Giving your daughters the edge: bequeathing reproductive dominance in a primitively social bee

Abstract

The ¢tness associated with behavioural strategies is usually estimated in terms of o¡spring number and size. However, in group-living animals the reproductive value of o¡spring may also depend on their social rank. We show here that in an allodapine bee Exoneura robusta, dominant mothers can behaviourally in£uence their daughters' reproductive rank by controlling insemination of other potential mothers. In E. robusta, group living is near mandatory and reproductive dominance among female nestmates is determined by order of adult emergence. Nests are single, undivided burrows and the dominant female assumes a guarding position closest to the nest entrance. We show that before the egg-laying period, subordinate females who have been absent from the nest are`screened' by the reproductive guard upon attempted re-entry. Those who have been in contact with foreign males are less likely to be granted access back into the nest than those who have been in contact with foreign females or with no bees at all. We argue that by controlling insemination patterns of their nestmates, dominant females ensure that their own daughters eclose ¢rst and are therefore more likely to assume dominance in the next generation. This presents a situation where dominance is bequeathed to daughters by behavioural means. The ability of mothers to in£uence social hierarchies in subsequent generations introduces a ¢tness component additional to the number and size of o¡spring produced.

Altruism in insect societies and beyond: voluntary or enforced?

“…Enforced cooperation in insect and vertebrate societies and interspecific mutualisms. (a) Worker policing prevents workers from reproducing in the honeybee Apis mellifera [6]; (b) queen policing (inset) prevents most workers from reproducing successfully in the bumblebee Bombus terrestris [18]; (c) a worker with active ovaries is aggressed in the queenless ant Harpegnathos saltator [19]; (d) in the honeybee, differential feeding forces most larvae to develop as workers; only larvae reared in royal cells (arrow) can develop as queens [1,7]; (e) subordinate workers from the allodapine bee Exoneura bicolor are evicted from the nest when they have been in contact with a foreign male [39]; (f) a worker that attempted to overthrow the breeder female is punished in the queenless ant Dinoponera quadriceps [40]; (g) in the cooperatively breeding cichlid Neolamprologus pulcher, subordinates that do not help look after the eggs and fry are evicted [57]; (h) rhesus monkeys (Macaca mulatta) who do not share food are punished [58]; (i) in meerkats (Suricata suricata) dominant females prevent successful breeding by subordinates [62]; (j) soybean plants (Glycine max) sanction root nodule bacteria that do not fix nitrogen, as shown by this split root experiment [55]. …”

“…For example, in the Asian paper wasp Polistes chinensis, the queen kills up to 70% of the eggs laid by workers [38]; in the allodapine bee Exoneura robusta, the queen can prevent workers that have mated from re-entering the nest [39]; in the ponerine ant Dinoponera quadriceps, workers that attempt to over-…”

Evolution of sociality in the allodapine bees: a review of sex allocation, ecology and evolution

“…This is because diploid eggs that are produced early on in the season should have a greater chance of completing development first, and therefore a greater chance of assuming dominance in the next generation. Bull et al (1998) examined this hypothesis by testing whether guarding queens discriminated between potentially mated and unmated foragers returning to the nest. They found that guarding queens refused nest entry to foragers who had been in physical contact with foreign males, but did not refuse entry to females who had been in contact with foreign females or no other bees at all.…”

“…They found that guarding queens refused nest entry to foragers who had been in physical contact with foreign males, but did not refuse entry to females who had been in contact with foreign females or no other bees at all. Bull et al (1998) argue that this guard-mediated form of reproductive hierarchy can operate because group nesting is largely mandatory. Controlling membership of a group allows queens to exclude potential rivals and the consequences of being denied access to the nest may provide strong disincentives for subordinates to mate.…”

Maternal effects in cooperative breeders: from hymenopterans to humans

“…For example, during this phase, mothers appear to suppress offspring growth in ponerine ants (O'Donnell 1998) and naked mole-rats (O'Riain et al 2000). In addition, mothers can evict competitors (allodapine bee Exoneura robusta, Bull et al 1998), kill them (naked mole-rats, Sherman et al 1991) or have them killed by workers (ponerine ants Dinoponera quadriceps, Monnin et al 2002). That reproductive conflict can clearly exist in such species (Ratnieks et al 2006) suggests that if maternal effects occur during early reproductive phases in such systems, they are largely inadequate to wholly control offspring phenotype.…”