Evolution of ageing, costs of reproduction and the fecundity-longevity trade-off in eusocial insects.

Eusocial insects provide special opportunities to elucidate the evolution of ageing as queens have apparently evaded costs of reproduction and reversed the fecundity-longevity trade-off generally observed in non-social organisms. But how reproduction affects longevity in eusocial insects has rarely been tested experimentally. In this study, we took advantage of the reproductive plasticity of workers to test the causal role of reproduction in determining longevity in eusocial insects. Using the eusocial bumblebee Bombus terrestris, we found that, in whole colonies, in which workers could freely 'choose' whether to become reproductive, workers' level of ovarian activation was significantly positively associated with longevity and ovary-active workers significantly outlived ovary-inactive workers. By contrast, when reproductivity was experimentally induced in randomly selected workers, thereby decoupling it from other traits, workers' level of ovarian activation was significantly negatively associated with longevity and ovary-active workers were significantly less long-lived than ovary-inactive workers. These findings show that workers experience costs of reproduction and suggest that intrinsically high-quality individuals can overcome these costs. They also raise the possibility that eusocial insect queens exhibit condition-dependent longevity and hence call into question whether eusociality entails a truly reversed fecundity-longevity trade-off involving a fundamental remodelling of conserved genetic and endocrine networks underpinning ageing

Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales

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.This research was funded by the UK Department for Environment, Food and Rural Affairs (research grant BD1625), and Natural England, Peterborough, UK

Anarchy in the UK: Detailed genetic analysis of worker reproduction in a naturally occurring British anarchistic honeybee, Apis mellifera, colony using DNA microsatellites

Anarchistic behaviour is a very rare phenotype of honeybee colonies. In an anarchistic colony, many workers’ sons are reared in the presence of the queen. Anarchy has previously been described in only two Australian colonies. Here we report on a first detailed genetic analysis of a British anarchistic colony. Male pupae were present in great abundance above the queen excluder, which was clearly indicative of extensive worker reproduction and is the hallmark of anarchy. Seventeen microsatellite loci were used to analyse these male pupae, allowing us to address whether all the males were indeed workers’ sons, and how many worker patrilines and individual workers produced them. In the sample, 95 of 96 of the males were definitely workers’ sons. Given that ≈ 1% of workers’ sons were genetically indistinguishable from queen’s sons, this suggests that workers do not move any queen-laid eggs between the part of the colony where the queen is present to the area above the queen excluder which the queen cannot enter. The colony had 16 patrilines, with an effective number of patrilines of 9.85. The 75 males that could be assigned with certainty to a patriline came from 7 patrilines, with an effective number of 4.21. They were the offspring of at least 19 workers. This is in contrast to the two previously studied Australian naturally occurring anarchist colonies, in which most of the workers’ sons were offspring of one patriline. The high number of patrilines producing males leads to a low mean relatedness between laying workers and males of the colony. We discuss the importance of studying such colonies in the understanding of worker policing and its evolution

The decline and conservation of bumblebees

Declines in bumblebee species in the last 60 years are well documented in Europe, where they are primarily driven by habitat loss and declines in floral abundance and diversity resulting from agricultural intensification. Impacts of habitat degradation and fragmentation are likely to be compounded by the social nature of bumblebees and their largely monogamous breeding system which renders their effective population size low. Hence populations are susceptible to stochastic extinction events and inbreeding. In North America, catastrophic declines of some bumblebee species since the 1990s are probably attributable to the accidental introduction of a non-native parasite from Europe, a result of global trade in domesticated bumblebee colonies used for pollination of greenhouse crops. Given the importance of bumblebees as pollinators of crops and wildflowers, it is vital that steps be taken to prevent further declines. Suggested measures include tight regulation of commercial bumblebee use and targeted use of agri-environment schemes to enhance floristic diversity in agricultural landscapes

Complex hybrid origin of genetic caste determination in harvester ants

Caste differentiation and division of labour are the hallmarks of insect societies and at the root of their ecological success. Kin selection predicts that caste determination should result from environmentally induced differences in gene expression, a prediction largely supported by empirical data. However, two exceptional cases of genetically determined caste differentiation have recently been found in harvester ants. Here we show that genetic caste determination evolved in these populations after complex hybridization events. We identified four distinct genetic lineages, each consisting of unique blends of the genomes of the parental species, presumably Pogonomyrmex barbatus and P. rugosus. Crosses between lineages H1 and H2 and between J1 and J2 give rise to workers, whereas queens develop from within-lineage matings. Although historical gene flow is evident, genetic exchange among lineages and between lineages and the parental species no longer occurs. This unusual system of caste determination seems to be evolutionarily stable

Unrelated Helpers in a Primitively Eusocial Wasp: Is Helping Tailored Towards Direct Fitness?

The paper wasp Polistes dominulus is unique among the social insects in that nearly one-third of co-foundresses are completely unrelated to the dominant individual whose offspring they help to rear and yet reproductive skew is high. These unrelated subordinates stand to gain direct fitness through nest inheritance, raising the question of whether their behaviour is adaptively tailored towards maximizing inheritance prospects. Unusually, in this species, a wealth of theory and empirical data allows us to predict how unrelated subordinates should behave. Based on these predictions, here we compare helping in subordinates that are unrelated or related to the dominant wasp across an extensive range of field-based behavioural contexts. We find no differences in foraging effort, defense behaviour, aggression or inheritance rank between unrelated helpers and their related counterparts. Our study provides no evidence, across a number of behavioural scenarios, that the behaviour of unrelated subordinates is adaptively modified to promote direct fitness interests

The Seasonal Natural History of the Ant, Dolichoderus mariae, in Northern Florida

Dolichoderus mariae Forel, (Hymenoptera: Formicidae) is an uncommon, monomorphic but locally abundant, reddish-brown ant of peculiar nesting habits, whose range includes most of the eastern USA. In north Florida the ant excavates soil under wiregrass clumps or other plants with fibrous roots to form a single, large, shallow, conical or ovoid chamber broadly open to the surface around the plant base. Colonies are highly polygyne and, during the warm season, inhabit multiple nests connected only by above ground trails, over which nests exchange workers. Although monomorphic, worker size may differ significantly between colonies. The colony cycle is dominated by strong seasonal polydomy. From one or two over-wintering nests, the colonies expanded to occupy up to 60 nests by late summer, then retract once more to one or two nests by mid-winter. The worker-to-queen ratio changed greatly during this cycle, with over two thousand workers per queen during fall and winter, dropping to a low of about 300 during midsummer. Most of these summer queens probably die during the fall. Colonies reoccupy roughly the same area year to year even though they contract down to one or two nests in winter. Observation of fights in the contact zone between colonies suggested that the colonies are territorial. The ants subsist by tending aphids and scale insects for honeydew and scavenging for dead insects within their territories

Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus

PMCID: PMC3744404This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

Extraordinary lifespans in ants: a test of evolutionary theories of ageing

Senescence presents not only a medical problem, but also an evolutionary paradox because it should be opposed by natural selection. Evolutionary hypotheses propose that ageing evolves as the necessary cost of processes increasing early reproductive success(1,2), or because of weaker selection against late-acting mutations(3). A prediction of these hypotheses is that the rate of ageing should increase and the average lifespan decrease as the rate of extrinsic mortality increases(1-7). Alternatively, non-adaptive, purely mechanistic hypotheses invoke damage to DNA, cells, tissues and organs as being the unique cause of senescence and ineluctable death of organisms(8). Here we show that the evolution of eusociality is associated with a 100-fold increase in insect lifespan. Such an increase is predicted by evolutionary theories because termite, bee and ant queens live in colonies that are sheltered and heavily defended against predators. Moreover, a comparison of ants with contrasting life histories also reveals an association between lifespan and extrinsic rate of mortality. These results provide strong support for evolutionary theories of ageing, as purely mechanistic hypotheses of senescence do not propose any association between the rate of extrinsic mortality and lifespans

Prediction of social structure and genetic relatedness in colonies of the facultative polygynous stingless bee Melipona bicolor (Hymenoptera, Apidae)

Stingless bee colonies typically consist of one single-mated mother queen and her worker offspring. The stingless bee Melipona bicolor (Hymenoptera: Apidae) shows facultative polygyny, which makes this species particularly suitable for testing theoretical expectations concerning social behavior. In this study, we investigated the social structure and genetic relatedness among workers from eight natural and six manipulated colonies of M. bicolor over a period of one year. The populations of M. bicolor contained monogynous and polygynous colonies. The estimated genetic relatedness among workers from monogynous and polygynous colonies was 0.75 ± 0.12 and 0.53 ± 0.16 (mean ± SEM), respectively. Although the parental genotypes had significant effects on genetic relatedness in monogynous and polygynous colonies, polygyny markedly decreased the relatedness among nestmate workers. Our findings also demonstrate that polygyny in M. bicolor may arise from the adoption of related or unrelated queens