Patterns of parasite infection in bumble bees (Bombus spp.) of Northern Virginia

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A newly-discovered mode of colony founding among fire ants

Summary Queen ants start new colonies either unassisted by workers (independent founding), assisted by workers from their natal nest (dependent founding), or assisted by the workers of other species (dependent, socially parasitic). The monogyne form of the fire ant,Solenopsis invicta, founds independently in summer, but in the fall it also produces a few sexuals some of which overwinter, then fly and mate in early spring. These overwintered queens lack the nutritional reserves and behaviors for independent colony founding. Rather, they seek out unrelated, mature, orphaned colonies, enter them and exploit the worker force to found their own colony through intraspecific social parasitism. Success in entering orphaned colonies is higher when these lack overwintered female alates of their own. When such alates are present, orphaning causes some to dealate and become uninseminated replacement queens, usually preventing entry of unrelated, inseminated replacement queens. Such colonies produce large, all-male broods. Successful entry of a parasitic queen robs the host colony of this last chance at reproductive success. Only overwintered sexuals take part in this mode of founding.     

Population and colony structure and morphometrics in the queen dimorphic harvester ant, <Emphasis Type="Italic">Pogonomyrmex pima</Emphasis>

The North American seed-harvester ant Pogonomyrmex (Ephebomyrmex) pima displays a dimorphism that consists of winged (alate) and wingless (intermorph) queens; both types of queens are fully reproductive. Microsatellite allele frequencies and a mitochondrial phylogeny demonstrate (1) alate and intermorph queens represent an intraspecific wing polymorphism, and (2) an absence of assortative mating and inbreeding by males. Surveys at our field site in southcentral Arizona, USA, demonstrated that only one type of queen (intermorph or dealate) occurred in each colony, including those excavated during the season in which reproductive sexuals were present. Colony structure appeared to vary by queen type as most intermorph colonies contained multiple mated queens. Alternatively, dealate queen colonies rarely contained a mated queen. Our inability to find mated dealate queens in these colonies probably resulted from difficulty in excavating the entire colony and reproductive queen, especially given that these colonies were only excavated over one day. A morphometric analysis demonstrated that intermorph queens are intermediate in size to that of workers and alate queens, but that intermorph queens retain all of the specialized anatomical features of alate queens (except for wings). Some colonies had queens that foraged and performed nest maintenance activities, and these queens sometimes accounted for a significant portion of colony foraging trips. Dissections revealed that these queens were uninseminated; some of these queens produced males in the laboratory. Received 24 October 2006; revised 1 December 2006; accepted 8 December 2006.     

The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis)

Host–parasite systems are characterised by coevolutionary arms races between host and parasite. Parasites are often the driving force, as they replicate much faster than their hosts and have shorter generation times and larger population sizes, resulting in higher mutation rates per time interval. This scenario does not fit all host–parasite systems. Socially parasitic cuckoo bumblebees (Bombus (Psithyrus) vestalis) parasitise colonies of Bombus terrestris share most life history characteristics with their hosts. As they parasitise only a subset of all available colonies, their population size should be lower than that of their hosts. This might have strong negative effects on the genetic diversity of B. vestalis and their adaptability. Here, we study for the first time the population structure of a Bombus/Bombus (Psithyrus) system. Highly polymorphic DNA markers were used to reconstruct sibships from individuals collected in the wild. The analysis of the host and parasite populations revealed a rate of parasitism of about 42% (range 33–50%). The population size of B. vestalis was lower compared to their hosts, which was also reflected in low within-group genetic distance. An analysis of the reconstructed queen genotypes revealed more supersisters amongst the B. vestalis queens when compared to the B. terrestris host. The data suggest that B. vestalis females and males do not disperse over long distances. This shows a potential for local adaptation to their hosts.     

Avoid mistakes when choosing a new home: Nest choice and adoption of Leptothorax ant queens

In ants, mating and colony founding are critical steps in the life of ant queens. Outside of their nests, young queens are exposed to intense predation. Therefore, they are expected to have evolved behavior to accurately and quickly locate a nesting place. However, data on the early life history of female reproductives are still lacking. Leptothorax gredleri is a suitable model organism to study the behavior of young queens. Reproductives can be reared under artificial conditions and readily mate in the laboratory. After mating, L. gredleri queens have the options to found solitarily, seek adoption into another colony, or return into their natal nest. In this study, we investigated the decision-making processes of female sexuals before and after mating. In particular, we tested whether female sexuals use chemical cues to find their way back to the nest, studied if they prefer their own nest over other nesting sites and followed the adoption dynamics of mated queens over 8 weeks (plus hibernation and spring). We showed that female sexuals and freshly mated queens spent more time on substrate previously used by workers from their own colony and from another colony than on a blank substrate. This discriminatory capability of queens appears to be lost in old, reproductive queens. Nest choice experiments showed that female sexuals and freshly mated queens can distinguish their own nest while old mated queens’ do not. When reintroduced in their maternal colony, young queens were readily adopted, but a few weeks later aggression against young queens led to their emigration from the maternal nest and eventually also death.     

The phylogenetic position of the bumble bee inquiline Bombus inexspectatus and implications for the evolution of social parasitism

The high alpine European bumble bee Bombus (Thoracobombus) inexspectatus is one of three taxa in which obligate social parasitism has evolved in bumble bees. Until now, the phylogenetic placement of this species has not been analyzed quantitatively because it is rare in nature. Here a specimen of B. inexspectatus is sequenced for five genes to assess its phylogenetic position relative to other bumble bee species. Phylogenetic estimation of B. inexspectatus places this species within the subgenus Thoracobombus, as expected based on morphology. This provides strong support for the acquisition of social parasitism in B. inexspectatus separate from that found in the bumble bees of the subgenus Psithyrus and B. (Alpinobombus) hyperboreus. Furthermore, B. inexspectatus is not the sister taxon of its host but is a near relative, suggesting a loose but not strict adherence to Emery’s rule. B. inexspectatus is a sister taxon to a clade including B. veteranus, a frequent nest usurper that has been suggested to be a facultative social parasite. The phylogenetic placement of all bumble bee social parasites relative to their hosts is discussed.     

Deceptive pollination of the Lady's Slipper Cypripedium tibeticum (Orchidaceae)

To test whether the nectarless flowers of Cypripedium tibeticum attract pollinators through mimicry like the allied species C. macranthos var. rebunense, pollination biology of C. tibeticum was investigated in western China. Although C. tibeticum was also pollinated by bumble bee queens, i.e. Bombus lepidus , B. lucorum and B. hypnorum , no special, rewarding model plants were found in the habitat. Field experimentation confirmed that the flowers were self-compatible but insects were required to transfer orchid pollen to the stigma. Both Bombus queens and workers were visitors, but queens were much more frequent than workers and only queens were effective pollinators. Floral functional morphology analysis showed that it was large queens rather than small workers that fitted well with the flowers of C. tibeticum. With the faint sweet-fruity scent, the minor floral fragrance compound, ethyl acetate, probably plays a role in attracting bumble bees by food deception. The dark flowers with the inflated, trap-like labellum are hypothesized to mimic the nest site of queens. Therefore, bumble bee queens tend to be attracted by C. tibeticum through nest site mimic combined with food deception. Considering that the co-blooming flowers of C. flavum are pollinated by the Bombus workers, and C. smithii pollinated by a queen, we suggest that using the same bumblebees with different body sizes as the pollinators is the main reproductive isolation between interfertile C. tibeticum and C. flavum, while C. tibeticum and C. smithii tend to hybridize naturally.     

The influence of hybridization on colony structure in the ant species Temnothorax nylanderi and T. crassispinus

The parapatric sibling ant species Temnothorax nylanderi and T. crassispinus hybridize in the contact zone in the Franconian Jura, Southern Germany. Aim of our study was to investigate the impact of hybridization on colony composition and fitness. We classified colonies as either ‘pure’ or containing hybrids by determining their allozyme pattern at GPI, an enzyme that is fixed for different alleles in the two parental species, and quantified their reproductive output. Most colonies with hybrid workers had a T. crassispinus queen. Colonies with heterozygous, hybrid workers produced more young workers than colonies of the parental species but similar numbers of male and female sexuals. Female sexuals from colonies with heterozygous workers had a significantly lower weight than female sexuals from pure colonies. Only a single reproductive queen was found to be heterozygous, suggesting reduced fitness of hybrid queens. As in the parental species, hybrid colonies appear to be frequently taken over by alien queens, which obscures the genetic colony structure. Received 6 April 2006; revised 10 June 2006; accepted 15 June 2006.     

No inbreeding depression but increased sexual investment in highly inbred ant colonies

Inbreeding can lead to the expression of deleterious recessive alleles and to a subsequent fitness reduction. In Hymenoptera, deleterious alleles are purged in haploid males moderating inbreeding costs. However, in these haplodiploid species, inbreeding can result in the production of sterile diploid males. We investigated the effects of inbreeding on the individual and colony level in field colonies of the highly inbred ant Hypoponera opacior. In this species, outbreeding winged sexuals and nest‐mating wingless sexuals mate during two separate reproductive periods. We show that regular sib‐matings lead to high levels of homozygosity and the occasional production of diploid males, which sporadically sire triploid offspring. On the individual level, inbreeding was associated with an increased body size in workers. On the colony level, we found no evidence for inbreeding depression as productivity was unaffected by the level of homozygosity. Instead, inbred colonies altered their allocation strategies by investing more resources into sexuals than into workers. This shift towards sexual production was due to an increased investment in both males and queens, which was particularly pronounced in the dispersive generation. The absence of inbreeding depression combined with increased reproductive investment, especially in outbreeding sexuals, suggests that these ants have evolved active strategies to regulate the extent and effects of frequent inbreeding.     

A method for year-round rearing of cuckoo bumblebees (Hymenoptera: Apoidea: Bombus subgenus Psithyrus)

Summary. The study of the social interactions between host bumblebees and their inquiline species requires rearing them. Here we provide a simple method for rearing of cuckoo bumblebees (Bombus subgenus Psithyrus) in the laboratory. Two bumblebee cuckoo-host systems are used: Bombus (Psithyrus) vestalis hosted by B. (Bombus) terrestris and B. (Psithyrus) sylvestris hosted by B. (Pyrobombus) pratorum. First, the invasion of the Psithyrus female is performed in species-specific host colonies containing approximately 10 young workers. On average, a parasitized colony of B. terrestris produced 90 ± 9 young males and 21 ± 3 young females of B. vestalis, whereas a parasitized colony of B. pratorum produced 16 ± 2 young males and 5 ± 1 young females of B. sylvestris. One week after emergence, Psithyrus virgin females are placed in a flight cage exposed to natural light, with Psithyrus males of other colonies. After successful mating, the females are isolated and overwintered in a cold room at 4°C for 2–4 months. This method enables a year-round and mass breeding of Psithyrus species to facilitate studies of these rare species.     

Reduced abundance and earlier collection of bumble bee workers under intensive cultivation of a mass‐flowering prairie crop

One of the most commonly seeded crops in Canada is canola, a cultivar of oilseed rape (Brassica napus). As a mass‐flowering crop grown intensively throughout the Canadian Prairies, canola has the potential to influence pollinator success across tens of thousands of square kilometers of cropland. Bumble bees (Bombus sp.) are efficient pollinators of many types of native and crop plants. We measured the influence of this mass‐flowering crop on the abundance and phenology of bumble bees, and on another species of social bee (a sweat bee; Halictus rubicundus), by continuously deploying traps at different levels of canola cultivation intensity, spanning the start and end of canola bloom. Queen bumble bees were more abundant in areas with more canola cover, indicating that this crop is attractive to queens. However, bumble bee workers were significantly fewer in these locations later in the season, suggesting reduced colony success. The median collection dates of workers of three bumble bee species were earlier near canola fields, suggesting a dynamic response of colonies to the increased floral resources. Different species experienced this shift to different extents. The sweat bee was not affected by canola cultivation intensity. Our findings suggest that mass‐flowering crops such as canola are attractive to bumble bee queens and therefore may lead to higher rates of colony establishment, but also that colonies established near this crop may be less successful. We propose that the effect on bumble bees can be mitigated by spacing the crop more evenly with respect to alternate floral resources.     

Nest takeover by queen and its positive impact on colony development in the Japanese bumblebee Bombus ignitus (Apidae: Hymenoptera)

Lone Bombus ignitus queens are known to start nests in small underground cavities. To examine the nest‐site preference of post‐hibernating queens, choice tests were carried out by providing queens with orphan colonies and empty cavities as possible nesting sites within an experimental box. Our results showed that the queens had a strong preference for takeover of an orphan colony, suggesting that nest takeover (usurpation) could occur in nature even with the presence of possible empty cavities for nesting. We compared the colony‐growth process and final production of sexuals between non‐takeover and takeover colonies. The increase in the number of egg cups was faster in the takeover colonies, suggesting that orphan broods elicit earlier oviposition by the usurping queen. Reproductives emerged earlier (significant for new queens) and in greater numbers (males) from takeover colonies than from non‐takeover colonies. Thus, post‐hibernating B. ignitus queens would search for and take over small orphan colonies to increase their fitness.     

Spatial ecology of a range‐expanding bumble bee pollinator

Molecular methods have greatly increased our understanding of the previously cryptic spatial ecology of bumble bees (Bombus spp.), with knowledge of the spatial ecology of these bees being central to conserving their essential pollination services. Bombus hypnorum, the Tree Bumble Bee, is unusual in that it has recently rapidly expanded its range, having colonized much of the UK mainland since 2001. However, the spatial ecology of B. hypnorum has not previously been investigated. To address this issue, and to investigate whether specific features of the spatial ecology of B. hypnorum are associated with its rapid range expansion, we used 14 microsatellite markers to estimate worker foraging distance, nest density, between‐year lineage survival rate and isolation by distance in a representative UK B. hypnorum population. After assigning workers to colonies based on full or half sibship, we estimated the mean colony‐specific worker foraging distance as 103.6 m, considerably less than values reported from most other bumble bee populations. Estimated nest density was notably high (2.56 and 0.72 colonies ha^?1 in 2014 and 2015, respectively), estimated between‐year lineage survival rate was 0.07, and there was no evidence of fine‐scale isolation by distance. In addition, genotyping stored sperm dissected from sampled queens confirmed polyandry in this population (mean minimum mating frequency of 1.7 males per queen). Overall, our findings establish critical spatial ecological parameters and the mating system of this unusual bumble bee population and suggest that short worker foraging distances and high nest densities are associated with its rapid range expansion.     

Evolutionary transition to a semelparous life history in the socially parasitic ant Acromyrmex insinuator

The recently discovered social parasite Acromyrmex insinuator ( 25 ) exploits colonies of the leafcutter ant A. echinatior. We document that A. insinuator represents a rare early stage in the evolution of social parasitism, because a worker caste is still partially present and mating phenology has remained at least partially similar to that of the host. A. insinuator is tolerant of host queens, and sexual offspring produced in parasitized colonies can be either exclusively A. insinuator or a mix of A. insinuator and A. echinatior. The remarkably high abundance of A. insinuator in nests of the investigated Panamanian host population and the fact that A. insinuator colonies readily reproduce under laboratory conditions allowed us to test evolutionary predictions on reproductive life history evolution that are not possible in most other socially parasitic ants. We show that (1) A. insinuator has a semelparous ‘big bang’ reproductive life history which exploits host colonies without leaving reserves for survival; (2) social parasite sexuals are significantly smaller than A. echinatior host sexuals, but still large compared to host workers, confirming an evolutionary scenario of gradual size reduction and loss of the worker caste after transition towards a socially parasitic life history; (3) major changes in the life history of ants can evolve relatively quickly compared to adaptations in morphology, caste differentiation and mating phenology.     

Both female castes contribute to colony emigration in the polygynous ant Mystrium oberthueri

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Does the diapause experience of bumblebee queens Bombus terrestris affect colony characteristics?

1. Bumblebee colonies show much variation in the number of workers, drones, and queens produced. Because this variation prevails even when colonies are kept under identical conditions, it does not seem to be caused by extrinsic factors but rather by differences between founding queens. 2. The most likely factor that could cause differences between queens is diapause. Although colonies are raised under standardised conditions, the queens often experience diapause of different length. If there are costs associated with diapause that influence post‐diapause reproduction, the diapause history of the queens could affect colony characteristics. 3. Here, several colony characteristics are compared: number of first and second brood workers; total number of workers, drones, and queens; energy spent on sexuals; sex ratio; rate of worker production; time to emergence of first reproductive; and colony lifetime. Colonies were used where the queens experienced a diapause treatment of 0 (nondiapause queens), 2, and 4 months. 4. Although no proof was found for the existence of costs associated with diapause, the colony characteristics of nondiapause queens were significantly different from those of diapause queens. Colonies of nondiapause queens produced the lowest number of workers but the highest number of young queens. 5. It is argued that these nondiapause colonies are more time‐constrained than diapause colonies because nondiapause colonies produce two generations within the same season and should therefore be more efficient in producing sexual offspring. 6. Moreover, nondiapause colonies should rear a more female‐biased sex ratio because they can be certain of the presence of males produced by other (diapause) colonies.     

Social interactions between an inquiline ant, <Emphasis Type="Italic">Ectatomma parasiticum</Emphasis>, and its host, <Emphasis Type="Italic">Ectatomma tuberculatum</Emphasis> (Formicidae,Ectatomminae)

Inquilines, workerless social parasites, frequently show advanced adaptations to their parasitic life style that indicate a long co-evolutionary history with their host. Ectatomma parasiticum, the first inquiline described in the poneromorph group, usurps established colonies of E. tuberculatum and produces only sexuals. In laboratory colonies, parasites were specifically attacked by the host workers, showing a failure in their social integration. Social interactions were frequent between parasites and their hosts, especially antennation, interpreted as attempts to promote colonial odor transfer. Inquilines destroyed eggs laid by the other queens (67 out of 209 eggs laid), including conspecific parasites, which is unusual. Such partial integration into the host colony and potential parasite virulence argue for a recent evolution of social parasitism in E. tuberculatum.     

Production of winged and wingless males in the ant, <Emphasis Type="Italic">Cardiocondyla minutior</Emphasis>

Summary Wingless (ergatoid) males of the tramp ant Cardiocondyla minutior attack and kill their young ergatoid rivals and thus attempt to monopolize mating with female sexuals reared in the colony. Because of the different strength of local mate competition in colonies with one or several reproductive queens, we expected the production of new ergatoid males to vary with queen number. Sex ratios were mostly female-biased, but in contrast to the sympatric species C. obscurior (Cremer and Heinze, 2002) neither the percentage of ergatoid males nor of female sexuals among the first 20 sexuals produced varied considerably with queen number. As in C. obscurior, experimental colony fragmentation led to the production of winged males, whereas in unfragmented control colonies only ergatoid males eclosed.Received 3 December 2003; revised 20 February 2004; accepted 23 February 2004.     

Facultative polygyny in Ectatomma tuberculatum (Formicidae, Ectatomminae)

Summary. Polygyny, the presence of several mated queens within the same colony, is widespread in insect societies. This phenomenon is commonly associated with ecological constraints such as limited nest sites. In habitats where solitary nest foundation is risky, monogynous colonies can reintegrate young daughter queens (secondary polygyny). We studied the reproductive structure (i.e. queen number) of the ectatommine ant Ectatomma tuberculatum from Bahia State, Brazil. This species was found to present facultative polygyny: out of a total of 130 colonies collected, 39.2% were monogynous, while 43.8% were polygynous. Polygynous colonies had significantly more workers than monogynous ones. Queen number in polygynous colonies ranged from 2 to 26, with an average of 4 ± 4 queens per colony. All nestmate queens were egg-layers with no apparent dominance hierarchy or agonistic behavior. Non-nestmate queens were adopted by monogynous colonies suggesting that polygyny is secondary, originating through queen adoption. This species is characterized by an open recognition system, which probably allows a switch from monogynous to polygynous colonies. The behavioral acts of queens showed that resident queens remained frequently immobile on or near the brood, contrarily to alien or adopted queens and gynes. In addition, monogynous queens showed no behavioral or physiological (i.e. by ovarian status) differences in comparison with polygynous ones. Secondary or facultative polygyny, probably associated with queen adoption, may have been favored in particular environmental conditions. Indeed, by increasing colony productivity (i.e. number of workers) and territory size (by budding and polydomy), polygyny could uphold E. tuberculatum as a dominant species in the mosaic of arboreal ants in Neotropical habitats.Received 7 April 2004; revised 11 November 2004; accepted 15 November 2004.     

Nesting patterns,ecological correlates of polygyny and social organization in the neotropical arboreal ant <Emphasis Type="Italic">Odontomachus hastatus</Emphasis> (Formicidae,Ponerinae)

Queen number varies in the population of O. hastatus in SE Brazil. Here, we evaluate how nesting ecology and colony structure are associated in this species, and investigate how reproduction is shared among nestmate queens. Queen number per colony is positively correlated with nesting space (root cluster of epiphytic bromeliads), and larger nest sites host larger ant colonies. Plant samplings revealed that suitable nest sites are limited and that nesting space at ant-occupied bromeliads differs in size and height from the general bromeliad community. Dissections revealed that queens in polygynous colonies are inseminated, have developed ovaries, and produce eggs. Behavioral observations showed that reproduction in polygynous colonies is mediated by queen–queen agonistic interactions that include egg cannibalism. Dominant queens usually produced more eggs. Field observations indicate that colonies can be initiated through haplometrosis. Polygyny in O. hastatus may result either from groups of cofounding queens (pleometrosis) or from adoption of newly mated queens by established colonies (secondary polygyny). Clumping of bromeliads increases nest space and probably adds stability through a strong root system, which may promote microhabitat selection by queens and favor pleometrosis. Rainstorms that frequently knock down bromeliads can be a source of colony break-up and may promote polygyny. Bromeliads are limited nest sites and may represent a risk for young queens leaving a suitable nest, thus favoring secondary polygyny. Although proximate mechanisms mediating queen number are poorly understood, this study suggests that heterogeneous microhabitat conditions probably contribute to the coexistence of variable forms of social structure in O. hastatus.