Born to be bee, fed to be worker? The caste system of a primitively eusocial insect

Frontiers in Zoology Born to be bee, fed to be worker? The caste system of a primitively eusocial insect Nayuta Brand 0 Michel Chapuisat 0 0 Department of Ecology and Evolution, University of Lausanne , Lausanne 1015 , Switzerland Introduction: Primitively eusocial halictid bees are excellent systems to study the origin of eusociality, because all individuals have retained the ancestral ability to breed independently. In the sweat bee Halictus scabiosae, foundresses overwinter, establish nests and rear a first brood by mass-provisioning each offspring with pollen and nectar. The mothers may thus manipulate the phenotype of their offspring by restricting their food provisions. The first brood females generally help their mother to rear a second brood of males and gynes that become foundresses. However, the first brood females may also reproduce in their maternal or in other nests, or possibly enter early diapause. Here, we examined if the behavioural specialization of the first and second brood females was associated with between-brood differences in body size, energetic reserves and pollen provisions. Results: The patterns of variation in adult body size, weight, fat content and food provisioned to the first and second brood indicate that H. scabiosae has dimorphic females. The first-brood females were significantly smaller, lighter and had lower fat reserves than the second-brood females and foundresses. The first-brood females were also less variable in size and fat content, and developed on homogeneously smaller pollen provisions. Foundresses were larger than gynes of the previous year, suggesting that small females were less likely to survive the winter. Conclusions: The marked size dimorphism between females produced in the first and second brood and the consistently smaller pollen provisions provided to the first brood suggest that the first brood females are channelled into a helper role during their pre-imaginal development. As a large body size is needed for successful hibernation, the mother may promote helping in her first brood offspring by restricting their food provisions. This pattern supports the hypothesis that parental manipulation may contribute to promote worker behaviour in primitively eusocial halictids. Evolution of eusociality; Caste differentiation; Parental manipulation; Provisioning behaviour; Sweat bees; Halictids; Halictus scabiosae - Introduction The hallmark of eusociality is reproductive division of labour between generations, a surprising social organization by which some individuals become functionally sterile helpers [1]. Primitively eusocial species are excellent systems to study the proximate mechanisms and ultimate causes leading to eusociality, because helpers have retained the ancestral ability to breed independently and may thus obtain both direct fitness benefits through reproduction and indirect fitness benefits by helping relatives [2-4]. Primitively eusocial halictids have a low degree of morphological differentiation between queens and helpers and a high degree of behavioural flexibility in both types of individuals [2]. As a result, females have multiple reproductive options that result in diverse types of social organisation. Many primitively eusocial species live in temperate zones, where females overwinter, found nests either alone or in association, and raise two broods per year [2]. The first brood daughters may become nonreproductive helpers that stay in their natal nest to assist their mother in raising a next brood of gynes and males. However, they may also gain direct fitness by reproducing in their natal nest, drifting to reproduce in other nests, or entering early diapause to become nest foundresses in the next spring [5-10]. In eusocial halictids, the various reproductive strategies of females are generally associated with some difference in body size [2,11,12]. Foundresses tend to be large-bodied females that have large energetic reserves enabling them to overwinter, establish nests and reproduce independently [13]. In contrast, helpers tend to be smaller-bodied daughters. For instance, across eight halictid species the proportion of helpers with undeveloped ovaries correlated with the degree of size divergence between foundresses and helpers [14]. Body size depends in part on larval diet, which has long been recognized to play an important role in caste differentiation and sociality [15]. For example, in primitively eusocial Polistinae wasps it has been proposed that the castes result from differential nourishment during larval development, with individuals experiencing relatively poor diet tending to become workers [16-18]. An interesting aspect of body size variation and diet is that that the mother might limit the amount of resources that she provides to her offspring, thus forcing them to develop into small and lean females that are incapable of independent reproduction and are thus constrained to become helpers [19-24]. Moreover, smallbodied females may be easier to manipulate into a subordinate role by dominance interactions and aggression [19,25]. In line with the hypothesis of parental manipulation, in Polistes metricus hand-fed female larvae became heavier and were more cold-resistant than those fed only by the queen [26]. Maternal control of body size is likely to be particularly effective in mass-provisioning species such as social halictids, which lay a single egg on a mass of pollen and nectar deposited in a closed cell, thus providing all the food that the offspring will need to develop into adulthood. In all annual species of eusocial sweat bees studied so far, pollen provisions of gyne-destined larvae were larger than those of worker-destined larvae [11,27]. Moreover, in one species the provisions provided to female offspring were more variable than the ones provided to male offspring [28]. Overall, in various bee species the provision quality and quantity were shown to affect adult body size, as well as the sex of the egg laid [29-32]. Together, these data indicate that mothers can control the body size of their offspring in mass-provisioning bees. It is therefore of interest to study the relationship between pollen provisions, body size and behaviour in species that have complex social systems, and where the first generation of offspring have multiple options. Body size variation also provides insights into the ecology, reproductive strategy and social behaviour of a species. If all offspring have similar fitness functions, a simple model predicts that there is a single optimal amount of resource that a parent should expend on each offspring [33]. Therefore, variations in parental expenditure and offspring body size generally reflect changes in availability of the limiting resources, in fitness expectations or in offspring role, for example switch from reproducing to helping [28,34]. Here, we study body size variation in the sweat bee Halictus scabiosae (Rossi, 1790), a ground (...truncated)