Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.
Haplodiploid organisms comprise about 20% of animals. Males develop from unfertilized eggs while females are derived from fertilized eggs. The underlying mechanisms of sex determination, however, appear to be diverse and are poorly understood. We have dissected the complementary sex determiner (csd) locus in the honeybee to understand its molecular basis. In this species, csd acts as the primary sex-determining signal with several alleles segregating in populations. Males are hemizygous and females are heterozygous at this locus; nonreproducing diploid males occur when the locus is homozygous. We have characterized csd by positional cloning and repression analysis. csd alleles are highly variable and no transcription differences were found between sexes. These results establish csd as a primary signal that governs sexual development by its allelic composition. Structural similarity of csd with tra genes of Dipteran insects suggests some functional relation of what would otherwise appear to be unrelated sex-determination mechanisms.
The colony-level phenotype of an insect society emerges from interactions between large numbers of individuals that may differ considerably in their morphology, physiology, and behavior. The proximate and ultimate mechanisms that allow this complex integrated system to form are not fully known, and understanding the evolution of social life strategies is a major topic in systems biology. In solitary insects, behavior, sensory tuning, and reproductive physiology are linked. These associations are controlled in part by pleiotropic networks that organize the sequential expression of phases in the reproductive cycle. Here we explore whether similar associations give rise to different behavioral phenotypes in a eusocial worker caste. We document that the pleiotropic genetic network that controls foraging behavior in functionally sterile honey bee workers (Apis mellifera) has a reproductive component. Associations between behavior, physiology, and sensory tuning in workers with different foraging strategies indicate that the underlying genetic architectures were designed to control a reproductive cycle. Genetic circuits that make up the regulatory ''ground plan'' of a reproductive strategy may provide powerful building blocks for social life. We suggest that exploitation of this ground plan plays a fundamental role in the evolution of social insect societies.
A fundamental goal of sociobiology is to explain how complex social behaviour evolves 1 , especially in social insects, the exemplars of social living. Although still the subject of much controversy 2 , 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 3,4 . A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes 5 to result in sib-care, the hallmark of highly evolved social life in insects 6 . A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies 3,4,7,8 . 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 socialinsect behavioural syndrome 1,5,7,9 , and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.Worker honey bees change the tasks that they perform with age 10 . This behaviour results in a division of labour that is age-associated 11 . Workers usually make a transition from working in the nest to foraging in their second or third week of life 12 , and foragers often specialize in collecting nectar or pollen. Recent studies have identified a suite of traits that differ between nectar and pollen foragers 9 . These traits are affected by a pleiotropic genetic network 13 , and it has been suggested that this pleiotropy can be explained if a reproductive regulatory network was co-opted by natural selection to differentiate the foraging behaviour of the facultatively sterile workers 7 . This hypothesis emerged from studies of honey bees that were selected to collect and store high (the high-hoarding strain) or low (the low-hoarding strain) amounts of pollen 14 . Traits of the strains diverge, so that high pollen-hoarding bees switch from nest tasks to foraging earlier in life, and are more likely to collect pollen and carry larger pollen loads. Bees from the high pollen-hoarding strain are more likely than bees from the low pollenhoarding strain to collect water and nectar with low sugar concentration, and at emergence they have higher haemolymph (blood) levels of juvenile hormone and vitellogenin protein 7 . Pollen foraging is a maternal reproductive behaviour in solitary bees, and non-reproductive females feed mainly on nectar 15 . Elevated juvenile hormone levels cause physiological and behavioural changes during the reproductive maturation of many insects 7,16,17 , and
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