Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees

Abstract

The differentiation of workers into morphological castes represents an important evolutionary innovation that is thought to improve division of labor in insect societies. Given the potential benefits of task-related worker differentiation, it is puzzling that physical worker castes, such as soldiers, are extremely rare in social bees and absent in wasps. Following the recent discovery of soldiers in a stingless bee, we studied the occurrence of worker differentiation in 28 stingless bee species from Brazil and found that several species have specialized soldiers for colony defence. Our results reveal that worker differentiation evolved repeatedly during the last ~ 25 million years and coincided with the emergence of parasitic robber bees, a major threat to many stingless bee species. Furthermore, our data suggest that these robbers are a driving force behind the evolution of worker differentiation as targets of robber bees are four times more likely to have nest guards of increased size than non-targets. These findings reveal unexpected diversity in the social organization of stingless bees.Although common in ants and termites, worker differentiation into physical castes is rare in social bees and unknown in wasps. Here, Grüter and colleagues find a guard caste in ten species of stingless bees and show that the evolution of the guard caste is associated with parasitization by robber bees.

Fig. 1

Comparison of guards and foragers in 28 species of stingless bees. a Phylogenetic reconstruction based on a previously published phylogeny. The color gradient from blue to red indicates the probability that a species evolved increased guard size, based on 1,000 simulations using a Bayesian framework. Numbers 1–5 indicate independent appearances of increased guard size. b Tetragonisca fiebrigi guards standing on the wax entrance tube (Photo: C. Grüter). c Size-frequency distribution of T. fiebrigi foragers and guards showing a bimodal distribution. Values (unit = mm) are centred for each colony (colony mean and total mean = 0) to correct for overall colony differences (N = 58 forager/65 guards/6 colonies). d Frieseomelitta flavicornis guard and forager (Photo: C. Grüter). e Size-frequency distribution of F. flavicornis foragers and guards, showing a unimodal distribution. Values (unit = mm) are centred for each colony (N = 37/39/6). f Head of a Frieseomelitta varia forager and guard (Photo: C. Grüter). g Melanization frequency distribution of F. varia guards and foragers. Values (unit = melanization level, see methods) are centred for each colony (N = 30/56/6)

Fig. 2

Factors explaining differences between species in worker diversity. a Relationship between queen-worker dimorphism (log-transformed) and worker diversity (log-transformed standard deviation of head width) (N = 12 species). The phylogeny is based on ref. and a generalized least squares model (GLS) assuming Brownian motion was applied. The best fit line is based on a linear regression through the origin based on phylogenetically independent contrasts (PICs). Queen-worker dimorphism explained 63% of the variation in worker size variation between species. b Relationship between colony size (log-transformed) and worker diversity (log-transformed standard deviation of head width) (N = 27 species). A GLS model revealed no relationship between colony size and worker diversity