Complex social behaviour derived from maternal reproductive traits

Abstract

A fundamental goal of sociobiology is to explain how complex social behaviour evolves, especially in social insects, the exemplars of social living. Although still the subject of much controversy, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes to result in sib-care, the hallmark of highly evolved social life in insects. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.

Figure 1. Distributions of ovariole number and patterns of previtellogenic ovarian activation in worker bees

a, Ovariole number in mature 10- to 21-day-old bees from strains selected for high or low levels of pollen hoarding (n = 109 bees per strain). b, Samples from wild-type bees collected at presumably their first foraging flight (n = 314). The mean numbers of ovarioles (±s.e.m.) for groups with 1–4, 5–7 and 8 or more ovarioles are 2.75 ± 0.06, 5.76 ± 0.08 and 9.30 ± 0.30, respectively. The joint distributions of ovarian activation are superimposed on the original densities and refer, therefore, to bees within the genotype-specific data sets.

Figure 2. Correlations between ovariole number and the social behaviour of wild-type bees

a, Honey bee age at presumably the first foraging flight. b, The probability of being a pollen forager. c, The sugar concentration of nectar collected by the worker bees. Data show mean ± s.e.m. Different letters (a, b) refer to groups that were different according to a Fisher’s post-hoc test (P < 0.05). Points connected by a dotted line in c denote the highest nectar concentration collected by any single bee in the respective ovariole groups.