Worker policing, worker reproduction, and nepotism in honey bees
Worker policing is any worker behaviour that reduces reproduction by other nestmate workers (Ratnieks 1988). Worker policing in the honey bee (Apis mellifera) occurs via egg eating. Worker-laid eggs, from queenless colonies, were quickly eaten when transferred to drone cells in queenright "discriminator" colonies but more than 50% of non-kin queen-laid male eggs survived (Ratnieks & Visscher 1989). However, worker-laid eggs treated with queen Dufour's gland extract had increased survival suggesting that queens mark their eggs with a pheromone from this gland (Ratnieks 1995) and that workers discriminate between queen and worker-laid eggs according to the presence or absence of this signal (Ratnieks 1995; Seeley 1995). Worker reproduction and worker policing both occur in normal queenright colonies (Ratnieks 1993). Although the proportion of workers in normal queenright colonies with fully-activated ovaries is only 0.01% (Ratnieks 1993) this represents several workers who can collectively lay a substantial fraction of the colony's male eggs (estimated at 7%, Visscher 1996). These are almost all policed before hatching (Ratnieks 1993, Visscher 1996) and in normal queenright colonies only one adult male in a thousand is a worker's son (Visscher 1989). Workers do not discriminate between queen's and worker's sons in the larval stage (Ratnieks & Visscher 1989).
In terms of inclusive fitness, honey bee workers gain from policing other workers' eggs because a worker is more related to her mother queen's sons (0.25) than to other workers' sons (0.15) (Ratnieks 1988). (Honey bee queens mate with approximately 10-30 males; the relatedness of 0.15 occurs at an effective paternity frequency of 10). Both the signal producer (queen) and the receivers (police workers) benefit from the egg-marking pheromone because it helps the colony to rear more related males (queen perspective: sons (0.5) versus grandsons (0.25); police worker perspective: brothers (0.25) versus nephews (0.15)). However, a worker is more related to her own sons (0.5) than to brothers (0.25) so there should still be selection for worker bees to lay eggs if attempted
reproduction has little cost to the colony.
In rare cases large numbers of adult males are produced by workers in queenright colonies. Three
such colonies have been studied (Page and Erickson 1988; Oldroyd et al. 1994; Montague and Oldroyd 1998). Oldroyd et al. (1994) showed that 49 of 50 male pupae analyzed were sons of workers of a single patriline. Montague and Oldroyd (1998) obtained similar data from an unrelated colony. Oldroyd and Osborne (1999) bred a line of honey bees whose colonies rear hundreds or thousands of workers' sons at any time and 3-9% of workers have fully-activated ovaries. This suggests that a rare heritable trait or traits can cause workers to have increased ovary activation and to lay eggs that evade policing. Queenright colonies in which large numbers of workers' sons are reared were dubbed `anarchistic´ (Oldroyd et al. 1994) because they lack the typical order of a honey bee colony in which the queen is effectively the sole reproductive. Oldroyd and Ratnieks (submitted) show that worker-laid eggs from anarchistic colonies are almost as acceptable in normal queenright colonies as queen-laid eggs. This suggests that anarchistic workers lay eggs that mimic queen-laid eggs, possibly by countefeiting the egg-marking pheromone.
Mr Nicolas Chaline
Professor T A Burke and Dr F Ratnieks
This project is funded by a studentship from the EC.