C1139 Social Insects. Male Production by Workers: Predictions & Tests. Lecture 11
Male production by workers: predictions and tests
Aims
1. To show how to use inclusive fitness theory to investigate male production by workers.
2. To show how these predictions have been tested empirically.
Objectives
1. Learn the theory and examples.
2. Integrate with material from previous lectures on kin value and sex allocation.
Big Picture
In a previous lecture we used inclusive fitness theory to determine worker-optimum sex-allocation, and
examined data testing these predictions. Here we use the theory to make predictions about male production. This
is easier than for sex allocation because we are comparing the kin value of different types of males that could be
reared, not males versus females. Therefore, we only need consider how relatedness varies among males. (Sex
specific reproductive value and average mating success are equal for all males in the population.) We will also
see how policing can prevent workers from reproducing successfully by killing worker-laid eggs, and how this
can prevent workers from laying eggs in the first place (acquiescence). Thus, in a honey bee colony with a
queen, even though 100% of the workers have ovaries less than 0.1% have active ovaries and lay eggs.
Whose sons to rear?
Workers in many social Hymenoptera possess ovaries but cannot mate. Workers almost always lay eggs in a
colony that is queenless, and the colony rears a batch of males before dying out. But should the workers produce
the males in a queenright colony?
Relatedness of workers to males reared in a colony with a single queen
type of male
regression relatedness to donor worker
own sons
1
brothers (= mother queen's sons)
0.5
full nephew (= full-sister workers' sons)
0.75
half nephew (= half-sister workers' sons)
0.25
life for life relatedness
0.5
0.25
0.375
0.125
How does the mating frequency of the mother queen affect relatedness between a worker and males?
own sons
no effect (always 1)
queen's sons
no effect (always 0.5—as a male has no father)
other workers' sons
relatedness reduces as queen mating frequency increases
queen mating frequency < 2
queen mating frequency > 2
own sons > other workers' sons > mother queen's sons
own sons > mother queen's sons > other workers' sons
Prediction from the above: on relatedness grounds alone, workers would benefit by preventing other workers
from producing males when queen mating frequency is > 2 (Ratnieks 1988). But note that a worker is always
more related to her own sons than other males. This means that there is an incentive to lay eggs.
Why so few workers’ sons in honey bee colonies?
Almost all the males reared in a normal queenright colony (99.9%) are the queen’s sons (Visscher 1989). Why
are not more workers’ sons reared, especially as a worker is more related to her sons than to her brothers? Maybe
workers stop each other from reproducing. That is, they police each other. Worker policing could be effective
even in a large colony. Queen policing, in which the mother queen, tries to stop the workers from reproducing
could be effective only in small colonies.
Discovery of worker policing in the honey bee
1
C1139 Social Insects. Male Production by Workers: Predictions & Tests. Lecture 11
Workers were found to kill worker-laid eggs (Ratnieks & Visscher 1989). The worker-laid eggs had been
experimentally transferred from queenless colonies into a queenright colony, and compared to queen-laid male
eggs that had also been transferred into adjoining cells. Subsequently, it was found that worker-laid eggs appear
and disappear in normal colonies with a queen (Ratnieks 1993, Visscher 1996). That is, some eggs are being laid
by workers but most are being killed.
How widespread in worker policing by egg eating
It is now known from many species of bee, wasps and ant. In some species, worker policing may also take place
via aggression towards workers with active ovaries (Ratnieks et al. 2006; Wenseleers & Ratnieks 2006).
Conditions that favour worker policing of worker-laid eggs
On relatedness grounds alone, worker policing should be favoured when queens are mated to two or more males.
When this occurs, workers will be more related to the mother queen’s sons that to other workers’ sons. There is
now considerable evidence for this, including a recent study comparing 90 species by Wenseleers & Ratnieks
(2006) and a study of the British wasp Dolichovespula saxonica (Foster & Ratnieks 2000) in which some
colonies have a queen mated to a single male and some to multiple males. Workers’ sons are rarer in the latter
colonies.
Consequences of policing: evasion
In some honey bee colonies workers can lay eggs that are not policed (Martin et al 2001). Presumably, they lay
eggs that smell like queen-laid eggs (Oldroyd & Ratnieks 2000). Possibly, ant workers can make their eggs
acceptable by placing them in the egg pile in order to obtain odours from touching queen laid eggs. However, a
study of this in the ponerine ant Pachycondyla inversa showed that worker-laid eggs sandwiched between two
queen-laid eggs were not more acceptable afterwards, and had not changed chemically (D’Ettorre et al 2006).
Consequences of policing: acquiescence
If you lay eggs and they are killed, why lay them in the first place? Policing does not just kill worker-laid eggs. It
stops workers laying eggs in the first place. In honey bee colonies, less that 0.1% of the workers have active
ovaries (Ratnieks 1993). Comparative study of 10 species (9 wasps and the honey bee Apis mellifera), showed
that fewer workers had active ovaries when policing was more effective at killing worker-laid eggs (Wenseleers
& Ratnieks 2006).
References
Worker policing in honey bees
Martin, S. J., Beekman, M., Wossler, T. C., Ratnieks, F. L. W. 2002. Parasitic worker honey bees, Apis mellifera
capensis, avoid policing. Nature 415: 163-165.
Miller, D. G., Ratnieks, F. L. W. 2001. The timing of worker reproduction and breakdown of policing behaviour
in queenless honey bee (Apis mellifera L. ) societies. Insectes Sociaux 48: 178-184.
Oldroyd, B. P., Halling, L. A., Good, G., Wattanachaiyingcharoen, W., Barron, A. B., Nanork, P., Wongsiri, S.,
Ratnieks, F. L. W. 2001. Worker policing and worker reproduction in Apis cerana. Behavioral Ecology &
Sociobiology 50: 371-377.
Oldroyd, B. P., Ratnieks, F. L. W. 2000. Anarchistic honey bee workers evade worker policing by laying eggs
that have low removal rates. Behavioral Ecology & Sociobiology 47: 268-273.
Oldroyd, B. P., Smolenski, A. J., Cornuet, J.-M., Crozier, R. H. 1994. Anarchy in the beehive. Nature 371: 749.
Ratnieks, F. L. W. 1995. Evidence for a queen-produced egg-marking pheromone and its use in worker policing
in the honey bee. J. Apicult. Res. 34: 31-37.
Ratnieks, F. L. W. 1993. Egg-laying, egg-removal, and ovary development by workers in queenright honey bee
colonies. Behav. Ecol. Sociobiol. 32: 191-198.
Ratnieks, F. L. W., Visscher, P. K. 1989. Worker policing in the honey bee. Nature 342: 796-797.
Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am.
Nat. 132: 217-236.
Visscher, P. K. 1989. A quantiative study of worker production of males in the honey bee. Behav. Ecol.
Sociobiol. 25: 247-254.
2
C1139 Social Insects. Male Production by Workers: Predictions & Tests. Lecture 11
Visscher, P. K. 1996. Reproductive conflict in honeybees: a stalemate of worker egg-laying and policing. Behav.
Ecol. Sociobiol. 39: 237-244.
Worker policing in wasps
Foster, K. R., Gulliver, J., Ratnieks, F. L. W. 2002. Why workers do not reproduce: worker policing in the
European hornet Vespa crabro. Insectes Sociaux (accepted).
Foster, K. R., Ratnieks, F. L. W. 2001. Paternity, reproduction and conflict in vespine wasps: a model system for
testing kin selection predictions. Behavioral Ecology & Sociobiology 50: 1-8.
Foster, K. R., Ratnieks, F. L. W. 2001. Convergent evolution of worker policing by egg eating in the honeybee
and common wasp. Proceedings of the Royal Society of London B 268: 169-174.
Foster, K. R., Ratnieks, F. L. W. 2000. Facultative policing in a social wasp. Nature 407:692-693
Worker policing in ants
D’Ettore, P., Tofilski, A., Heinze, J., Ratnieks, F. L. W. Non-transferrable signals on ant queen eggs.
Naturwissenschaften (accepted)
Monnin, T., Ratnieks, F. L. W. 2001. Policing in queenless ponerine ants. Behavioral Ecology & Sociobiology
50: 97-108.
Worker policing reviews/general
Barron, A.., Oldroyd, B. P, Ratnieks, F. L. W. 2001. Worker reproduction in honey-bees (Apis) and the anarchic
syndrome: a review. Behavioral Ecology & Sociobiology 50: 199-208.
Foster, K. R., Ratnieks, F. L. W. 2001. The effect of sex allocation biasing on the evolution of worker policing.
American Naturalist 158: 615-624.
Ratnieks, F. L. W. 2000. Worker policing in the honey bee: basic facts and ideas. Insect Social Life 3: 3-10
Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am.
Nat. 132: 217-236.
Ratnieks, F. L. W., Wenseleers, T., Foster, K. R. 2006. Conflict resolution in insect societies. Annual Review of
Entomology 51: 581-608.
Ratnieks, F. L. W., Monnin, T., Foster, K. R. 2001. Inclusive fitness theory: novel predictions and tests in
eusocial Hymenoptera. Annales Zooogici Fennici 38: 201-214.
Ratnieks, F. L. W., Reeve, H. K. 1992. The structure of conflict in hymenopteran societies: processes that reduce
conflict in advanced eusocial species. J. Theor. Biol. 158: 33-65.
Wenseleers, T., Ratnieks, F. L. W. 2006. Comparative analysis of worker policing and reproduction in eusocial
Hymenoptera supports relatedness theory. American Naturalist 168: E164-E179.
Wenseleers, T., Ratnieks, F. L. W. 2006. Enforced altruism in insect societies. Nature 444: 50.
3