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Eusocial insect colonies are vulnerable to exploitation by egg-laying workers arising either as natal reproductive workers or as non-natal reproductive ‘drifting’ workers (intraspecific social parasites). Worker egg-laying is potentially costly to the colony, but queens and workers can counter its costs via egg eating (queen or worker policing). Bumblebee colonies exhibit egg laying by both natal and non-natal workers: natal workers collectively lay more eggs but do so only after a specific point in the colony cycle, the ‘competition point’, whereas non-natal workers potentially lay eggs throughout the colony cycle. These features create a special opportunity to investigate whether policing of worker-laid eggs is context-dependent (i.e. depends on worker origin of eggs and/or colony stage). We introduced artificial egg cells containing eggs laid by either natal or non-natal workers into colonies of the bumblebee Bombus terrestris both before and after their competition points and observed the fate of introduced egg cells and eggs. In both colony stages, the majority of introduced egg cells and eggs were policed, demonstrating that policing was not activated only after the competition point. However, in the pre-competition point stage alone, a smaller proportion of non-natal workers' eggs (15%) remained after 20 h compared to the proportion of natal workers' eggs remaining (24%). More effective policing of non-natal workers' eggs early in the colony cycle potentially represents an adaptive, context-dependent response to the stage in the cycle when all worker-laid eggs are normally unrelated to the natal colony.

The standard evolutionary theory of ageing predicts a negative relationship (trade-off) between fecundity and longevity. However, this relationship can become positive: (i) under the influence of longevity-enhancing mutations; (ii) when individuals have unequal resources; and (iii) in eusocial insects, in which reproductive queens outlive less- or non-reproductive workers. Developmental diet is likely to be central to determining trade-offs as it affects key fitness traits such as adult body size, but its exact role remains uncertain. For example, inDrosophila melanogasterfruit flies, changes in adult diet can affect fecundity, longevity, and gene expression throughout life, but it is unknown how changes in developmental (larval) diet affect fecundity-longevity relationships or gene expression in adults. UsingD. melanogaster, we therefore tested the hypothesis that variation in developmental diet alters the directionality of fecundity-longevity relationships in adults, and characterised associated gene expression changes. We rearedD. melanogasterlarvae on low (20%), medium (100%), and high (120%) SYA (Sugar Yeast Agar) diets, and transferred adult females developing from these larvae to a common (110% SYA) adult diet. We measured life-time fertility (realised fecundity) and longevity of individual adult females and, using mRNA-seq, profiled gene expression changes across two time-points. Adult females raised on the different larval diets exhibited fecundity-longevity relationships that were significantly different in directionality, i.e., varied from positive to negative, despite minimal differences in mean life-time fertility or longevity. Treatments also differed in age-related gene expression, including expression of genes known to be associated with ageing. Hence, this study shows that the sign of fecundity-longevity relationships in adult insects can be altered and even reversed by variation in larval diet quality. Furthermore, larval diet quality may be a key mechanistic factor underpinning positive fecundity-longevity relationships observed in species such as eusocial insects.

Eusocial insect queens have been suggested to be counter-examples to the standard evolutionary theory of ageing through lacking costs of reproduction. Using the bumblebee (Bombus terrestris), we tested this hypothesis experimentally against the alternative that costs of reproduction exist in eusocial insect queens, but are latent, resulting in the positive fecundity-longevity relationship typically found in unmanipulated queens. We experimentally increased queens’ costs of reproduction by removing their eggs, which causes queens to increase their egg-laying rate. Treatment queens had significantly reduced longevity relative to control queens whose egg-laying rate was not increased. In addition, treatment and control queens differed in age-related gene expression based on mRNA-seq in both their overall expression profiles and the expression of ageing-related genes. Remarkably, this occurred principally with respect to relative age, not chronological age. These results provide the first simultaneously phenotypic and transcriptomic experimental evidence of costs of reproduction in queens of eusocial insects and suggest how the genetic pathways underpinning ageing might become remodelled during eusocial evolution.

Inclusive fitness theory shows that social partners must be related for altruism to evolve, yet some models suggest that relatedness is not needed. An analysis concludes that assumptions in those models build in a role for relatedness, after all. Assessment of models used to explain how altruism might have evolved.

Inclusive fitness theory is the leading framework for explaining the major transitions in evolution, whereby free-living subunits (e.g. cells, organisms) have cooperated to form new, higher-level units (e.g. organisms, eusocial societies). The theory has attracted considerable controversy. From a brief survey of the controversy's present status, I conclude that inclusive fitness theory continues to provide both a concept and a principled modelling tool of value for understanding social evolution, including major transitions. Turning to new developments in the study of major transitions, I describe work defining the point of occurrence of major transitions and, from inclusive fitness theory, the required conditions. I also suggest that it remains important to understand the evolution of individuality that occurs beyond such thresholds.

The queen‐worker caste system of eusocial insects represents a prime example of developmental polyphenism (environmentally‐induced phenotypic polymorphism) and is intrinsic to the evolution of advanced eusociality. However, the comparative molecular basis of larval caste determination and subsequent differentiation in the eusocial Hymenoptera remains poorly known. To address this issue within bees, we profiled caste‐associated gene expression in female larvae of the intermediately eusocial bumblebee Bombus terrestris. In B. terrestris, female larvae experience a queen‐dependent period during which their caste fate as adults is determined followed by a nutrition‐sensitive period also potentially affecting caste fate but for which the evidence is weaker. We used mRNA‐seq and qRT‐PCR validation to isolate genes differentially expressed between each caste pathway in larvae at developmental stages before and after each of these periods. We show that differences in gene expression between caste pathways are small in totipotent larvae, then peak after the queen‐dependent period. Relatively few novel (i.e., taxonomically‐restricted) genes were differentially expressed between castes, though novel genes were significantly enriched in late‐instar larvae in the worker pathway. We compared sets of caste‐associated genes in B. terrestris with those reported from the advanced eusocial honeybee, Apis mellifera, and found significant but relatively low levels of overlap of gene lists between the two species. These results suggest both the existence of low numbers of shared toolkit genes and substantial divergence in caste‐associated genes between Bombus and the advanced eusocial Apis since their last common eusocial ancestor.

Genetic bottlenecks can limit the success of populations colonizing new ranges. However, successful colonizations can occur despite bottlenecks, a phenomenon known as the genetic paradox of invasion. Eusocial Hymenoptera such as bumblebees (Bombusspp.) should be particularly vulnerable to genetic bottlenecks, since homozygosity at the sex-determining locus leads to costly diploid male production (DMP). The Tree Bumblebee (Bombus hypnorum) has rapidly colonized the UK since 2001 and has been highlighted as exemplifying the genetic paradox of invasion. Using microsatellite genotyping, combined with the first genetic estimates of DMP in UKB. hypnorum, we tested two alternative genetic hypotheses (‘bottleneck’ and ‘gene flow’ hypotheses) forB. hypnorum's colonization of the UK. We found that the UK population has not undergone a recent severe genetic bottleneck and exhibits levels of genetic diversity falling between those of widespread and range-restrictedBombusspecies. Diploid males occurred in 15.4% of reared colonies, leading to an estimate of 21.5 alleles at the sex-determining locus. Overall, the findings show that this population is not bottlenecked, instead suggesting that it is experiencing continued gene flow from the continental European source population with only moderate loss of genetic diversity, and does not exemplify the genetic paradox of invasion.

Agri-environment schemes (AES) have been implemented across Europe, aiming to mitigate effects of habitat loss in agro-ecosystems for a range of declining species. These include pollinating insects such as bumblebees, for which positive effects of AES on abundance and species richness have been shown. However, there is a lack of evidence for effects of AES on reproduction of target species, at either local or landscape scales. We conducted a large-scale study across landscapes exhibiting a gradient of agricultural intensity to investigate the effects of a targeted flower mixture, sown in patches of three different sizes, on an index of the total biomass of bumblebee sexuals (males and queens) on replicated transects within each landscape. We used this index (MQ) as a measure of bumblebee reproduction. After controlling for floral density on transects, we found that MQ was significantly higher on sown flower patches than on conventionally managed control patches at local scales throughout the three-year study. While sown flower patches did not significantly increase MQ in surrounding landscapes, MQ was higher in landscapes surrounding larger (1 ha) than smaller (0.25 ha) sown patches. Our results suggest that, while responses of different bee species may vary depending on the plant species sown, targeted flower mixtures can enhance bumblebee reproduction by providing locally attractive forage resources to bumblebees of all castes and sexes from nests within foraging distance. If established at large enough scales, sown flower patches may lead to a detectable spill-over of reproductives into surrounding landscapes. Furthermore, effects of sown patches on MQ were moderated by landscape context, the strongest positive responses being detected at sites with high proportions of arable land. This supports previous findings that AES can deliver greater net benefits for pollinators in more intensively farmed landscapes.

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female-biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The Wilson– Nowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female-biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen–worker conflict over sex allocation is absent. Here, I argue that the Wilson–Nowak sex ratio hypothesis is flawed because it contradicts Fisher’s sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain ‘split’ (bimodal) sex ratios or data showing queen and worker control and ongoing queen–worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson–Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.

Insect pollinators such as bumblebees (Bombus spp.) are in global decline1,2, a major cause of which is habitat loss due to agricultural intensification3. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed4-6. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages7, in target species. Such understanding is lacking for bumblebees because of the difficulty of systematically finding and monitoring colonies in the wild. We used a novel combination of habitat manipulation, land-use and habitat surveys, molecular genetics8 and demographic and spatial modelling to examine between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250-1000 m of the natal colony. This is the first evidence of a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. The findings provide strong support for conservation interventions that increase floral resources at a landscape scale and throughout the season having positive effects on wild pollinators in agricultural landscapes.

In cooperatively-breeding or eusocial societies, opportunities may arise for helper individuals to gain direct fitness by reproducing. However, the extent to which helpers respond differentially, in terms of their reproductive behaviour, to the probability that reproductive opportunities will arise is not fully known. In many eusocial Hymenoptera, workers lay eggs only in queenless conditions following the death of the queen or queens. Relative to polygyny (multiple queens per colony), monogyny (single queen per colony) increases the probability that queenless conditions arise. We therefore tested the hypothesis that ant workers respond differentially to queenless conditions as a function of the probability of queenlessness. We compared worker behaviour and reproduction before and after removal of queens from monogynous and polygynous colonies of the ant Leptothorax acervorum. We found that, in queenless conditions, workers from monogynous colonies were significantly more likely to lay eggs, showed a significantly reduced latency to egg-laying, and laid eggs at a significantly higher rate per capita, than workers from polygynous colonies. In addition, before queen removal, workers that laid eggs in queenless conditions across both monogynous and polygynous colonies performed a range of behaviours associated with reproduction at significantly higher rates compared to non-reproductive, control workers. These 'future reproductive' workers also significantly reduced their rates of brood care following queen removal. These findings show that workers under monogyny reproduce more readily in queenless conditions than workers under polygyny, and that would-be reproductive workers alter their behaviour before they experience the opportunity for future reproduction. They therefore suggest that workers adaptively modulate their reproductive behaviour as a function of the likelihood of opportunities for direct reproduction arising, and that workers' behaviour is affected by the ability to gain direct fitness even when reproduction is currently not occurring.

Inclusive fitness theory explains why workers in insect societies sometimes kill their queen. As the theory predicts, workers in a wasp species are more likely to act matricidally when more highly related to potential worker offspring.

I argue that Grafen’s formal darwinism project could profitably incorporate a gene’s-eye view, as informed by the major transitions framework. In this, instead of the individual being assumed to maximise its inclusive fitness, genes are assumed to maximise their inclusive fitness. Maximisation of fitness at the individual level is not a straightforward concept because the major transitions framework shows that there are several kinds of biological individual. In addition, individuals have a definable fitness, exhibit individual-level adaptations and arise in a major transition, only to the extent that the inclusive-fitness interests of genes within them coincide. Therefore, as others have suggested, the fundamental level at which fitness is maximised is the gene level. Previous reconciliations of the concepts of gene-level fitness and individual-level fitness implicitly recognise this point. Adaptations always maximise the fitness of their causative genes, but may be simple or complex. Simple adaptations may be controlled by single genes and be maladaptive at higher levels, whereas complex adaptations are controlled by multiple genes and rely on those genes having coinciding fitness interests at a higher level, for a given trait.

In eusocial Hymenoptera (ants, bees and wasps), queen and worker adult castes typically arise via environmental influences. A fundamental challenge is to understand how a single genome can thereby produce alternative phenotypes. A powerful approach is to compare the molecular basis of caste determination and differentiation along the evolutionary trajectory between primitively and advanced eusocial species, which have, respectively, relatively undifferentiated and strongly differentiated adult castes. In the advanced eusocial honeybee, Apis mellifera, studies suggest that microRNAs (miRNAs) play an important role in the molecular basis of caste determination and differentiation. To investigate how miRNAs affect caste in eusocial evolution, we used deep sequencing and Northern blots to isolate caste-associated miRNAs in the primitively eusocial bumblebee Bombus terrestris. We found that the miRNAs Bte-miR-6001-5p and -3p are more highly expressed in queen- than in worker-destined late-instar larvae. These are the first caste-associated miRNAs from outside advanced eusocial Hymenoptera, so providing evidence for caste-associated miRNAs occurring relatively early in eusocial evolution. Moreover, we found little evidence that miRNAs previously shown to be associated with caste in A. mellifera were differentially expressed across caste pathways in B. terrestris, suggesting that, in eusocial evolution, the caste-associated role of individual miRNAs is not conserved.

Eusocial insects provide special insights into the genetic pathways influencing aging because of their long-lived queens and flexible aging schedules. Using qRT-PCR in the primitively eusocial bumble bee Bombus terrestris (Linnaeus), we investigated expression levels of four candidate genes associated with taxonomically widespread age-related pathways (coenzyme Q biosynthesis protein 7, COQ7; DNA methyltransferase 3, Dnmt3; foraging, for; and vitellogenin, vg). In Experiment 1, we tested how expression changes with queen relative age and productivity. We found a significant age-related increase in COQ7 expression in queen ovary. In brain, all four genes showed higher expression with increasing female (queen plus worker) production, with this relationship strengthening as queen age increased, suggesting a link with the positive association of fecundity and longevity found in eusocial insect queens. In Experiment 2, we tested effects of relative age and social environment (worker removal) in foundress queens and effects of age and reproductive status in workers. In this experiment, workerless queens showed significantly higher for expression in brain, as predicted if downregulation of for is associated with the cessation of foraging by foundress queens following worker emergence. Workers showed a significant age-related increase in Dnmt3 expression in fat body, suggesting a novel association between aging and methylation in B. terrestris. Ovary activation was associated with significantly higher vg expression in fat body and, in younger workers, in brain, consistent with vitellogenin's ancestral role in regulating egg production. Overall, our findings reveal a mixture of novel and conserved features in age-related genetic pathways under primitive eusociality.

Bumble bees (Bombus spp.) are important pollinators of both crops and wildflowers. Their contribution to this essential ecosystem service has been threatened over recent decades by changes in land use, which have led to declines in their populations. In order to design effective conservation measures, it is important to understand the effects of variation in landscape composition and structure on the foraging activities of worker bumble bees. This is because the viability of individual colonies is likely to be affected by the trade-off between the energetic costs of foraging over greater distances and the potential gains from access to additional resources. We used field surveys, molecular genetics, and fine resolution remote sensing to estimate the locations of wild bumble bee nests and to infer foraging distances across a 20-km2 agricultural landscape in southern England, UK. We investigated five species, including the rare B. ruderatus and ecologically similar but widespread B. hortorum. We compared worker foraging distances between species and examined how variation in landscape composition and structure affected foraging distances at the colony level. Mean worker foraging distances differed significantly between species. Bombus terrestris, B. lapidarius, and B. ruderatus exhibited significantly greater mean foraging distances (551, 536, and 501 m, respectively) than B. hortorum and B. pascuorum (336 and 272 m, respectively). There was wide variation in worker foraging distances between colonies of the same species, which was in turn strongly influenced by the amount and spatial configuration of available foraging habitats. Shorter foraging distances were found for colonies where the local landscape had high coverage and low fragmentation of seminatural vegetation, including managed agri-environmental field margins. The strength of relationships between different landscape variables and foraging distance varied between species, for example the strongest relationship for B. ruderatus being with floral cover of preferred forage plants. Our findings suggest that management of landscape composition and configuration has the potential to reduce foraging distances across a range of bumble bee species. There is thus potential for improvements in the design and implementation of landscape management options, such as agri-environment schemes, aimed at providing foraging habitat for bumble bees and enhancing crop pollination services.

Inclusive fitness theory predicts that, other things equal, individuals within social groups should direct altruistic behaviour towards their most highly related group-mates to maximise indirect fitness benefits. In the social insects, most previous studies have shown that within-colony kin discrimination (nepotism) is absent or weak. However, the number of studies that have investigated within-colony kin discrimination at the level of individual behaviour remains relatively small. We tested for within-colony kin discrimination in the facultatively multiple-queen (polygynous) ant, Leptothorax acervorum. Specifically, we tested whether workers within polygynous colonies treated queens differently as a function of their relatedness to them. Colonies containing two egg-laying queens were filmed to measure the rate at which individually marked workers antennated and groomed or fed each queen. Relatedness between individual queens and workers was calculated from their genotypes at four microsatellite loci. The results showed there were no differences in the rates at which workers antennated or groomed/fed their more related queen and their less related queen. Workers interacted preferentially with their potential mother queen with respect to grooming/feeding but not with respect to antennation. However, because of high queen turnover, the frequency of adult workers with their potential mother queen still present within the colony was relatively low. Overall, therefore, we found no evidence for within-colony kin discrimination in the context of the average worker's treatment of queens in polygynous L. acervorum colonies.

Worker policing (mutual repression of reproduction) in the eusocial Hymenoptera represents a leading example of how coercion can facilitate cooperation. The occurrence of worker policing in "primitively" eusocial species with low mating frequencies, which lack relatedness differences conducive to policing, suggests that separate factors may underlie the origin and maintenance of worker policing. We tested this hypothesis by investigating conflict over male parentage in the primitively eusocial, monandrous bumblebee, Bombus terrestris. Using observations, experiments, and microsatellite genotyping, we found that: (a) worker- but not queen-laid male eggs are nearly all eaten (by queens, reproductive, and nonreproductive workers) soon after being laid, so accounting for low observed frequencies of larval and adult worker-produced males; (b) queen- and worker-laid male eggs have equal viabilities; (c) workers discriminate between queen- and worker-laid eggs using cues on eggs and egg cells that almost certainly originate from queens. The cooccurrence in B. terrestris of these three key elements of "classical" worker policing as found in the highly eusocial, polyandrous honeybees provides novel support for the hypothesis that worker policing can originate in the absence of relatedness differences maintaining it. Worker policing in B. terrestris almost certainly arose via reproductive competition among workers, that is, as "selfish" policing.

Specialization in plant-pollinator systems represents an important issue for both the ecological understanding and conservation of these systems. We investigated the extent to which the bumblebee Bombus hortorum (Linnaeus) is the main potential pollinator of Common Foxglove, Digitalis purpurea L. Twenty D. purpurea patches were selected in North Yorkshire, U.K., ten each in woodland and garden or park habitat. All insects visiting D. purpurea within the patches were recorded over seventy 30-min bouts. The relative frequency of insect visitors to other flowering plant species within 15 m of each patch was also determined. B. hortorum and B. pascuorum were the two most frequent visitors to D. purpurea , accounting for 82 - 92% and 3 -17%, respectively, of all insect visits ( n = 1682), depending on habitat. B. hortorum showed a significant preference for visiting D. purpurea relative to its frequency of visits to other available plant species. The relationship of D. purpurea with B. hortorum , which pollinates several plant species with long corollas, therefore represents a potential case of asymmetric specialization, albeit one that may vary spatially. Because D. purpurea reproduction appears dependent on insect pollination, B. hortorum and B. pascuorum may help underpin the viability of D. purpurea populations.

Foraging distance is a key determinant of colony survival and pollination potential in bumblebees Bombus spp. However this aspect of bumblebee ecology is poorly understood because of the difficulty in locating colonies of these central place foragers. Here, we used a combination of molecular microsatellite analyses, remote sensing and spatial analyses using kernel density estimates to estimate nest location and foraging distances for a large number of wild colonies of two species, and related these to the distribution of foraging habitats across an experimentally manipulated landscape. Mean foraging distances were 755 m for Bombus lapidarius and 775 m for B. pascuorum (using our most conservative estimation method). Colony-specific foraging distances of both species varied with landscape structure, decreasing as the proportion of foraging habitats increased. This is the first time that foraging distance in wild bumblebees has been shown to vary with resource availability. Our method offers a means of estimating foraging distances in social insects, and informs the scale of management required to conserve bumblebee populations and enhance their pollination services across different landscapes.

The conservation genetics of bees is of particular interest because many bee species are in decline, so jeopardizing the essential ecosystem service of plant pollination that they provide. In addition, as social haplodiploids, inbred bees may be vulnerable to the extra genetic load represented by the production of sterile diploid males. Using microsatellite markers, we investigated the genetic structure of populations of the Great Yellow Bumblebee (Bombus distinguendus Morawitz) in the UK, where this species has undergone a precipitous decline. By means of a mixture of analytical methods and simulation, we also extended--and then applied--genetic methods for estimating foraging distance and nest density in wild bees. B. distinguendus populations were characterized by low expected heterozygosity and allelic richness, inbreeding coefficients not significantly different from zero, absence of detected diploid males, absence of substantial demographic bottlenecking, and population substructuring at large (c. 100+ km) but not small (10s of km) spatial scales. The minimum average effective population size at our sampling sites was low (c. 25). In coastal grassland (machair), the estimated modal foraging distance of workers was 391 m, with 95% of foraging activity occurring within 955 m of the nest, and estimated nest density was 19.3 nests km(-2). These findings show that B. distinguendus exhibits some genetic features of scarce, declining or fragmented populations. Moreover, B. distinguendus workers appear to forage over above-average distances and nests remain thinly distributed even in current strongholds. These considerations should inform future conservation actions for this and similar species.

Queens in some species of ant with several queens per colony are believed to inhibit one another's fecundity pheromonally. This paper describes a repeat of an experimental test of this idea in the multiple-queen ant Leptothorax acervorum. The three most fecund queens from a field-collected colony were housed together in an experimental nest. This was then filmed for 10 h per day over 36 consecutive days (i.e. for 360 h in total). Over the first 12 d, all queens were present in the colony. For the middle 12 d, the two most fecund queens were removed, but were returned for the final 12 d. The queen that was observed throughout the experiment failed to show a rise in fecundity when the other queens were removed. Instead, her egg-laying rate fell, although this drop was not significant. These results confirm previous findings that short-term, strong pheromonal inhibition of fecundity does not occur among L. acervorum queens. The phenomena of pheromonal inhibition in other species may be a result of workers treating queens differentially in response to rapid, short-term changes in the numbers of queens and eggs. If so, the results presented here could stem from the relative infrequency of such changes in L. acervorum.

Social Hymenoptera have been relatively little studied in terms of conservation genetics even though their sociality and complementary sex determination potentially influence the interaction of genetics with extinction risk. Using microsatellite markers, we investigated the social and genetic structure of nests and populations of the Black Bog Ant Formica picea at four sites in the UK, where this habitat specialist has a localized and fragmented range. Nests were weakly polygynous (effective queen number, 4-27 per nest) with low worker relatedness. Isolation by distance tended to be present within sites, indicating limited dispersal, but inbreeding was rare. The four study sites fell into three main populations (two in South Wales, one in southern England). We conclude that, although UK F. picea populations are not at immediate risk from genetic factors, their limited dispersal abilities at both within- and between-site scales should inform conservation management decisions.

Researchers are increasingly recognizing that social effects influence the evolution of aging. Kin selection theory provides a framework for analyzing such effects because an individual's longevity and mortality schedule may alter its inclusive fitness via effects on the fitness of relatives. Kin-selected effects on aging have been demonstrated both by models of intergenerational transfers of investment by caregivers and by spatially explicit population models with limited dispersal. They also underlie coevolution between the degree and form of sociality and patterns of aging. In this review I critically examine and synthesize theory and data concerning these processes. I propose a classification, stemming from kin selection theory, of social effects on aging and describe a hypothesis for kin-selected conflict over parental time of death in systems with resource inheritance. I conclude that systematically applying kin selection theory to the analysis of the evolution of aging adds considerably to our general understanding of aging.

International audience; We tested the hypotheses that a non-volatile pheromone inhibiting worker egg-laying and queen development produced by Bombus terrestris queens has effects transferable (a) from workers to other workers or larvae, or (b) on wax. We subdivided small, young colonies with a single mesh screen (Experiment 1) and larger, older colonies with a double mesh screen (Experiment 2). One treatment (in both experiments) involved the transfer of workers, and one treatment (in Experiment 2 only) involved the transfer of wax, from the queenright to the queenless compartments. Queenlessness induced significantly earlier onset of worker aggression (followed by egg-laying) in all treatments in both experiments, and significantly earlier queen production in all treatments in Experiment 2 (small colony sizes probably hindered queen production in Experiment 1). These findings suggested that the effects of B. terrestris queen pheromone are not transferable via workers or wax.

Pollinating insects are of major ecological and commercial importance, yet they may be facing ecological disruption from a changing climate. Despite this threat, few studies have investigated the life-history responses of pollinators to experimentally controlled changes in temperature, which should be especially informative for species with complex life histories such as eusocial insects. This study uses the key pollinator Bombus terrestris, a eusocial bumble bee with an annual colony cycle, to determine how temperature affects life-history traits at both individual and colony levels. In two laboratory experiments, we reared B. terrestris colonies at either 20°C or 25°C, and measured differences in a set of life-history traits including colony longevity, queen longevity, worker longevity, production of workers, production of sexuals (queen and male production) and growth schedule, as well as effects on thermoregulatory behaviours. Higher rearing temperature had a significant positive effect on colony longevity in one of the two experiments but no significant effects on queen or worker longevity. Higher rearing temperature significantly increased colony size but did not affect the timing of peak colony size. It was also associated with significantly higher queen production but had no effect on the production of workers or males or the timing of male production. Higher temperature colonies exhibited significantly more wing-fanning by workers and significantly less wax canopy construction. Hence an increase in rearing temperature of a few degrees increased colony longevity, colony size and queen production. However, individual longevity was not affected and so may have been buffered by changes in costly thermoregulatory behaviours. We conclude that eusocial insects may show complex phenotypic responses to projected temperature increases under climate change, including effects on productivity and reproduction at the colony level. Such effects should be considered when predicting the impact of climate change on the provision of essential pollination services.

Made available in DSpace on 2015-10-21T20:31:01Z (GMT). No. of bitstreams: 0 Previous issue date: 2015-04-24. Added 1 bitstream(s) on 2015-10-22T09:48:01Z : No. of bitstreams: 1 WOS000353676700001.pdf: 2518339 bytes, checksum: d1f8d18bd059b76504f3fcd9aa639a74 (MD5) National Institutes of Health (NIH) Agriculture and Food Research Initiative Competitive grant from the USDA National Institute of Food and Agriculture Research Council of Norway (NFR) PEW Charitable Trust University of East Anglia, UK Israel Science Foundation (ISF) Biotechnology and Biological Sciences Research Council, UK University of East Anglia University of Alabama College of Arts and Sciences Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) Marie Curie International Outgoing Fellowship Swiss National Science Foundation New Faculty Initiative Grant (NFIG) from Illinois State University College of Arts and Sciences DFG Instituto Nacional de Bioinformatica (INB) from ISCIII in Spain Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation. Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA ETH, Inst Integrat Biol, Expt Ecol, CH-8092 Zurich, Switzerland E Carolina Univ, Dept Biol, Greenville, NC 27858 USA Hebrew Univ Jerusalem, Alexander Silberman Inst Life Sci, Dept Ecol Evolut &Behav, Jerusalem, Israel Univ Ghent, Fac Sci, Lab Zoophysiol, B-9000 Ghent, Belgium Univ Otago, Dept Biochem, Labo Evolut &Dev Genet, Dunedin 9054, New Zealand Univ Otago, Dept Biochem, Natl Res Ctr Growth &Dev, Dunedin 9054, New Zealand Univ Missouri, Div Plant Sci, Div Anim Sci, Columbia, MO 65211 USA Univ Missouri, MU Informat Inst, Columbia, MO 65211 USA Georgetown Univ, Dept Biol, Washington, DC 20057 USA Arizona State Univ, Sch Life Sci, Tempe, AZ 85287 USA Univ Copenhagen, Dept Biol, Ctr Funct &Comparat Insect Gen, Copenhagen, Denmark Univ Hohenheim, Inst Anim Sci, D-70599 Stuttgart, Germany Univ Alabama, Dept Biol Sci, Tuscaloosa, AL 35487 USA Univ Illinois, Dept Entomol, Urbana, IL 61801 USA Univ Ghent, Fac Biosci Engn, Dept Crop Protect, Lab Agrozool, B-9000 Ghent, Belgium Univ Halle Wittenberg, Inst Biol, Wittenberg, Germany Univ Geneva, Sch Med, Dept Genet Med &Dev, CH-1211 Geneva, Switzerland Swiss Inst Bioinformat, CH-1211 Geneva, Switzerland MIT, Comp Sci &Artificial Intelligence Lab, Cambridge, MA 02139 USA MIT &Harvard, Broad Inst, Cambridge Ctr 7, Cambridge, MA 02142 USA Univ Munster, Inst Evolut &Biodivers, D-48149 Munster, Germany Ctr Genom Regulat CRG, Barcelona 08003, Spain UPF, Barcelona, Spain Ernst Moritz Arndt Univ Greifswald, Inst Math &Comp Sci, D-17487 Greifswald, Germany Univ Calif Berkeley, Lawrence Berkeley Natl Lab, Genom Div, Berkeley, CA 94720 USA Natl Lib Med, Natl Ctr Biotechnol Informat, Bethesda, MD 20894 USA Norwegian Univ Food Sci, Dept Chem Biotechnol &Food Sci, N-1432 As, Norway Univ E Anglia, Sch Comp Sci, Norwich NR4 7TJ, Norfolk, England Univ Dusseldorf, Inst Evolut Genet, D-40225 Dusseldorf, Germany Univ Cologne, Inst Genet, Cologne, Germany Univ Sao Paulo, Dept Biol, Fac Filosofia Ciencias &Letras Ribeirao Preto, BR-14040901 Ribeirao Preto, Brazil Univ Edinburgh, Ashworth Labs, Inst Evolutionary Biol &Edinburgh Gen, Edinburgh EH9 3FL, Midlothian, Scotland Univ E Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England Royal Holloway Univ London, Sch Biol Sci, London, England Maynooth Univ, Dept Biol, Co, Kildare, Ireland Univ Bristol, Sch Biol Sci, Bristol BS8 1TQ, Avon, England CSIRO, Land &Water Flagship, Canberra, ACT, Australia Trin Coll Dublin, Sch Nat Sci, Dept Zool, Dublin, Ireland Zool Soc London, Inst Zool, London NW1 4RY, England ETH, Inst Integrat Biol, Theoret Biol, CH-8092 Zurich, Switzerland Swiss Inst Bioinformat, Lausanne, Switzerland Swiss Fed Inst Technol, Dept Biosyst Sci &Engn, Computat Evolut, Basel, Switzerland USDA ARS, Bee Res Lab, Washington, DC 20250 USA Univ Sao Paulo, Dept Genet, Fac Med Ribeirao Preto, BR-14040900 Ribeirao Preto, Brazil N Carolina State Univ, Ctr Res Sci Computat, Raleigh, NC 27695 USA Kyoto Univ, Grad Sch Agr, Lab Insect Ecol, Kyoto, Japan Univ Sao Paulo, Dept Biol Celular &Mol &Bioagentes Patogen, Fac Med Ribeirao Preto, BR-14040900 Ribeirao Preto, Brazil Inst Fed Educ Ciencia &Tecnol Sao Paulo, BR-15991502 Matao, Brazil Ohio State Univ, Dept Entomol, Wooster, OH 44791 USA Oxford Brookes Univ, Fac Hlth &Life Sci, Dept Biol &Med Sci, Oxford OX3 0BP, England Xian Jiaotong Liverpool Univ, Dept Biol Sci, Suzhou, Peoples R China Univ Hosp Halle Saale, Dept Lab Med, Halle, Germany German Ctr Integrat Biodivers Res iDiv, Leipzig, Germany Univ Southampton, Southampton, Hants, England Univ Leicester, Dept Biol, Leicester, Leics, England Univ Fed Sao Carlos, Ctr Ciencias Biol &Saude, Dept Genet &Evolucao, BR-13565905 Sao Carlos, SP, Brazil Univ Estadual Paulista, Fac Ciencias Agr &Vet, Dept Tecnol, BR-14884900 Jaboticabal, Brazil Univ N Carolina, Dept Biol, Greensboro, NC 27403 USA Natl Ctr Sci Res Demokritos, Inst Biosci &Applicat, Athens, Greece Univ Munich, Munich, Germany Baylor Coll Med, Dept Mol &Human Genet, Human Genome Sequencing Ctr, Houston, TX 77030 USA Univ Illinois, Roy J Carver Biotechnol, Urbana, IL 61801 USA Univ Illinois, Dept Crop Sci, Urbana, IL 61801 USA Univ Illinois, Inst Genom Biol, Urbana, IL 61801 USA MD Anderson Canc Ctr, Sch Hlth Profess, Mol Genet Technol Program, Unit 2, Houston, TX 77025 USA Univ Chicago, Dept Human Genet, Chicago, IL 60637 USA Univ Ghent, Dept Biochem &Microbiol, Lab Prot Biochem &Biomol Engn, B-9000 Ghent, Belgium Queen Mary Univ London, Sch Biol &Chem Sci, Dept Biol &Expt Psychol, London E1 4NS, England Guangzhou Univ, Sch Life Sci, Guangzhou, Guangdong, Peoples R China Johns Hopkins Univ, McKusick Nathans Inst Genet Med, Ctr Computat Biol, Baltimore, MD 21205 USA Univ Illinois, Neurosci Program, Dept Entomol, Carl R Woese Inst Genom Biol, Urbana, IL 61801 USA Departamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, 14884-900, Brazi National Institutes of Health (NIH): DP1 OD006416 National Institutes of Health (NIH): U54 HG003273 Agriculture and Food Research Initiative Competitive grant from the USDA National Institute of Food and Agriculture: 2010-65106-21301 FAPESP: 11/03171-5 Marie Curie International Outgoing Fellowship: PIOF-GA-2011-303312 Swiss National Science Foundation: 31003A-125350 Swiss National Science Foundation: 31003A-143936

Kin-selected conflict over reproduction in social groups is predicted to occur when group members are unequally related to progeny. Whether kin-selected conflict is expressed may depend on individuals' ability to obtain and use information about their social environment to make decisions affecting their fitness. In some colonies of the bumblebee Bombus terrestris, workers delay laying male eggs until approximately 21 days after the queen starts (at the ‘switch point’) to lay male eggs. This delay is difficult to explain with kin selection theory, because workers are more closely related to their own sons and so should commence reproduction immediately after the switch point. Bourke & Ratnieks (2001, Proceedings of the Royal Society of London, Series B, 268, 347–355) hypothesized that the delay occurs because workers detect the sex only of older larvae (ca. 10 days after emergence from the egg) and hence are delayed in detecting the switch point. We tested this hypothesis by adding male larvae greater or less than 10 days old to each member of nine pairs of B. terrestris colonies. We found no significant difference between the treatments in the timing of the start of worker reproduction, which occurred ca. 19 days after male larvae were added. The results therefore failed to support the hypothesis. We conclude that workers have access to information that would allow them to take a reproductive decision enhancing their inclusive fitness, but for unknown reasons do not act on it. Workers may use other cues to begin reproduction, possibly a queen signal (cessation of pheromone production) to female larvae to start development as queens.

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.

Non-lethal sampling of DNA from individuals in wild populations will often be required for studies of the conservation genetics of social insects, since it avoids destroying members of scarce or declining species. We investigated the effectiveness and consequences of methods of non-lethal sampling of DNA from bumble bee workers. In an experiment with two captive and confined Bombus terrestris colonies, we found that, unlike sampling haemolymph, sampling the terminal portion of the tarsus of a mid-leg of a worker reliably yielded amplifiable microsatellite DNA and did not significantly reduce worker survivorship. In a further experiment with four B. terrestris colonies whose workers were allowed to forage freely at flowers in the external environment, tarsal sampling of either a mid-leg or a hind-leg had no significant effects on worker survivorship, the mean body mass of foraging workers, the frequency or duration of foraging trips, mass of pollen loads or mass of nectar loads. We therefore suggest that tarsal sampling of either a mid-leg or a hind-leg is an effective and acceptable means of non-lethally sampling DNA from workers in wild populations of bumble bees, because effects on individual and colony performance are likely to be absent or minimal.

Bumblebees (Bombus species) are major pollinators of commercial crops and wildflowers but factors affecting their abundance, including causes of recent population declines, remain unclear. Investigating the ecology of species with expanding ranges provides a potentially powerful means of elucidating these factors. Such species may also bring novel pollination services to their new ranges. We therefore investigated landscape-scale habitat use and foraging preferences of the Tree Bumblebee, B. hypnorum, a recent natural colonist that has rapidly expanded its range in the UK over the past decade. Counts of B. hypnorum and six other Bombus species were made in March-June 2012 within a mixed landscape in south-eastern Norfolk, UK. The extent of different landscape elements around each transect was quantified at three scales (250 m, 500 m and 1500 m). We then identified the landscape elements that best predicted the density of B. hypnorum and other Bombus species. At the best fitting scale (250 m), B. hypnorum density was significantly positively associated with extent of both urban and woodland cover and significantly negatively associated with extent of oilseed rape cover. This combination of landscape predictors was unique to B. hypnorum. Urban and woodland cover were associated with B. hypnorum density at three and two, respectively, of the three scales studied. Relative to other Bombus species, B. hypnorum exhibited a significantly higher foraging preference for two flowering trees, Crataegus monogyna and Prunus spinosa, and significantly lower preferences for Brassica napus, Glechoma hederacea and Lamium album. Our study provides novel, quantitative support for an association of B. hypnorum with urban and woodland landscape elements. Range expansion in B. hypnorum appears to depend, on exploitation of widespread habitats underutilised by native Bombus species, suggesting B. hypnorum will readily co-exist with these species. These findings suggest that management could target bumblebee species with distinctive habitat requirements to help maintain pollination services.

Land-use changes have threatened populations of many insect pollinators, including bumble bees. Patterns of dispersal and gene flow are key determinants of species' ability to respond to land-use change, but have been little investigated at a fine scale (IS = 0.01-0.02). Using queen genotypes reconstructed from worker sibships and colony locations estimated from the positions of workers within these sibships, we found that significant isolation by distance was absent in B. lapidarius, B. hortorum and B. ruderatus. In B. terrestris and B. pascuorum, it was present but weak; for example, in these two species, expected relatedness of queens founding colonies 1 m apart was 0.02. These results show that bumble bee populations exhibit low levels of spatial genetic structure at fine spatial scales, most likely because of ongoing gene flow via widespread queen dispersal. In addition, the results demonstrate the potential for agri-environment scheme conservation measures to facilitate fine-scale gene flow by creating a more even distribution of suitable habitats across landscapes. © 2014 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd.

Social insects (ants, bees, wasps and termites) as a group are species rich and ecologically dominant. Many are outstanding “ecological engineers”, or providers of “ecosystem services”, or potential bioindicator species. Few social insects are currently formally classified as Threatened, but this is almost certainly due to a lack of information on population sizes and trends in scarce species. The main influence that sociality has on threats faced by social insects is in reducing effective population sizes, increasing population genetic subdivision and possibly reducing levels of genetic variation relative to solitary species. The main influence that sociality has on threats from social insects is via its role in the ecological success of invasive species, which frequently pose a major hazard to native biotas. In some cases, social features underpinning ecological success in the original range almost certainly contribute to the success of invasive social insects. However, recent studies show or strongly suggest that, in some of the most notoriously invasive populations of ants, bees and wasps, novel social traits have arisen that greatly enhance the rate of spread and ecological competitiveness of these populations. Sociality can therefore represent either a liability or an asset in its contribution to the persistence of social insect populations.

Multiple mating by queens (polyandry) and the occurrence of multiple queens in the same colony (polygyny) alter patterns of relatedness within societies of eusocial insects. This is predicted to influence kin-selected conflicts over reproduction. We investigated the mating system of a facultatively polygynous UK population of the ant Leptothorax acervorum using up to six microsatellite loci. We estimated mating frequency by genotyping 79 dealate (colony) queens and the contents of their sperm receptacles and by detailed genetic analysis of 11 monogynous (single-queen) and nine polygynous colonies. Results indicated that 95% of queens were singly mated and 5% of queens were doubly mated. The corrected population mean mating frequency was 1.06. Parentage analysis of adults and brood in 17 colonies (10 monogynous, 7 polygynous) showed that female offspring attributable to each of 31 queens were full sisters, confirming that queens typically mate once. Inbreeding coefficients, queen–mate relatedness of zero and the low incidence of diploid males provided evidence that L. acervorum sexuals mate entirely or almost entirely at random. Males mated to queens in the same polygynous colony were not related to one another. Our data also confirmed that polygynous colonies contain queens that are related on average and that their workers had a mixed maternity. We conclude that the mating system of L. acervorum involves queens that mate near nests with unrelated males and then seek readoption by those nests, and queens that mate in mating aggregations away from nests, also with unrelated males.

Kin selection theory predicts conflict in social Hymenoptera between the queen and workers over male parentage because each party is more closely related to its own male offspring. Some aspects of the reproductive biology of the bumble-bee Bombus terrestris support kin selection theory but others arguably do not. We present a novel hypothesis for how conflict over male parentage should unfold in B. terrestris colonies. We propose that workers delay laying eggs until they possess information showing that egg laying suits their kin-selected interests. In colonies where queens start to lay haploid eggs early, we hypothesize that this occurs when workers detect the presence of queen-produced male brood in the brood's larval stage. In colonies where queens start to lay haploid eggs late, we hypothesize that it occurs when workers detect a signal from the queen to female larvae to commence development as queens. Our hypothesis accounts for previously unexplained aspects of the timing of reproductive events in B. terrestris, provides ultimate explanations for the results of a recent study of mechanisms underlying queen-worker conflict and helps explain this species' characteristic bimodal (split) sex ratios. Therefore, kin selection theory potentially provides a good explanation for reproductive patterns in B. terrestris.

We argue that caste determination, the process whereby females in the social Hymenoptera develop into either queens or workers, is subject to kin-selected conflict. Potential conflict arises because developing females are more closely related to their would-be offspring than to those of other females. Therefore, they may favour becoming queens contrary to the interests of other developing females and of existing queens and workers. We suggest two contexts leading to potential caste conflict. The first occurs when queens are reared in a reproductive phase following an ergonomic phase of worker production, while the second occurs when queens and workers are reared simultaneously. The first context assumes that workers' per capita contribution to colony survival and productivity falls with rising colony size. A critical feature influencing whether potential conflict is realized is the extent to which developing females can determine their own caste (“self-determination”). Self-determination is facilitated when female larvae control their own food intake and when queen-worker size dimorphism is low. We know of no strong evidence for actual conflict over caste fate arising in the first context. However, stingless bees and polygynous ants with excess queen-potential larvae that are either forced to develop as workers or are culled as adults demonstrate actual caste conflict in the second context. Caste conflict does not preclude caste regulation for “the good of the colony”, but such regulation is contingent on either the absence of potential conflict or on developing females losing control of their caste fate.

An important idea from kin selection theory as applied to life-history evolution in perennial insect societies suggests that potential conflict exists between the queen and workers over the relative allocation of resources to colony reproduction and colony growth. This prediction assumed a colony with one singly mated queen, sterile workers, and independent colony foundation by dispersing queens. We argue that this prediction is mistaken because queen and workers under these circumstances can only invest in sexuals (new queens and males) derived from the colony queen. Assuming population sex ratio equilibrium, potential conflict is absent because both parties maximize fitness by maximizing the colony's total output of these sexuals. However, a similar queen-worker conflict is predicted in facultatively polygynous species in which existing queens are superseded. We hypothesize that queens favor the production of relatively more new workers to prolong their lives as reproductives, whereas workers favor raising relatively more new queens as possible replacements. We tested this hypothesis using productivity data from the ant Leptothorax acervorum. As predicted, queen number and worker number were, respectively, positively and negatively associated with the investment ratio of new workers to new queens. These findings imply a queen-worker conflict over caste determination in ants.

We investigated sex allocation in three U.K. populations of the facultatively polygynous ant Leptothorax acervorum over 1–3 years. The first main finding was that, across sites, the population sex-investment ratio changed from significantly female biased to significantly male biased with increasing polygyny. This was consistent with workers controlling sex allocation and reacting to changes in their population-level relatedness asymmetry. It was also consistent with local resource competition due to reproduction by colony budding under polygyny. Worker control was supported by the finding that queen number had no effect on sex allocation among polygynous colonies. The second main result was that monogynous colonies consistently produced more female-biased sex-investment ratios than polygynous colonies in one site only (Santon). The results from Santon supported both the relative relatedness asymmetry hypothesis and the idea of sex ratio compensation due to colony budding. The workers’ response to their population-level relatedness asymmetry reinforced the case for relatedness asymmetry being influential at the colony level. The other populations could have lacked split sex ratios because polygynous colonies were either comparatively rare or common, making them behave as almost entirely monogynous (Aberfoyle) or polygynous (Roydon) populations. In Roydon, this was consistent with the inference from allozyme data that monogynous and polygynous colonies did not differ in their worker relatedness asymmetries. The final principal finding was that, of hypotheses linking the colony sex-investment ratio with sexual productivity, there was support for the constant female hypothesis but not for the constant male, cost variation, or multifaceted parental investment hypotheses.

1. Workers in several bee species travel to conspecific nests (‘drifting’), enter them, and produce male offspring inside them, so acting as intra-specific social parasites. This adds a new dimension to bees' reproductive behaviour and spatial ecology, but the extent to which drifting occurs over field scales, i.e. at natural nest densities in field conditions, has been unclear. 2. Using the bumble bee Bombus terrestris (Linnaeus) as a model system, we sought to determine rates of worker drifting at field scales and the frequency of potential drifter workers in wild nests. 3. A field experiment with 27 colonies showed that workers travelled to, and became accepted in, conspecific nests that were up to 60 m away, although the number of accepted drifter workers within nests fell significantly with distance. The rate at which nests were entered by drifters was relatively high and significantly exceeded the rate at which drifters became accepted. 4. Microsatellite genotyping of eight field-collected nests from Greater London, U.K., showed that a low frequency (3%) of workers were not full sisters of nestmate workers and hence were likely to have been drifter workers. 5. It is therefore concluded that workers can drift to conspecific nests over field scales and confirmed that successful drifting occurs in natural populations. Drifting appears to be a natural but low-frequency behaviour permitting B. terrestris workers to gain direct fitness.

We investigated the fine genetic structure of colonies of the ant, Leptothorax acervorum, to examine how queens share parentage (skew) in a social insect with multiple queens (polygyny). Overall, 494 individuals from eight polygynous field colonies were typed at up to seven microsatellite loci each. The first main finding was that surprisingly many sexual progeny (60% of young queens and 49% of young males) were not the offspring of the extant queens within their colonies. This implies that a high turnover (brief reproductive lifespan) of queens within colonies could be an important feature of polygyny. The second main result was that in most colonies relatedness among sexual progeny fell significantly below that expected among full siblings, proving that these progeny were produced by more than one singly-mated queen, but that skew in two colonies where the data permitted its calculation was moderate to high. However, relative to a German population, the study population is characterized by low queen-queen relatedness and low skew in female production, which is in line with the predictions of skew theory.

Worker policing (mutual repression of reproduction) in the eusocial Hymenoptera represents a leading example of how coercion can facilitate cooperation. The occurrence of worker policing in "primitively" eusocial species with low mating frequencies, which lack relatedness differences conducive to policing, suggests that separate factors may underlie the origin and maintenance of worker policing. We tested this hypothesis by investigating conflict over male parentage in the primitively eusocial, monandrous bumblebee, Bombus terrestris. Using observations, experiments, and microsatellite genotyping, we found that: (a) worker- but not queen-laid male eggs are nearly all eaten (by queens, reproductive, and nonreproductive workers) soon after being laid, so accounting for low observed frequencies of larval and adult worker-produced males; (b) queen- and worker-laid male eggs have equal viabilities; (c) workers discriminate between queen- and worker-laid eggs using cues on eggs and egg cells that almost certainly originate from queens. The cooccurrence in B. terrestris of these three key elements of "classical" worker policing as found in the highly eusocial, polyandrous honeybees provides novel support for the hypothesis that worker policing can originate in the absence of relatedness differences maintaining it. Worker policing in B. terrestris almost certainly arose via reproductive competition among workers, that is, as "selfish" policing.

According to Hamilton’s kin selection theory (also known as “inclusive fitness” theory), kin selection is the process by which social evolution occurs in nature. The theory extends the genetical theory of natural selection to social behaviors and finds that their evolution is affected by the likelihood that individuals share genes (relatedness). In biology, a social behavior occurs when one individual (the actor) behaves so as to affect the direct fitness (number of offspring) of itself and another individual (the recipient). For example, altruism occurs when the actor’s behavior decreases the actor’s direct fitness and increases the recipient’s direct fitness. Conversely, selfishness occurs when the actor’s behavior increases the actor’s direct fitness and decreases the recipient’s. Social behaviors are widespread in nature. A classic example is the altruism shown by the sterile workers of social insects such as ants, which sacrifice their own reproduction in order to rear the queen’s offspring. At first sight, altruism poses a problem for the genetical theory of natural selection, which seems to preclude the spread of a gene for reduced reproduction. Kin selection was devised by William Hamilton in the early 1960s to address this “problem of altruism.” The basic principle behind kin selection had been hinted at by Darwin, Fisher, and Haldane, but it was Hamilton who provided the first general model. Hamilton called his idea “inclusive fitness” theory, and it was later dubbed “kin selection” by Maynard Smith in 1964. For most purposes, the two can be considered identical, although inclusive fitness theory technically includes kin selection theory because the relatedness it invokes need not involve kin (genealogical relatives). Kin selection theory solved the problem of altruism by showing that a gene for altruism can spread if altruism is directed at individuals likely to bear the same gene. By definition, kin are likely to share genes. So, a gene for altruism can spread if altruism is directed at kin and the loss of gene copies through the actor’s decreased reproduction is more than offset by the gain in gene copies through the increased reproduction of the recipient. The algebraic version of this condition is termed “Hamilton’s rule.” Although kin selection theory was devised to explain altruism, it also applies to the other forms of social behavior such as selfishness. The theory is therefore now widely used to investigate and explain many kinds of social behavior in living organisms as diverse as bacteria and human beings.

Split sex ratio theory is an important extension of sex allocation theory. It suggests that colony sex ratios in social insects vary because workers control sex allocation and respond to variations in their comparative relatedness with females and males (relatedness asymmetry). In a population of the ant Leptothorax acervorum, 21 monogynous (single-queen) colonies produced a female-biased sex ratio (62% females), and 24 polygynous (multiple-queen) colonies produced a male-biased sex ratio (28% females). Within the polygynous colonies, queen number did not affect sex ratio (with colony productivity statistically controlled). As colony productivity rose, the sex ration either did not change (monogynous colonies) or became more male-biased (polygynous colonies). The fraction invested in sexuals rose with increasing colony size and productivity in monogynous but not in polygynous colonies, which invested less in sexuals. These findings suggest that split sex ratios in L. acervorum stem from two processes. The first is workers9 response to the variation in relatedness asymmetry caused by variable queen numbers. The second is sexratio compensation by monogynous colonies for male-biased production in polygynous colonies. This arises because polygynous colonies reproduce, partly, by colony budding and so have daughter colonies subject to local resource competition.

Multiple-queen societies of ants are key subjects in the study of communal breeding. Societies of leptothoracine ants may be obligately monogynous (contain a single reproductive queen), functionally monogynous (only one of several mated queens lays eggs), or facultatively polygynous (some colonies contain more than one egg-laying, mated queen). This paper presents a framework for understanding these diverse social systems as a function of leptothoracine ecology. The framework is derived from a synthesis of empirical information - in particular, a link between the social system and the degree of habitat patchiness - with three bodies of theory. These are ecological constraints theory, ESS (evolutionarily stable strategy) models of dispersal, and kin selection models predicting the stable reproductive skew (allocation of reproduction). In contrast to several previous ecological hypotheses, multiplequeening in leptothoracines almost certainly results from high costs to single queens of dispersal and colony foundation (high ecological constraints), which select for queens to seek adoption in their natal colony. Factors raising these costs include nest-site limitation, cold climate, and habitat patchiness. ESS models suggest that high dispersal costs lead to a larger stable fraction of non-dispersers and hence to higher relatedness between queens. Skew models predict that high ecological constraints and high relatedness promote high skew (one or a few individuals dominate reproduction) and high within-colony aggression. Therefore, (i) extensive habitats with moderate costs of solitary colony foundation should promote multiple-queening with high dispersal levels, moderate queen relatedness, low reproductive skew, and low queen aggression. By contrast, (ii) patchy habitats should induce multiple-queening with less dispersal, higher queen relatedness, higher skew, and higher aggression. In addition, (iii) habitats with small or widely spaced nest-sites, or with low costs of founding colonies alone, should lead to universal dispersal without multiple-queening. These associations of traits occur in facultatively polygynous, functionally monogynous and obligately monogynous leptothoracines respectively. Therefore, the framework in this paper explains a substantial amount of the social and ecological diversity of leptothoracine ants.

In bumble bees (Bombus) and vespine wasps (Vespa, Vespula, Dolichovespula), workers have regularly been observed to kill their colony's single queen (worker matricide). Workers gain a fitness payoff in worker-produced males from matricide because it removes the queen's inhibition over their reproduction. There is selection for the queen's death when this gain outweighs the fitness penalty of losing queen-derived offspring. A kin selection model explores this condition for three parties, the queen, nonlaying workers, and laying workers. Matricide is favoured by (i) annual life cycles, (ii) late-season colonies, (iii) declining queen productivity, (iv) male-only production by queens, and (v) single mating. Conflict and relative power among workers also affect whether matricide occurs. Existing data largely support these predictions. Queen dominance loss arguably culminates in matricide because of positive feedback between the queen's condition and worker treatment of her. Worker matricide represents an extreme form of kin-selected queen-worker conflict over sexual production.

Societies of ants with several egg-laying queens (polygyny) permit the study of the evolution of a stable allocation of reproduction (reproductive skew). One factor that could influence the stable skew in the polygynous ant Leptothorax acervorum is cannibalism by queens of other queens9 eggs. To test for discrimination during egg-eating, isolated queens were offered a choice between their own eggs and eggs laid by either a nestmate queen or a queen from another colony. The eggs had been made distinguishable by exposing queens to dye. In a total of 45 trials, queens preferentially ate non-nestmate eggs but did not show a significant preference for a nestmate9s over their own eggs. This suggests that mutual egg-eating within colonies does not affect the stable reproductive skew. Once established, indiscriminate egg-eating could be evolutionarily stable because queens that give up egg-eating suffer the costs of having their eggs eaten but lose the nutritional benefits.

A recent study is the first to sequence a gene known to underlie a complex social phenotype. In the fire ant, Solenopsis invicta, a single allelic difference at the Gp-9 locus specifies the number of queens a colony has, and hence the social structure of the colony. Gp-9 appears to encode a protein implicated in chemical recognition of nestmates, consistent with workers determining queen number by selectively executing queens as a function of workers’ and queens’ Gp-9 genotypes. Other Solenopsis species exhibit the same social and genetic polymorphism. This study pioneers the integrated understanding of the evolution of social behaviour at molecular, individual and social levels.

The global decline of insect pollinators, especially bees, is cause for concern, and there is an urgent need for cost-effective conservation measures in agricultural landscapes. While landscape context and habitat quality are known to influence species richness and abundance of bees, there is a lack of evidence from manipulative field experiments on bees' responses to adaptive management across differently structured landscapes. We present the results of a large-scale study that investigated the effects of a targeted agri-environment scheme (AES) on bumble bees (Bombus spp.) over three years in the United Kingdom. Forage patches of different sizes were sown with a conservation flower mixture across eight sites covering a broad range of agricultural land use types. Species richness and worker densities (especially of the longer-tongued Bombus species for which the mixture was targeted) were significantly higher on sown forage patches than on existing non-crop control habitats throughout the three-year study, but the strength of this response depended on both the proportions of arable land and abundance of herbaceous forb species in the surrounding landscape. The size of sown patches also affected worker density, with smaller patches (0.25 ha) attracting higher densities of some species than larger patches (1.0 ha). Our models show that a targeted AES can deliver greater net benefits in more intensively farmed areas, in terms of the number and species richness of bumble bees supported, than in heterogeneous landscapes where other foraging habitats exist. These findings serve to strengthen the evidence base for extending agri-environment schemes to boost declining pollinator populations to a larger number of agricultural landscapes across the globe.