Behavioral Ecology Advance Access originally published online on November 3, 2004
Behavioral Ecology 2005 16(2):403-409; doi:10.1093/beheco/ari003
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Absence of nepotism toward imprisoned young queens during swarming in the honey bee
Laboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, U.K.
Address correspondence to N. Châline. E-mail: n.g.chaline{at}sheffield.ac.uk.
Received 14 May 2004; revised 18 September 2004; accepted 28 September 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Nepotism is an important potential conflict in animal societies. However, clear evidence of nepotism in the rearing of queens in social insects is limited and controversial. In the honey bee, Apis mellifera, multiple mating by queens leads to the presence of many patrilines within each colony. When the colonies reproduce through swarming, workers rear a number of new queens, only a few of which will ultimately head a colony. Workers can potentially increase their inclusive fitness by nepotistically favoring full-sister over half-sister queens during the queen rearing and elimination process. Most studies have focused on interactions between workers and immature queens (eggs and larvae) or adult queens who have exited their queen cells. However, adult queens often remain in their queen cells for up to 1 week after emerging from their pupa. In this situation, workers prevent the queens from emerging, feed them, and protect them from other emerged queens. This stage in queen rearing is therefore one in which nepotism could occur. The current study is the first to investigate the kinship between workers and adult queens who have not emerged from their queen cells. We observed the full suite of behaviors expected during this phase of colony reproduction. Although there was no evidence for nepotism in the worker–queen interactions, there was a nonrandom distribution across patrilines of the workers interacting with the queen cells. In addition, in one colony we found differential treatment of fostered (nonkin)-queen cells.
Key words: Apis mellifera, honey bee, nepotism, queen imprisonment, swarming.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Insect societies are typically nonclonal, and this leads to a wide range of potential reproductive conflicts, including conflicts over sex ratio (Trivers and Hare, 1976
), male production (Ratnieks, 1988), caste fate (Wenseleers and Ratnieks, 2004), and queen rearing (Visscher, 1993). Nepotism should play an important role in the resolution of these conflicts. However, clear evidence of nepotism in social insects is limited and controversial (see Hannonen and Sundström, 2003, for an example in ants). Multiple mating by honey bee (Apis mellifera) queens leads to the presence of many patrilines (paternal subfamilies within the single matriline) within each colony (Estoup et al., 1994; Palmer and Oldroyd, 2000). This causes potential conflict over queen rearing because it creates relatedness asymmetries between the workers who rear the queens and the young queens themselves, with workers being either full sisters (r = .75) or half sisters (r = .25) to these queens (Visscher, 1986). When colonies reproduce through swarming, workers rear approximately 10–20 new queens, but only a few of these (one to four) will ultimately head a colony. Workers can potentially increase their inclusive fitness if they nepotistically favor full-sister queens or disfavor half-sister queens during the queen rearing and elimination process (Visscher, 1998). However, if workers' recognition ability of full-sister queens against half-sister queens is error prone or if nepotism is costly to the colony as a whole because it reduces queen quality or number, then nepotism would not be selected or would be selected for only the weakly (Ratnieks and Reeve, 1991; Tarpy et al., 2004).
When the primary swarm leaves with the old (mother) queen, the new (sister) queens are immature. When these queens mature into adults, they compete to head a new colony either by leaving with a secondary swarm or by becoming the queen in the established nest site. In both cases, the interests of individual queens may be different from those of the workers (Visscher, 1993). The process of queen elimination has been described extensively (Bruinsma et al., 1981; Butler, 1623; Fletcher, 1978; Grooters, 1987), and theoretical work shows that it could be an important stage for queen-queen, worker-queen, and worker-worker conflict (Visscher, 1993). However, the precise role and importance of worker behavior in the outcome of the process have only recently been studied in detail (reviewed in Tarpy et al., 2004). The elimination process is characterized by numerous queen-queen interactions, including queen fights in the form of "duels" between adult queens, "assassinations" in which a pupal queen in her cell is killed by an adult queen free in the colony, vibratory signals made by adult queens (piping), and queen-worker interactions (vibratory signals, aggressive behavior, and feeding). These interactions suggest that workers could play an important role in the queen selection process, motivated by either nepotism or "quality control" unconnected with nepotism (Tarpy et al., 2004). Tarpy and Fletcher (1998) found that queens who were sisters of the workers had an advantage in winning duels over unrelated queens. However, Gilley (2003) found that in colonies with naturally mated queens, aggressive behavior by workers was not more directed toward half-sister queens. Queen quality has little influence on worker-queen interactions and survival (Gilley et al., 2003; Schneider and DeGrandi-Hoffman, 2003; Tarpy et al., 2000). Despite these many studies, our understanding of the queen elimination process remains incomplete.
All studies of the influence of workers on the selection of new queens have focused on interactions between workers and immature queens (Châline et al., 2003; Noonan, 1986; Page et al., 1989; Schneider and DeGrandi-Hoffman, 2002; Visscher, 1998) or between workers and adult queens who have exited their special queen cells (Gilley, 2001, 2003; Tarpy and Fletcher, 1998). However, adult queens often remain in their queen cells for up to 1 week (Bruinsma et al., 1981; Fletcher, 1978; Grooters, 1987) before exiting into the colony. During this time, workers cluster on each cell containing an adult queen and feed the queen through slits in the tip of the cell (Figure 1c), which are then resealed. They vibrate the queen cells and prevent the queens from exiting by repairing openings in the cells. Workers sometimes even press their head against the tip of the queen cell to prevent the queen from exiting while other workers close the cell (Fletcher, 1978). They also protect the queens by aggressively preventing access to queens who have already left their cells (Gilley, 2001). In natural queen rearing during swarming, all queens eventually exit their cells or are killed by another queen. Adult queens communicate during this process through vibratory signals (quacking from imprisoned queens and tooting from queens free in the colony, collectively known as piping; Kirchner, 1993; Simpson and Cherry, 1969), which influence queen exit from cells (Bruinsma et al., 1981; Grooters, 1987). In addition to relatedness, individual queens and workers may differ in their interests with regard to the time of exiting queen cells, fighting, and whether the colony should divide further by producing secondary swarms (Visscher, 1993). Nevertheless, the confinement of the queens is a likely ground for nepotism as workers prevent emerged queens to attack the cells, thus protecting the imprisoned queens.
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This allows the queens to mature in the cells before emerging. Consequently, the later the queen emerges, the more likely she is to win the remaining fights with queens possibly weakened by previous fights and to inherit the original colony.
Here we present the first investigation of the effect of kinship on interactions between workers and adult queens who have not exited their queen cells. To do this, we used an apparatus that allowed us to ensure that newly emerged adult queens were imprisoned in their own cells for 4 days, as occurs naturally. This experimental setup allowed us to re-create a secondary swarming situation where queens are confined in their cells by workers and so allowed prolonged behavioral observations of the workers interacting with the confined queens to be made. During the experiments, queens often tried to emerge by cutting an opening through the tip of their cells (Figure 1d), but the workers always tried to close the hole. We observed the full suite of behaviors normally expected during this phase of colony reproduction, including piping from the queens. Although there was no evidence for nepotism in the worker-queen interactions, the workers interacting with the queen cells were not randomly distributed across patrilines. In addition, in one colony we found differential treatment of fostered (nonkin) queens.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Study species
We studied three populous colonies of A. mellifera mellifera consisting of more than 30,000 workers. Colony 1 was studied in early July 2003 (experiment 1), and colonies 2A and 2B were studied simultaneously in August 2003 (experiment 2). Colonies 2A and 2B were paired to allow the cross-fostering of queen cells. The exceptionally good summer weather in 2003 resulted in a prolonged swarming season, which continued well into August.
Colony setup
All study colonies were prepared identically for the behavioral observations. Colonies were fed sucrose syrup continuously for 2 weeks to increase brood rearing and create swarming conditions. Queen rearing was then initiated in each colony by dry grafting 1- to 2-day-old worker larvae from each colony into plastic queen cups, which were returned to their own colony between frames of young brood for rearing.
After 10 days, the then sealed queen cells were removed from their colonies and an apparatus that prevented queens from exiting their cells was fitted (Figure 1d). The apparatus consisted of three thin copper wires interwoven to form a six-legged star. In the center, we attached a small piece of acetate sheet using new (white) wax taken from the colony in which the cell was reared (Figure 1d). The apparatus prevented the queen from exiting through the tip of the cell, the normal exit location, while the side of the cell was still accessible to workers, who could interact with the queen through slits made around the perimeter of the tip, as occurs naturally. Tests had previously confirmed that this apparatus allowed normal interactions between workers and the confined queen.
The modified cells were then returned to their colonies for 24 h, which gave the workers time to embed the wires into the wax of the cell. At the same time, queen cells from colony 2A and 2B were randomly chosen and cross-fostered between the two colonies. All cells had therefore been built in their original mother colonies. After this period, we simulated swarming by removing the queen and approximately half the workers but no brood. The remaining part of the hive containing the brood was fitted with an observation box with a removable panel on one side (Figure 1a). This formed an integral part of the nest cavity and allowed observation of all the queen cells, which were attached to two wooden bars in the observation box (Figure 1b). The box also contained two frames of unsealed brood (larvae and eggs). In experiment 2, a second set of queen cells was initiated 5 days after the first set to increase the sample size. After the observations on the first set had been completed, the second set was transferred to the observation box.
Observations
The observations were carried out by double-blind protocol as kinship was only determined afterward using microsatellite markers. During each day of observations, we sampled workers performing one of the three following behaviors on queen cells showing openings.
- Closing: the worker repaired slits made in the queen cell by the queen trying to exit (Figure 1d).
- Feeding: the worker was performing trophallaxis with the queen who had her tongue extended through a slit or small hole in the queen cell (Figure 1c).
- Vibrating: the worker grabbed the queen cell with its legs and then performed a short dorsoventral abdominal vibration (1–3 s) on the queen cell. This behavior is believed to regulate queen exit (Bruinsma et al., 1981).
Before the collection of each worker, we made sure that the worker had been directly in contact with the queen with its antennae through the slits in the cell. This was possible because workers would often be seen staying on the same queen cell for a long time. Workers interacting with the queens and queen cells were very active and so were not confused with other workers. Typically, one worker would first be seen closing the cell, then contacting the queen inside the cell, and then vibrating the cell and going back to close the cell. Feeding workers would show the same pattern. For this reason, the three behaviors recorded appeared to belong to the same repertoire of interactions with the queens and queen cells.
Workers were stored frozen at –20°C individually in Eppendorf vials until genetic analyses. We aimed to collect 30 or more workers observed interacting with each queen cell. Collection of samples ended after 4 days for each set of queens. After the observations, the queen cells were opened and the queens inspected for any physical deformation and frozen at –20°C for genetic analyses.
DNA microsatellite analysis
To determine the kin structure of the colonies, we used polymorphic DNA microsatellite markers. In addition to the sampled workers and queens, we also analyzed 94 newly emerged workers and 92–94 adult workers per colony taken randomly at the start of observations from the comb next to the queen cells. These samples allowed us to assess the number of matings and effective paternity in the study colonies and to test for patriline differences in the probability to perform the observed behaviors.
DNA was extracted from the antennae using chelex®100 (Châline et al., 2004; Walsh et al., 1991). Polymerase chain reactions were performed as described in Châline et al. (2004). The products were multiplexed and visualized using an Applied Biosystems ABI 3730 capillary sequencer and analyzed with the dedicated software GeneMapper v 3.0.
To reduce the number of markers used, we first screened the young worker sample and the queens at six microsatellite loci: A107, A14, A29, A76, Ap33, and B124 (Baudry et al., 1998; Estoup et al., 1994). Having determined the patriline structure of each colony, we then chose three marker loci sufficient to distinguish all patrilines in each colony, plus one extra locus for added confidence in patriline assignment. The markers used were A107, A14, A29, and A76 for colony 1 and A107, A29, A76, and Ap33 for colonies 2A and 2B.
The rest of the workers were genotyped at these four markers, and each worker was then assigned to a particular patriline. A few adult workers who could not be assigned as the colony queen's progeny were considered to have drifted from other colonies. In some cases, they could be assigned to another experimental colony as the colonies were all located in the same apiary.
Statistical analyses
The sampling technique, which did not permit constant observation of the cells, resulted in relatively few vibrating and feeding events (see Results). The higher proportion of closing behavior could also be due to the presence of the apparatus, which prevented even the most motivated queens to emerge. Because of the small sample sizes for feeding and closing, we pooled all the behavioral data per queen for the statistical analysis. This allowed more powerful tests. This pooling of data is biologically reasonable because we often saw individual workers performing a combination of behaviors (i.e., vibrating and closing or feeding and closing). For safety, we still confirmed the overall results for each behavior by comparing the proportion of full-sister interactions with the expected proportion from a random sample of bees (calculated with the effective paternity) with a chi-square test (Table 1, B).
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At any one time, many workers were interacting with each queen cell. The sampled workers thus constitute only a small subset of the interacting workers. This means that any differences in numbers of workers of a particular patriline would also reflect the frequency at which workers of this patriline interacted with the queen cells. To test for differences in the distribution of patrilines in the different groups of workers (young, random, interacting with the queen cells, and interacting with cross-fostered–queen cells), we used a Fisher's Exact test with an exact method using the program "Monte Carlo RxC 2.2" developed by W. Engels, University of Wisconsin. When differences between groups were significant, we analyzed differences in individual patriline proportions using a chi-square test with Yates' correction. Because differences in the patriline proportions were observed (see Results), we could not use the two control samples to test for nepotism in the interacting workers. Instead, we used the overall distribution of patrilines across all queens in the interacting worker samples.
To test for nepotism between workers and each queen, we used a 2 x 2 chi-square test with Yates' corrections to compare the proportion of interacting workers of the same patriline as the focal queen versus the proportion of interacting workers of the patriline interacting with all the queens of other patrilines. We then tested for each colony and for all queens for an overall trend in workers interacting with full-sister queens by using Gilley's (2003) nepotism index. In this case the index was the difference between the proportion of full sisters of the focal queen interacting with this queen and the proportion of workers from the same patriline interacting with queens of other patrilines. We used a two-tailed z test to detect significant differences. We also calculated the effect sizes for each of the tests performed using Cohen's d (1988), calculated with Becker's formulae (1988). We did not perform a retrospective power analysis as its use is now considered inconclusive and flawed (Nakagawa and Foster, in press).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Behavioral observations
During the experiments, 24 out of the 82 queen cells transferred to the colonies contained dead queens and were not attended by workers. These deaths probably happened during the fitting of the star apparatus, or before, as the queens inside these cells were unemerged pupae of various ages.
In experiment 1, we observed 15 cells with live queens in colony 1. In experiment 2, we observed 22 queens in total in colony 2A, four of which were cross-fostered, and 21 in colony 2b, three of which were cross-fostered.
We genotyped 2026 workers performing feeding (208, 10.3%), closing (1715, 84.6%), and vibrating (103, 5.1%) behaviors on 58 queen cells. The mean number of workers sampled per queen cell was 34.8 ± 9.8 (mean ± SD). Throughout the observations the queens could be heard piping, mostly quacking but sometimes tooting, which suggests that they were behaving in a normal way while being experimentally confined to their cells.
Colony kin structure
The queens of the three colonies had mated with 12, 11, and 20 males (Table 1A) with short-term, effective paternity frequencies of 9.46, 6.00, and 13.43, respectively, calculated from the young worker sample (Table 1A).
The random sample of workers was significantly different from the sample of young workers in both colonies 2A and 2B (Table 1A). The sample of interacting workers was also significantly different from the random sample of workers for all the three study colonies. When examining the cause of these differences, between three and six patrilines differed significantly between the two samples (Figure 2B) either by being over- or underrepresented in the sample of workers interacting with queen cells. The most striking difference is for patriline F in colony 2A, which was 29.8% of the random sample but 48.3% of the cell-attending workers. Patriline E of colony 2B, which was overrepresented in the interacting worker sample, also contributed to nine of the 13 drifted workers interacting with queen cells in colony 1. Fewer or zero drifted workers were found in the other colonies (Table 1).
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Nepotism
The frequencies of interactions between full sisters for each behavior (Table 1B) were not different from an expected random distribution, except in one case. This is for vibrating in colony 2B. However, the small sample of bees (n = 19) for this case suggests that this is an artifact. This absence of difference bolsters the fact that the three behaviors can be collapsed in a single "interacting" category.
There was no significant effect of relatedness on the probability of interacting with individual queens confined in their cells (Figure 2A). There was also no significant overall trend toward nepotism in individual colonies or overall, as measured by the nepotism index (Gilley, 2003; Table 2). The large sample size of the interacting workers makes it highly unlikely that this result is a false negative for anything other than a weak effect because the effect sizes (d) were in all cases small (Table 2; Cohen, 1988).
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Cross-fostered queens
When we compared the distribution of workers interacting with their sister queens against unrelated cross-fostered queens in the paired-colony experiment, there was a significant difference only in colony 2A (p = .024). This was mainly because workers of patriline F were less likely to interact with cross-fostered queens (p = .0004).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our results clearly show that although workers of different patrilines differ significantly in their likelihood of interacting with adult queens imprisoned in their cells, nepotism almost certainly does not occur. The absence of nepotism is further confirmed by the absence of any nepotistic trends in subsets of the overall data. There was no significant nepotistic effect in any of the study colonies or toward any single confined queen. The large sample size, both in terms of the 58 confined queens and the mean of 35 interacting workers per queen, and the small effect sizes make our conclusion robust. Furthermore, Gilley (2003)
, in a study of the influence of relatedness on worker aggression toward queens, using a power analysis found that a smaller sample size of 20.37 ± 9.96 (mean ± SD) allowed him to detect all but weak and biologically insignificant nepotism. The experimental setup closely mirrored natural conditions and resulted in behaviors of both confined queens and interacting workers that are naturally observed. The situation only differed by the absence of "roaming" queens in the colony and the fact that we "helped" workers in keeping the queens in their cells. However, workers cannot directly assess the presence of an emerged queen in the colony and rely on other cues like queen piping. Because queens were frequently piping during the experiment, it is highly likely that workers were behaving normally. This fact was also supported by previous observations of two observation hives that produced two and three secondary swarms spontaneously, with the queens remaining within their cells for up to 6 days. No behavioral differences were seen between the study colonies or the two observation hives. The protection of queen cells from the emerged queens, which could potentially be nepotistic as well, could not be observed because no emerged queens were present, but the same set of workers probably would have performed this behavior as interacting workers were very active on the cells. This makes us confident that the absence of nepotism was not an experimental artifact but a true reflection of what occurs naturally. In one instance (vibrating in colony 2B), there was a significant difference in the proportion of full sisters performing the behavior. Although the small sample size and the single occurrence of this make us doubt the relevance of this result, further experiments could be needed to confirm this.
There were differences in the tendencies of different patrilines to interact with the queen cells, both in over- and underrepresentation. In colony 2A, the most abundant patriline (F) was overrepresented in interacting workers, and this caused the mean relatedness between the workers interacting with a confined queen to increase from 0.42 to 0.53. However, no similar trend occurred in the other two colonies, where representation of the patrilines in the workers interacting with the queens was not linked to relative abundance in the colony. These marked differences could be due to genetic differences among patrilines in their tendency to perform different tasks. This has been documented for other behaviors like guarding and undertaking (Robinson and Page, 1988). This result also emphasizes the fact that when investigating nepotism, great care has to be taken in the selection of the controls as differences in the probability to perform a behavior can lead to erroneous conclusion as to whether nepotism occurs or not. An example of this in this study is patriline F in colony 2A, which represented more than 50% of the interacting workers who would have given positive nepotism toward F queens had we considered the newly emerged worker sample as a control.
Interestingly, the workers in colony 2A seemed able to discriminate between queens from their own colony and cross-fostered queens. However, because the queen cells were built in a different colony, discrimination may have been mediated by wax odor rather than by the queen inside. Wax odors are known to influence honey bee nest-mate recognition (Breed et al., 1998). Other studies using cross-fostered queens (Tarpy and Fletcher, 1998) found a significant effect of kinship on aggression by workers toward queens, which disappeared when workers were confronted only with full-sister and half-sister queens (Gilley, 2003).
Extreme multiple paternity, although increasing potential reproductive conflicts between patrilines (Visscher, 1986), may also hamper recognition and increase the cost of nepotism by decreasing the probability of encountering a full-sister queen (Ratnieks and Reeve, 1991). This may explain why nepotism studies using unnaturally low number of patrilines (two to three or unrelated bees; Noonan, 1986; Page et al., 1989; Schneider and DeGrandi-Hoffman, 2002, 2003) tend to find an effect while studies done with naturally mated queens (10–20 patrilines; Gilley, 2003) tend not to.
Another factor that could influence queen care is queen quality. Specialist workers could preferentially take care of higher quality queens regardless of kinship. We were unable to correlate any pattern of interaction to the quality of queens as measured by wing length or fresh weight. Future research might study the influence of queen piping on cell attendance and the interactions of workers with confined queens.
In conclusion, our data mirror most previous research on honey bees, but in the novel context of interactions with confined queens, in showing that the potential reproductive conflict in queen rearing caused by multiple paternity does not seem to translate into detectable nepotism (Tarpy et al., 2004).
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ACKNOWLEDGEMENTS |
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N.C. and S.J.M. were funded by the European Community network "Beekeeping and Apis Biodiversity in Europe". We thank Adam Hart for comments on the manuscript.
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