The Mechanistic, Genetic, and Evolutionary Basis of Worker Sterility in the Social Hymenoptera

Ronai, Isobel; Vergoz, Vanina; Oldroyd, Benjamin P.

doi:10.1016/bs.asb.2016.03.002

Cited by 50 publications

(42 citation statements)

References 312 publications

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“…Eusocial societies are characterized by a reproductive division of labour, in which the majority of females are workers that forego their own reproduction to assist in rearing the offspring of one or a few female kin, the queens. Among hymenopteran eusocial insects (ants, some bees and wasps), worker sterility can be absolute (workers lack functional ovaries), but typically is not; that is, workers have lost the ability to mate but remain capable of laying unfertilized haploid eggs that produce males (Ronai, Vergoz, & Oldroyd, ). Theory predicts that direct male production by workers has consequences for population genetics (Crozier, ; Crozier & Pamilo, ; Nomura & Takahashi, ; Owen, ; Owen & Owen, ).…”

Section: Introductionmentioning

confidence: 99%

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

et al. 2019

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The hallmark of eusociality is the division of labour between reproductive (queen) and nonreproductive (worker) females. Yet in many eusocial insects, workers retain the ability to produce haploid male offspring from unfertilized eggs. The reproductive potential of workers has well‐documented consequences for the structure and function of insect colonies, but its implications at the population level are less often considered. We show that worker reproduction in honey bees can have an important role in maintaining genetic diversity at the sex locus in invasive populations. The honey bee sex locus is homozygous‐lethal, and, all else being equal, a higher allele number in the population lead to higher mean brood survival. In an invasive population of the honey bee Apis cerana in Australia, workers contribute significantly to male production: 38% of male‐producing colonies are queenless, and these contribute one‐third of all males at mating congregations. Using a model, we show that such male production by queenless workers will increase the number of sex alleles retained in nascent invasive populations following founder events, relative to a scenario in which only queens reproduce. We conclude that by rescuing sex locus diversity that would otherwise be lost, workers' sons help honey bee populations to minimize the negative effects of inbreeding after founder events and so contribute to their success as invaders.

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Section: Introductionmentioning

confidence: 99%

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

et al. 2019

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“…Our results 27 suggest that the queen and the brood of primitively eusocial bees coordinate synergistically, 28 additively, and sometimes even redundantly to regulate worker behavior and reproduction, and 29 the interaction between them exists in multiple regulatory levels. 30 31 42 of species, queen's behavior and pheromonal signaling, as well as interactions between nestmate 43 workers, were found to affect worker reproduction (Ronai et al, 2016;Wenseleers et al, 2004).…”

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confidence: 99%

A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee

Orlova

Starkey

Amsalem

2019

Preprint

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8The mechanisms that maintain reproductive division of labor in social insects are still 9 incompletely understood. Most studies focus on the relationship between adults, overlooking 10 another important stakeholder in the gamethe juvenile offspring. Recent studies from various 11 social species show that not only the queen, but also the brood regulates reproductive division of 12 labor between females, but how the two coordinate to maintain reproductive monopoly remained 13 unexplored.14 Our study aims at disentangling the roles of the brood and the queen in regulating worker 15 reproduction in primitively eusocial bees. We examined the effects induced by the brood and 16 queen, separately and together, on the behavioral, physiological and brain gene expression of 17 Bombus impatiens workers. We found that young larvae induce a releaser effect in workers, 18 decreasing egg laying and aggressive behaviors, while the queen induces both releaser and primer 19 effects, modifying worker aggressive and egg laying behavior and reproductive physiology. The 20 expression of reproduction-and aggression-related genes was altered in the presence of both 21 queen and brood, but the effect was stronger or the same in the presence of the queen. 22We identified two types of interactions between the queen and the brood in regulating worker 23 reproduction: (1) synergistic interactions regulating worker physiology, where the combined 24 effect of the queen and the brood was greater than each of them separately; (2) additive 25 interactions regulating worker behavior, where the combined effects of the queen and the brood 26 are the gross sum of their separated effects. In these interactions the brood acted in a manner 27 similar to the queen but to a much smaller extent and improved the quality of the effect induced 28 by the queen. Our results suggest that the queen and the brood of primitively eusocial bees 29 coordinate synergistically, additively, and sometimes even redundantly to regulate worker 30 behavior and reproduction, and the interaction between them exists in multiple regulatory levels. 31 32

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“…From a theoretical standpoint, the functional sterility of a worker caste in this and other eusocial Hymenoptera is intriguing because it must have evolved, at least in part, through indirect selection on specific genes (Linksvayer & Wade, ; Mullen & Thompson, ). In essence, worker sterility is not a discrete trait but rather a suite of behavioral, physiological, and anatomical changes that accrue at multiple environmentally cued control points (Ronai, Vergoz, & Oldroyd, ). Therefore, the role of indirect selection can be assumed because the expression of this suite of traits is costly to a worker's direct fitness.…”

Section: Network Biology Meets Sociobiologymentioning

confidence: 99%

From gene list to gene network: Recognizing functional connections that regulate behavioral traits

et al. 2018

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The study of social breeding systems is often gene focused, and the field of insect sociobiology has been successful at assimilating tools and techniques from molecular biology. One common output from sociogenomic studies is a gene list. Gene lists are readily generated from microarray, RNA sequencing, or other molecular screens that typically aim to prioritize genes based on the differences in their expression. Gene lists, however, are often unsatisfying because the information they provide is simply tabular and does not explain how genes interact with each other, or how genetic interactions change in real time under social or environmental circumstances. Here, we promote a view that is relatively common to molecular systems biology, where gene lists are converted into gene networks that better describe the functional connections that regulate behavioral traits. We present a narrative related to honeybee worker sterility to show how network analysis can be used to reprioritize candidate genes based on connectivity rather than their freestanding expression values. Networks can also reveal multigene modules, motifs, clusters or other system‐wide properties that might not be apparent from an ab initio list. We argue that because network analyses are not restricted to “genes” as nodes, their implementation can potentially connect multiple levels of biological organization into a single, progressively complex study system.

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The Mechanistic, Genetic, and Evolutionary Basis of Worker Sterility in the Social Hymenoptera

Cited by 50 publications

References 312 publications

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population

A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee

From gene list to gene network: Recognizing functional connections that regulate behavioral traits

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