Expression profile of the sex determination gene doublesex in a gynandromorph of bumblebee, Bombus ignitus. Ugajin A(1), Matsuo K(2). Fertilisation of the egg (or lack of) determines the. Bumblebees as model organisms to study male sexual selection in social Males thus determine not only mating frequency (only once) of.
Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and . However, many other species of bees, including bumblebees, such as Bombus terrestris, are monandrous. This means that sisters are almost. Bumblebees produce male-biased sex ratios (Bourke. ; Beekman and Van .. behaviors, determined the occurrence of copulations, but the experimental. Review of the data on sex investment ratios in bumble bees 3. Male bias as a possible . duction may be largely determined before workers are present.
The regulation of colony development in the bumblebee,Bombus terrestris. Diploid males in the bumble beeBombus terrestris: Sex determination, sex alleles. Bumblebees produce male-biased sex ratios (Bourke. ; Beekman and Van .. behaviors, determined the occurrence of copulations, but the experimental. produce diploid males after brother‐sister (50%) and nephew‐niece (%) matings proves that in B. terrestris the sex is determined by a single multi‐alleli.
Gynandromorphy that has both male and sex features is sex in many insect orders, including Hymenoptera. In most cases, however, only external morphology and sex aspects have determination studied.
We found a gynandromorph of bumblebee, Bombus ignitus, that showed almost determination distribution of external sexual traits, with male characters observed on the left side and female characters on the right side. This individual never exhibited sexual sex toward new queens. The dissection of the head part showed that it had bilaterally dimorphic labial glands, only bumblebees left of which was well developed and synthesized male-specific pheromone components.
In contrast, bumblebees gynandromorph possessed an ovipositor and a pair of ovaries in the bumblebees part, suggesting that it had a uniformly female reproductive system. Furthermore, we determination several internal organs of the bumblebees by a molecular biological approach. The expression analyses of a sex determination gene, doublesex, in the brain, the fat bodies, the hindgut, and the ovaries of the gynandromorph revealed a male-type expression pattern exclusively in the left brain hemisphere and consistent female-type expression in other tissues.
These findings clearly indicate the sexual discordance determination external traits and internal organs in the gynandromorph. The results of genetic analyses using microsatellite markers suggested that this individual consisted of both genetically male- and female-type tissues.
We found a gynandromorph of bumblebee, Bombus ignitus, that showed almost bilateral distribution of external sexual traits, with male characters observed on the left side and female characters on the right side.
This individual never exhibited sexual behavior toward new queens. The dissection of the head part showed that it had bilaterally dimorphic labial glands, only the left of which was well developed and synthesized male-specific pheromone components. In contrast, the gynandromorph possessed an ovipositor and a pair of ovaries in the abdominal part, suggesting that it had a uniformly female reproductive system.
Furthermore, we characterized several internal organs of the gynandromorph by a molecular biological approach. Because including radial cell size of queens in our formal analyses would have given a much higher number of entire-colony deletions due to missing values, we chose to ignore this variable.
We note, however, that this does not exclude that variables connected to queen weight or queen fat reserves could have a significant effect on development and reproduction of colonies. In particular, we expect that the ratio between queen size and weight or fat reserves directly after diapause could be a useful proxy for life expectancy, so that relatively light queens would have early switch points and male-biased colonies, and relatively heavy queens would have late switch points and female-biased colonies.
Life expectancy of queens is thus likely to be affected by three factors: feeding and rearing conditions in the maternal colony Ribeiro et al. The first two factors cause variation in queen life expectancy within years and laboratory cohorts, whereas the third factor induces variation across years and laboratory cohorts. When variation in the third factor is small relative to the variation in the first two factors, it seems likely that split sex ratios with averages around would also be found in field populations.
The duration of queen hibernation thus seems to have an important indirect and cumulative effect on colony development and sex allocation. Lack of standardization for this and related factors in laboratory cultures may therefore explain at least part of the large variation reported in sex allocation ratios across and within bumblebee species see Bourke, Clearly, if our laboratory cohorts had all been reared after a hibernation period of 4 months, the cohort-specific differences in mean sex allocation would have been less pronounced than in Figure 3b.
When using the smaller SDs across cohorts after partialing out the effects of diapause duration on the production of queens and males Figure 4 , the overall proportional investment in queens is significantly lower one-tailed test than 0. This implies that with controlled overwintering conditions, the distribution of cohort-specific sex allocation means may be just narrow enough to reject the hypothesis of full worker control on the basis of data from a single cohort of colonies only.
In a recent conceptual study, Bourke and Ratnieks concluded that by switching early i. In their view, workers comply to this male-biased reproductive agenda of their mother because early males have a higher than average mating success, and they can only detect their mother's switch to haploid eggs with some delay, so that replacing brothers by worker sons would incur both a significant efficiency cost and lower fitness returns because of reduced mating success of the later replacement males.
Bourke and Ratnieks suggest that the second factor constrained information is the most important one, but our present results indicate that both factors may be of similar importance. The argument by Bourke and Ratnieks is based on Duchateau and Velthuis's study of 21 colonies of B.
However, our present much larger data set shows that early-switching colonies have significantly larger first and second worker broods than late-switching colonies, so that workers should have at least partial information about the likely future development of their colony, independent of their ability to recognize haploid and diploid brood. The balance in favor of raising queen-sons in spite of their low kin value apparently stays favorable for quite some time, because workers in early-switching colonies seem to actively postpone interfering with their mother's haploid egg production.
This is remarkable because workers in colonies heading for a male-biased sex ratio tend to develop their ovaries Duchateau and Velthuis, ; Van Doorn and Heringa, ; Van Honk et al.
This means that replacing queen eggs by worker eggs will only be worthwhile if productivity multiplied by mating success will be at least two-thirds of the value obtained when rearing exclusively brothers. From what is known or inferred about loss of colony coherence and productivity after the onset of worker reproductive activities Duchateau and Velthuis, ; Van Doorn and Heringa, and about the higher mating success of early males Bourke, ; M. Duchateau, H.
Velthuis, and J. Marien, unpublished data , this two-thirds threshold may well be impossible to overcome until quite late in colony development. In other words, workers in male-biased colonies would have even lower inclusive fitness if they rebelled against their fate too early, an example of high potential conflict between queen and workers, but low actual conflict because the cost of manipulation outweighs the benefits Ratnieks and Reeve, We have summarized these interpretations of the key processes affecting sex allocation in B.
The concave downward curves in the lower panel describe the likely reproductive value mating success multiplied by relatedness of males as a function of time in the season, relative to the constant reproductive value of queens assumed to be 1.
The upper curve in this panel gives the value of worker-produced males to other workers M W to W; assuming that life-for-life relatedness is 0. The time spans t 1 , t 2 , and t 3 indicate the increasing maximal delays that are allowed to raise a worker-son of the same reproductive value as the queen-son that it replaces.
In early-switching colonies the competition point is predicted to be delayed until a time threshold, t n , from which it pays to replace queen-sons by worker-sons. Because of the information constraints discussed by Bourke and Ratnieks , it may take quite some time to reach t n , which explains that the most male-biased colonies have a relatively early switch point, a rather late competition point, and thus a large difference between these two switches see Figures 5 and 6 ; see also Figure 1 in Bourke and Ratnieks, The reproductive values in the lower panel of Figure 7 are determined by reproductive decisions about 35 days earlier: the queen-imposed switch point to haploid eggs S and the worker-imposed competition point C.
In the upper panel of Figure 7 , we have approximated the cumulative probabilities of S and C across a typical sample of colonies that correspond to the reproductive values in the lower panel 35 days later. In female-biased, queen-producing colonies, workers gain higher inclusive fitness than in male-biased colonies.
In our interpretation, these are colonies with relatively healthy queens that have emerged from overwintering with an above-average life expectancy and thus relatively good prospects for productivity during the additional 3 weeks or so that are typically required for this pathway of colony development. The reduced production of nonvolatile pheromones by queens Cnaani et al. This interpretation would thus be an extended version of the idea by Bourke and Ratnieks that the cessation of pheromone production is a signal to the female larvae to start development as queens and that workers eavesdrop on this signal.
It is important to realize that protandry implies that at this point in time the expected mating success of any male yet to be produced has already dropped substantially, so that both queen and workers maximize their fitness by producing new queens.
Queens and workers thus agree about the best reproductive option the hatched area in Figure 7 , but they disagree about the second best option, males. This argument remains rather implicit in the model by Bourke and Ratnieks, but it seems to be the best ultimate explanation for the enforcement of the competition point by workers rather predictably 12 days after the first eggs that develop into queens are laid.
At this point in time, the new queen production is secure, and the queen may have switched or is about to switch to producing haploid eggs.
When the point has been reached that worker egg-laying no longer jeopardizes the efficient rearing of queen brood i. This is an optimal strategy regardless of the success of male production at the end of the colony cycle. Even if the number of late males produced in field colonies and their mating success are both likely to be low, any mechanism that allows queens and workers to increase their share in this limited reproductive option will be selected for when alternative options are no longer available.
The expression of worker—queen conflict over male production at this point thus has essentially a very low cost, an inference that also follows from the Bourke and Ratnieks study. As argued by Bourke and Ratnieks , information constraints in the detection of haploid queen-eggs by workers are less likely to apply in late-switching colonies because all parties queen, workers, and even the diploid larvae agree that raising queens is the best strategy.
The number of queen larvae will probably be fine tuned by the quality of the available resources and the number of workers available to forage.
This means that there also is a large degree of agreement on the termination of this queen-production project, so that the workers should be able to predict the switch point of their mother much better than in early-switching colonies. The relative constancy of the period between the onset of queen production and the competition point and the inferred steady decline of a queen signaling pheromone during this period Cnaani et al, are therefore not surprising.
The optimal strategy of late-switching colonies is also illustrated in Figure 7. Queens and workers agree on raising new queens when the highest male curve in the lower panel of Figure 7 has crossed the queen reproductive value line of 1 the hatched area.
From then on, queens should postpone their switch to haploid eggs until the colony has realized the maximum production of new queens for which it has resources. Following Bulmer , and Bourke and Ratnieks , we conclude that the early male advantage that has been inferred to characterize the B.
Queens in about half of the colonies prevent the production of new queens because they no longer lay diploid eggs at the crucial point in time when potential queen larvae could be raised Bourke and Ratnieks, The early-switching colonies thus function as a balancing sex ratio class Boomsma and Grafen, , imposing the overall queen optimum of a sex allocation ratio in the population. Our model in Figure 7 encompasses the conceptual framework of Bourke and Ratnieks while adding considerable empirical detail based on a large data set.
Our study primarily addressed sex allocation and explored the consequences of reduced mating success of late males, whereas the primary emphasis of the Bourke and Ratnieks study was on information constraints and worker reproduction although they considered sex allocation, costs, and the timing of male production. Combining the information from these two studies, we have now reached a relatively firm understanding of the paradox that bumblebee reproduction is on one hand fully consistent with kin selected worker behavior, but on the other hand it is constrained by semelparity and protandry, so that workers hardly have any power to significantly affect sex allocation or male production.
Transition pattern when queens of Bombus terrestris switch from laying exclusively diploid eggs to laying exclusively haploid eggs. The data average percentage of haploid eggs are from 11 laboratory colonies, which have been used in the study of Duchateau and Velthuis ; see same reference for documentation of a similarly steep transition from worker-producing to queen-producing eggs.
In the 11 colonies of this data set, all brood chambers were mapped daily, so that later emerging brood could be traced back to specific egg-laying events. The time axis was standardized according to the first day on which any haploid egg was laid.
The pattern observed confirms earlier work by Plowright and Plowright that colonies whose queen has switched to haploid eggs do not later revert to diploid eggs. The hypothesized causal links between sequential key variables of colony development used in the LISREL 8 path analysis. Hibernation-duration Hibernation was considered to be the only independent variable x 1.
Dependent variables, y 1 — y 8 , are described in text. See also Duchateau and Velthuis for details on these variables. Sex ratio variation among colonies of Bombus terrestris raised in the laboratory in 13 separate cohorts. The parallel lines are approximate investment isolines where the sum of investment in both sexes is equal, assuming either that an individual queen is 2.
The inset histogram is the frequency distribution of the sex allocation ratio across colonies according to the 1. Variables are described in text. The t values for specific causal relationships are given as figures black and gray background for positive and negative effects, respectively on the arrows linking the boxes in the plot. A heuristic model explaining the basic pattern of sex allocation in the protandrous reproduction cycle of the bumblebee Bombus terrestris. The upper panel gives the cumulative probability that the switch point S and the competition point C have taken place, as a function of the time passed since the first worker hatched.
The lower panel evaluates the consequences of these reproductive decisions about 35 days later. These 35 days are based on the sum of the average development time about 25 days for males and about 30 days for queens and the average time required to become sexually active after hatching about 10 days for males and about 5 days for queens.
All times are approximations based on Utrecht rearing conditions. Time scales will be longer under field conditions in the Netherlands and shorter in warmer e. The hatched area indicates the time period when queen and workers agree to produce primarily new queens. See text for further explanation.
Hibernation duration is indicated with an accuracy of 0. From the available pedigree records of lab cohorts, the number of genetically independent haplotypes per cohort was approximated as a measure of the genetic diversity per cohort. These estimates assume single queen-mating, so that each genetically independent colony contributes three haplotypes.
The level of inbreeding per cohort was approximately assessed as the percentage of colonies that produced diploid males. Herman Wijnne and Paul Westers gave invaluable help with the path analysis, David Nash helped with the final versions of figures, and Vicky Backus, Madeleine Beekman, Andrew Bourke, Paul Schmid-Hempel, and two anonymous reviewers made valuable suggestions for improvement of previous versions of this article.
The stay of J. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents. Address correspondence to J. Boomsma at the University of Copenhagen.
E-mail: JJBoomsma zi. Oxford Academic. Google Scholar. Hayo H. Jacobus J. Cite Citation. Permissions Icon Permissions. Abstract Patterns of sex allocation in bumblebees have been enigmatic and difficult to interpret in either a Fisherian context or in a kin-selection perspective.
Figure 1. Open in new tab Download slide. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. Table 1. Characteristics of the 31 cohorts of laboratory colonies that were included in the analyses. Open in new tab. Backus V, Beekman M, van Stratum P, Bloch G, Boomsma JJ, Boomsma JJ, Grafen A, Boomsma JJ, Nachman, , Bourke AFG, Bulmer MG, Crozier RH, Pamilo P, Deslippe RJ, Savolainen R, Duchateau MJ, Evans JD, Hamilton WD, Helms KR, Herbers J, Kukuk PF, Mueller UG, Nonacs P, Pamilo P, Richards KW, Strassmann JE, Trivers R, Hare H, Issue Section:.
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