Queen-worker conflict and social parasitism in bumble bees (Hymenoptera: Apidae)

Psithyrus ashtoni (Hymenoptera: Apidae) is an obligate, workerless bumble, bee social parasite which invades nests of Bombus affinis. Although parasites are limited by host worker defence to invading very small colonies, there is considerable flexibility in the way parasites control host brood bionomics once they are accepted inside the nest. A study of 46 parasitized and 22 non-parasitized laboratory colonies of B. affinis showed that P. ashtoni females cohabited with host queens and workers while the worker force increased, but not to the maximum normally achieved in non-parasitized nests. While colony reproductive success was correlated with the number of workers reared, parasites risked being killed or ejected from the comb by workers, after the queen had lost dominance. Host bees usually succeeded in rearing offspring, and Psithyrus reproductive success was related to the ability of parasites to control proportional investment in the two species. In addition to displacing P. ashtoni females, host bees ate the eggs of parasites and ejected their larvae. These behaviours were also exhibited by workers in the later stages of development of non-parasitized colonies. These results indicate that social parasites are at least partially subject to the conflict of genetic self-interest between the queen and her workers which is believed to influence the control of reproductive investment in haplodiploid Bombus societies.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

Molecular and spatial analyses reveal links between colony‐specific foraging distance and landscape‐level resource availability in two bumblebee species

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.     

Colony pace: a life-history trait affecting social insect epidemiology

Among colonies of social insects, the worker turnover rate (colony ‘pace’) typically shows considerable variation. This has epidemiological consequences for parasites, because in ‘fast-paced’ colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.     

Long-Term Disease Dynamics for a Specialized Parasite of Ant Societies: A Field Study

Many studies have investigated how social insects behave when a parasite is introduced into their colonies. These studies have been conducted in the laboratory, and we still have a limited understanding of the dynamics of ant-parasite interactions under natural conditions. Here we consider a specialized parasite of ant societies (Ophiocordyceps camponoti-rufipedis infecting Camponotus rufipes) within a rainforest. We first established that the parasite is unable to develop to transmission stage when introduced within the host nest. Secondly, we surveyed all colonies in the studied area and recorded 100% prevalence at the colony level (all colonies were infected). Finally, we conducted a long-term detailed census of parasite pressure, by mapping the position of infected dead ants and foraging trails (future hosts) in the immediate vicinity of the colonies over 20 months. We report new dead infected ants for all the months we conducted the census – at an average of 14.5 cadavers/month/colony. Based on the low infection rate, the absence of colony collapse or complete recovery of the colonies, we suggest that this parasite represents a chronic infection in the ant societies. We also proposed a “terminal host model of transmission” that links the age-related polyethism to the persistence of a parasitic infection.     

Using citizen science to monitor Bombus populations in the UK: nesting ecology and relative abundance in the urban environment

Citizen science can provide a valuable tool for collecting large quantities of ecological data over a larger geographic area than would otherwise be possible. Here, data were collected on 1,022 bumblebee nests by means of a public survey in which participants were asked to record attributes of bumblebee nests discovered in their gardens. All commonly reported species appeared to be generalist in their nest site selection and though species-specific differences in nest site choice were evident, there was a high degree of overlap in nesting habitat between most species. There was little evidence supporting the hypothesis that bumblebees tend to nest in the same site in consecutive years. A comparison of the contributions made by different species to the total nests reported in this and previous similar surveys suggests that the common bumblebee species Bombus pascuorum may have declined over the past 20?years relative to other species, comprising ~21% of colonies discovered in a survey conducted in 1989–1991, but just 8–9% of colonies in 2007–2009. This was accompanied by a reduction in the proportion of nests on the ground surface (the preferred position of this species). This is the first quantitative evidence of potential declines in the one of the UK’s ‘big six’ common bumblebee species.     

Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance

The evolutionary interactions between permanently social parasiticspecies and their hosts are of special interest because socialparasites are not only closely dependent on, but are also closelyrelated to, their hosts. The small European slavemaker Harpagoxenussublaevis has evolved several characters that help manipulateits host. In this study we investigated adaptations of thissocial parasite to its local hosts and the geographic patternof host resistance in two main host species from three differentpopulations. In behavioral experiments, we examined whetherhost colonies from three geographically distant Leptothoraxacervorum populations varied in their ability to defend thenest against social parasites. Naive colonies from the unparasitizedEnglish population killed attacking slavemakers more often thandid host colonies from two parasitized populations. We alsofound strong interpopulation variation in the ability of theslavemaker to manipulate host behavior. H. sublaevis uses theDufour gland secretion to induce intracolonial fights and, ingeneral, this "propaganda" substance was most effective againstlocal hosts. Our results suggest that the social parasite isleading the arms race in this aspect. Similar experiments uncovereddifferences between two populations of the second host speciesL. muscorum and could demonstrate that nest defense in bothhost species is similarly efficient. In L. acervorum, monogynouscolonies were more successful in nest defense, whereas socialstructure had no impact in L. muscorum. Colony size did notaffect the efficacy of nest defense in either host species.The caste of the slavemaker had a strong influence on the successof an attack.     

Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites

Abstract.

• 1 In natural populations, colonies of bumble bees vary in many important life history traits, such as colony size and age at maturity, or the number and sex of reproductives produced. We investigated how the presence of parasites in field populations of the bumble bee Bombus lucorum L. relates to variation in life history traits and reproductive performance. A total of thirty-six colonies was placed in accessible nest sites in the field and monitored at regular intervals throughout a season.
• 2 Among the life history correlates, early nest foundation was strongly associated with large maximum colony size, old age and large size at maturity, and this in turn with successful production of males and queens, as well as with the number of sexuals produced. Overall, reproductive success was highly skewed with only five colonies producing all the queens. Sixteen colonies failed to reproduce altogether.
• 3 The social parasite Psithyrus was abundant early in the Bombus colony cycle and preferentially invaded host nests with many first brood workers and thus disproportionately large size, i.e. those colonies that would otherwise be more likely to reproduce or produce (daughter) queens rather than males. To prevent nest loss, Psithyrus had to be removed soon after invasion. Therefore, the effects reported here can only be crude estimates.
• 4 Parasitoid conopid flies are likely to cause heavy worker mortality when sexuals are reared by the colonies. Their inferred effect was a reduction in biomass that could be invested in sexuals as well as a shift in the sex ratio at the population level resulting from failure to produce queens. We suggest to group the inferred correlates into ‘early events’ surrounding colony initiation and social parasitism, and ‘late events’ surrounding attained colony size in summer and parasitism by conopid flies. Our evidence thus provides a heuristic approach to understand the factors that affect reproductive success of Bombus colonies.

     

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens. Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.     

The Value of Uncropped Field Margins For Foraging Bumblebees

The intensification of agriculture has led to declines in species diversity and abundance within groups of certain flora and fauna. Bumblebees (Bombus spp.) are one group where a decline has been documented, and it is thought to be attributable to a decrease in forage resources and potential nest sites. As bumblebees play an important role in the pollination of many entomophilous crops, this decline could impact on agricultural productivity. We examined the role of naturally regenerated field margins in providing forage plants on land where nectar resources are otherwise impoverished. The following question was addressed – Are naturally regenerated unsprayed field margins more attractive to foraging bumblebees and honeybees than cropped field margins managed as conservation headlands? Significantly more bees visited naturally regenerated field margins than cropped field margins. Honeybees (Apis mellifera), Bombus terrestris, and Bombus lapidarius were the most commonly observed bee species. Different wildflower species within the naturally regenerated margins varied greatly in relative number of visits received, and bumblebee species were found to prefer different flower species to honeybees. The potential role that naturally regenerated field margins could play in the conservation of bumblebee species, and the implications for other species of flora and fauna, are discussed.     

Prudent inquilines and proactive hosts: behavioral dynamics between an ant social parasite, Megalomyrmex symmetochus and its fungus-growing ant host, Sericomyrmex amabilis

Ant social parasites evolve adaptive relationships with their hosts. Theoretically, coevolution predicts strong selection to maximize fitness of the parasite that minimizes costs to its host, which potentially leads to the evolution of benign interactions. We studied the demographic and behavioral traits of the ant social parasite Megalomyrmex symmetochus (Solenopsidini), an agro-predator that feeds on larvae and fungal garden products of their host, Sericomyrmex amabilis (Attini). Based on demographic data from 15 parasitized colonies, the proportion of parasitic workers to those of the host is 1:2. Moreover, defensive prophylactic behaviors observed during infections with Metarhizium brunneum, a generalist entomopathogen, and Escovopsis, a specialized fungal garden parasite, showed that S. amabilis works extensively to remove and control fungal infections, in contrast to M. symmetochus. M. symmetochus, however, performed intraspecific allogrooming during infections with Escovopsis and M. brunneum, suggesting that they may recognize fungal pathogens and indirectly limit dispersion of spores. Our results indicate that M. symmetochus did not have a strong role in maintaining a hygienic nest.     

Inhibition of Host Queen Reproductive Capacity by the Obligate Social Parasite Polistes atrimandibularis (Hymenoptera,Vespidae)

Polistes atrimandibularis is the obligate and permanent parasite of the social paper wasp Polistes biglumis bimaculatus. This parasite lives together with the host foundress for a considerable period on the invaded nest. Ovarian development was measured in females of the host species (foundresses and, when present, workers) from 18 parasitized and 14 non-parasitized colonies. The reproductive capacity of foundresses from parasitized nests decreased faster than that of foundresses from non-parasitized nests. These results indicate that the presence of the parasite lowers reproductive capacity of the host queen. Simultaneously, the fertility of the host worker is inhibited.     

Species and Colony Components in the Recognition Odor of Young Social Wasps: Their Expression and Learning (Polistes biglumis and P. atrimandibularis; Hymenoptera: Vespidae)

In Polistes, nestmate recognition relies on the learning of recognition cues from the nest. When wasps recognize nestmates, they match the template learned with the odor of the encountered wasp. The social wasp Polistes biglumis use the homogeneous odor of their colony to recognize nestmates. When these colonies become host colonies of the social parasite P. atrimandibularis, colony odor is no longer homogeneous, as the parasite offspring have an odor that differs from that of their hosts. In trying to understand how the mechanism of nestmate recognition works in parasitized colonies and why parasite offspring are accepted by hosts, we tested the responses of resident Polistes biglumis wasps from parasitized and unparasitized colonies to newly emerged parasites and to nestmate and non-nestmate conspecifics. The experiments indicate that immediately upon eclosion both young parasites and young hosts lack a colony odor and that colony odor can be soon acquired from the accepting colony. In addition, while residents of nonparasitized colonies recognize only the odor of their species, resident hosts of parasitized colonies have learned a template that fits the odors of two species.     

Do host species evolve a specific response to slave-making ants?

Background

Social parasitism is an important selective pressure for social insect species. It is particularly the case for the hosts of dulotic (so called slave-making) ants, which pillage the brood of host colonies to increase the worker force of their own colony. Such raids can have an important impact on the fitness of the host nest. An arms race which can lead to geographic variation in host defenses is thus expected between hosts and parasites. In this study we tested whether the presence of a social parasite (the dulotic ant Myrmoxenus ravouxi) within an ant community correlated with a specific behavioral defense strategy of local host or non-host populations of Temnothorax ants. Social recognition often leads to more or less pronounced agonistic interactions between non-nestmates ants. Here, we monitored agonistic behaviors to assess whether ants discriminate social parasites from other ants. It is now well-known that ants essentially rely on cuticular hydrocarbons to discriminate nestmates from aliens. If host species have evolved a specific recognition mechanism for their parasite, we hypothesize that the differences in behavioral responses would not be fully explained simply by quantitative dissimilarity in cuticular hydrocarbon profiles, but should also involve a qualitative response due to the detection of particular compounds. We scaled the behavioral results according to the quantitative chemical distance between host and parasite colonies to test this hypothesis.

Results

Cuticular hydrocarbon profiles were distinct between species, but host species did not show a clearly higher aggression rate towards the parasite than toward non-parasite intruders, unless the degree of response was scaled by the chemical distance between intruders and recipient colonies. By doing so, we show that workers of the host and of a non-host species in the parasitized site displayed more agonistic behaviors (bites and ejections) towards parasite than toward non-parasite intruders.

Conclusions

We used two different analyses of our behavioral data (standardized with the chemical distance between colonies or not) to test our hypothesis. Standardized data show behavioral differences which could indicate qualitative and specific parasite recognition. We finally stress the importance of considering the whole set of potentially interacting species to understand the coevolution between social parasites and their hosts.

     

The genetic population structure of the ant Plagiolepis xene-implications for genetic vulnerability of obligate social parasites

Obligatory social parasites, such as ant species that need colonies of other ant species for reproduction, are rare and many of them are classified as vulnerable. This is especially the case with highly adapted permanent inquilines that are specialised on one or a few host species. Their rarity may be due to reduced dispersal abilities, as a result of reduced body size, altered wing morphology, and curtailed nuptial flight, eventually leading to inbreeding. Furthermore, the host populations may differ in their ability to resist the parasite, yet the conditions of successful parasite invasion are largely unknown. Here we investigated the population structure of the inquiline ant Plagiolepis xene and its host P. pygmaea, using microsatellite data. Genetic differentiation, inbreeding, the effective population size and nest kin structure were analysed. We found that populations of P. xene are established by a single or at most a few individuals, and that the populations were genetically highly differentiated. However, within individual host populations the parasite is able to maintain panmixia, although data on the host suggests that the local distribution of the parasite also follows patterns of substructuring in the host population. Altogether our results suggest that inquiline parasite populations are genetically highly vulnerable.     

Effective population size as a driver for divergence of an antimicrobial peptide (Hymenoptaecin) in two common European bumblebee species

Social insects are the target of numerous pathogens. This is because the high density of closely‐related individuals frequently interacting with each other enhances the transmission and establishment of pathogens. This high selective pressure results in the rapid evolution of immune genes, which might be counteracted by a reduced effective population size (N_e) lowering the effectiveness of selection. We tested the effect of N_e on the evolutionary rate of an important immune gene for the antimicrobial peptide Hymenoptaecin in two common central European bumblebee species: Bombus terrestris and Bombus lapidarius. Both species are similar in their biology and are expected to be under similar selective pressures because pathogen prevalence does not differ between species. However, previous studies indicated a higher N_e in B. terrestris compared to B. lapidarius. We found high intraspecific variability in the coding sequence but low variability for silent polymorphisms in B. lapidarius. Estimates of long‐ and short‐term N_e were three‐ to four‐fold higher N_e in B. terrestris, although the species did not differ in census population sizes. The difference in N_e might result in less efficient selection and suboptimal adaptation of immune genes (e.g. hymenoptaecin) in B. lapidarius, and thus this species might become less resistant and more tolerant, turning into a superspreader of diseases.     

Ecological Variation in Response to Mass-Flowering Oilseed Rape and Surrounding Landscape Composition by Members of a Cryptic Bumblebee Complex

The Bombus sensu stricto species complex is a widespread group of cryptic bumblebee species which are important pollinators of many crops and wild plants. These cryptic species have, until now, largely been grouped together in ecological studies, and so little is known about their individual colony densities, foraging ranges or habitat requirements, which can be influenced by land use at a landscape scale. We used mass-flowering oilseed rape fields as locations to sample bees of this complex, as well as the second most common visitor to oilseed rape B. lapidarius, and molecular RFLP methods to distinguish between the cryptic species. We then used microsatellite genotyping to identify sisters and estimate colony densities, and related both proportions of cryptic species and their colony densities to the composition of the landscape surrounding the fields. We found B. lucorum was the most common member of the complex present in oilseed rape followed by B. terrestris. B. cryptarum was also present in all but one site, with higher proportions found in the east of the study area. High numbers of bumblebee colonies were estimated to be using oilseed rape fields as a forage resource, with B. terrestris colony numbers higher than previous estimates from non-mass-flowering fields. We also found that the cryptic species responded differently to surrounding landscape composition: both relative proportions of B. cryptarum in samples and colony densities of B. lucorum were negatively associated with the amount of arable land in the landscape, while proportions and colony densities of other species did not respond to landscape variables at the scale measured. This suggests that the cryptic species have different ecological requirements (which may be scale-dependent) and that oilseed rape can be an important forage resource for many colonies of bumblebees. Given this, we recommend sustainable management of this crop to benefit bumblebees.     

Genetic variation within social insect colonies reduces parasite load

In colonies of social Hymenoptera (ants, bees and wasps), workers are often not very closely related to each other, because queens mate with several different males (polyandry) or because several functional queens are present (polygyny). Both characteristics increase genetic variation among the queens'' reproductive and worker offspring, but the benefits of this increased variation remain obscure. Here we report an experiment where genetically homogeneous and genetically heterogeneous colonies of the bumble bee, Bombus terrestris, have been exposed to parasitism under field conditions. Colonies of high or low genetic variation were achieved by adding and removing brood from donor colonies. The results showed a consistent effect in that genetically variable colonies experienced reduced parasite loads, i.e. lower prevalence, intensity and parasite species richness, for a range of protozoa, nematodes, mites or parasitoids affecting the workers. We therefore propose that polyandry and/or polygyny of social insects may be beneficial under parasitism.     

Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae)

Eusociality and male haploidy of bumblebees (Bombus spp.) enhance the deleterious effects of population decline and aggravate the degeneration of population fitness compared to solitary and diploid species. The highly dispersive male sex may be the prime driver to connect otherwise isolated populations. We therefore studied the temporal and spatial structure of the male population of Bombus terrestris (Linnaeus 1758) and Bombus lapidarius (Linnaeus 1758) using microsatellite DNA markers. We found that the majority of the males in a 1000 m2 sampling area originated from colonies located outside of the workers foraging range, which was consistent with the genetic distances among colonies. The analyses of temporal population sub-structure based on both colony detection rate over time and the clustering software STRUCTURE consistently suggested one large and temporally unstructured male population. Our results indicate an extended male flight distance for both species. Though the range of queen dispersal remains to be studied, the effective size (N _e) of bumblebees is increased by extended male mating flight ranges (A _m ) exceeding worker foraging distance by factor 1.66 (A _m  = 69.75 km²) and 1.74 (A _m  = 13.41 km²), B. terrestris and B. lapidarius, respectively. Thus this behaviour may counteract genetic deprivation and its effects. All populations were genetically highly diverse and showed no signs of inbreeding. We discuss the implications of our findings in context of bumblebee population dynamics and conservation. We also highlight the effects and benefits of sampling both workers and males for population genetic studies.