal territories. With this study, we provide long-term observational results that may be a basis for further experiments intended to unravel proximate mechanisms underpinning density-dependent patterns in wild breeding colonies.

Life history shapes variation in egg composition in the blue tit Cyanistes caeruleus

Maternal investment directly shapes early developmental conditions and therefore has long-term fitness consequences for the offspring. In oviparous species prenatal maternal investment is fixed at the time of laying. To ensure the best survival chances for most of their offspring, females must equip their eggs with the resources required to perform well under various circumstances, yet the actual mechanisms remain unknown. Here we describe the blue tit egg albumen and yolk proteomes and evaluate their potential to mediate maternal effects. We show that variation in egg composition (proteins, lipids, carotenoids) primarily depends on laying order and female age. Egg proteomic profiles are mainly driven by laying order, and investment in the egg proteome is functionally biased among eggs. Our results suggest that maternal effects on egg composition result from both passive and active (partly compensatory) mechanisms, and that variation in egg composition creates diverse biochemical environments for embryonic development.

Reduced telomere length in embryos exposed to predator cues.

It is often assumed that embryos are isolated from external influences, but recent studies indicate that environmental stressors during prenatal stages can exert long-term negative effects on fitness. A potential mechanism by which predation risk may lastingly shape life-history traits and phenotypes is via effects on telomeres. However, whether prenatal exposure to environmental stressors, such as cues of predator presence, affects postnatal telomere length has not hitherto been investigated. Using an experimental design in which we modified the exposure of yellow-legged gull (Larus michahellis) embryos to social cues of predator presence (i.e. alarm calls), we show that prenatally exposed chicks had shorter telomeres after hatching. As young birds with shorter telomere lengths have reduced fledging success, reproductive success and lifespan, the reduced telomere length in the exposed chicks is likely to have long-term fitness consequences. Moreover, our results provide a mechanistic link through which predators may negatively affect population dynamics.

Heightened Immune System Function in Polar Bears Using Terrestrial Habitats.

Climate change is altering the distribution of some wildlife species while warming temperatures are facilitating the northward expansion of pathogens, potentially increasing disease risk. Melting of Arctic sea ice is increasingly causing polar bears (Ursus maritimus) of the southern Beaufort Sea (SBS) to spend summer on land, where they may encounter novel pathogens. Here, we tested whether SBS polar bears on shore during summer exhibited greater immune system activity than bears remaining on the sea ice. In addition, we tested whether the type of immune response correlated with body condition, because adaptive responses (slowly developing defenses against specific pathogens) often require less energy than innate responses (rapid defenses not based on pathogen identity). After accounting for body condition, we found that polar bears on shore exhibited higher total white blood cell counts, neutrophils, and monocytes than bears on the ice, suggesting more infections. Lymphocytes, eosinophils, basophils, and globulins did not differ. C-reactive protein, an indicator of inflammation, also did not differ between habitats. Body condition was associated with variables indicative of both innate and adaptive immunity, suggesting that neither response was uniquely limited by energy resources. Our data indicate that as more polar bears spend longer periods of time on shore, they may experience more infections. We encourage continued health monitoring of this species and studies of the long-term fitness consequences from disease.

Silver spoon effects of hatching order in an asynchronous hatching bird

The silver spoon hypothesis proposes that individuals which develop under favorable conditions will gain fitness benefits throughout their lifetime. Hatching order may create a considerable size hierarchy within a brood and lead to earlier-hatched nestlings having a competitive advantage over their siblings, which has been illustrated in some studies. However, there have been few explorations into the effect on subsequent generations. Here, using a 15-year-long study, we investigated the long-term fitness consequences of hatching order in the endangered crested ibis, Nipponia nippon, a species with complete hatching asynchrony. In this study, we found strong support for silver spoon effects acting on hatching order. Compared with later-hatched nestlings, first-hatched nestlings begin reproduction at an earlier age, have higher adult survival rates, possess a longer breeding life span, and achieve higher lifetime reproductive success. Interestingly, we found carry-over effects of hatching order into the next generation. Nestlings which hatched earlier and became breeders in turn also produced nestlings with larger tarsus and better body condition. Additionally, we found a positive correlation among life-history traits in crested ibis. Individuals which started reproduction at a younger age were shown to possess a longer breeding life span, and the annual brood size increased with an individual's breeding life span. This suggests that the earlier-hatched nestlings are of better quality and the silver spoon effects of hatching order cover all life-history stages and next generation effects.

Developmental stress and telomere dynamics in a genetically polymorphic species.

A central objective of evolutionary biology is understanding variation in life-history trajectories and the rate of aging, or senescence. Senescence can be affected by trade-offs and behavioural strategies in adults but may also be affected by developmental stress. Developmental stress can accelerate telomere degradation, with long-term longevity and fitness consequences. Little is known regarding whether variation in developmental stress and telomere dynamics contributes to patterns of senescence during adulthood. We investigated this question in the dimorphic white-throated sparrow (Zonotrichia albicollis), a species in which adults of the two morphs exhibit established differences in behavioural strategy and patterns of senescence, and also evaluated the relationship between oxidative stress and telomere length. Tan morph females, which exhibit high levels of unassisted parental care, display faster reproductive senescence than white females, and faster actuarial senescence than all of the other morph-sex classes. We hypothesized that high oxidative stress and telomere attrition in tan female nestlings could contribute to this pattern, since tan females are small and potentially at a competitive disadvantage even as nestlings. Nestlings that were smaller than nest mates had higher oxidative stress, and nestlings with high oxidative stress and fast growth rates displayed shorter telomeres. However, we found no consistent morph-sex differences in oxidative stress or telomere length. Results suggest that oxidative stress and fast growth contribute to developmental telomere attrition, with potential ramifications for adults, but that developmental oxidative stress and telomere dynamics do not account for morph-sex differences in senescence during adulthood.

Factors influencing individual participation during intergroup interactions in mountain gorillas

In group-living species, encounters with extragroup rivals can be one of the riskiest actions in which individuals participate. Different group members often have different incentives to participate during intergroup interactions, and individuals with fewer payoffs of competition, including those of the smaller sex and/or lower rank, may ‘free-ride’ to avoid the costs of conflict. However, there is little evidence for how different types of intergroup interactions (e.g. interactions that do not involve conflict) can influence the participation of individuals. We examined the ecological, demographic and social predictors of individual participation in interactions between 14 fully habituated mountain gorilla groups in Volcanoes National Park, Rwanda from 2003 to 2015. The probability of an individual participating decreased with group size but remained relatively high in aggressive interactions and in multimale groups, illustrating the potential for ‘load lightening’ among group members. Males with fewer mating opportunities participated less often than males with more mating opportunities; however, male participation was significantly higher than female participation across all types of intergroup interactions. Females were more likely to be involved in aggressive interactions with solitary males, possibly to avoid the potential cost of infanticide if a resident male is killed or injured. Both sexes demonstrated more affiliative behaviours towards familiar groups, indicating a benefit of maintaining social relationships with familiar groups. Individuals show considerable variation in behaviour during intergroup interactions, and our results suggest that this variation is primarily driven by intergroup familiarity and individual reproductive benefits, both of which may have long-term consequences for individual fitness.

Sulfoxaflor exposure reduces bumblebee reproductive success.

Intensive agriculture currently relies on pesticides to maximize crop yield1,2. Neonicotinoids are the most widely used insecticides globally3, but increasing evidence of negative impacts on important pollinators4-9 and other non-target organisms10 has led to legislative reassessment and created demand for the development of alternative products. Sulfoximine-based insecticides are the most likely successor11, and are either licensed for use or under consideration for licensing in several worldwide markets3, including within the European Union12, where certain neonicotinoids (imidacloprid, clothianidin and thiamethoxam) are now banned from agricultural use outside of permanent greenhouse structures. There is an urgent need to pre-emptively evaluate the potential sub-lethal effects of sulfoximine-based pesticides on pollinators11, because such effects are rarely detected by standard ecotoxicological assessments, but can have major impacts at larger ecological scales13-15. Here we show that chronic exposure to the sulfoximine-based insecticide sulfoxaflor, at dosages consistent with potential post-spray field exposure, has severe sub-lethal effects on bumblebee (Bombus terrestris) colonies. Field-based colonies that were exposed to sulfoxaflor during the early growth phase produced significantly fewer workers than unexposed controls, and ultimately produced fewer reproductive offspring. Differences between the life-history trajectories of treated and control colonies first became apparent when individuals exposed as larvae began to emerge, suggesting that direct or indirect effects on a small cohort may have cumulative long-term consequences for colony fitness. Our results caution against the use of sulfoximines as a direct replacement for neonicotinoids. To avoid continuing cycles of novel pesticide release and removal, with concomitant impacts on the environment, a broad evidence base needs to be assessed prior to the development of policy and regulation.